Comparison of DC-plasma, DC-pulse plasma, PECVD, and RF-DC plasma nitriding processes.
\\n\\n
Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\\n\\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'IntechOpen is proud to announce that 179 of our authors have made the Clarivate™ Highly Cited Researchers List for 2020, ranking them among the top 1% most-cited.
\n\nThroughout the years, the list has named a total of 252 IntechOpen authors as Highly Cited. Of those researchers, 69 have been featured on the list multiple times.
\n\n\n\nReleased this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\n\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
\n'}],latestNews:[{slug:"stanford-university-identifies-top-2-scientists-over-1-000-are-intechopen-authors-and-editors-20210122",title:"Stanford University Identifies Top 2% Scientists, Over 1,000 are IntechOpen Authors and Editors"},{slug:"intechopen-authors-included-in-the-highly-cited-researchers-list-for-2020-20210121",title:"IntechOpen Authors Included in the Highly Cited Researchers List for 2020"},{slug:"intechopen-maintains-position-as-the-world-s-largest-oa-book-publisher-20201218",title:"IntechOpen Maintains Position as the World’s Largest OA Book Publisher"},{slug:"all-intechopen-books-available-on-perlego-20201215",title:"All IntechOpen Books Available on Perlego"},{slug:"oiv-awards-recognizes-intechopen-s-editors-20201127",title:"OIV Awards Recognizes IntechOpen's Editors"},{slug:"intechopen-joins-crossref-s-initiative-for-open-abstracts-i4oa-to-boost-the-discovery-of-research-20201005",title:"IntechOpen joins Crossref's Initiative for Open Abstracts (I4OA) to Boost the Discovery of Research"},{slug:"intechopen-hits-milestone-5-000-open-access-books-published-20200908",title:"IntechOpen hits milestone: 5,000 Open Access books published!"},{slug:"intechopen-books-hosted-on-the-mathworks-book-program-20200819",title:"IntechOpen Books Hosted on the MathWorks Book Program"}]},book:{item:{type:"book",id:"346",leadTitle:null,fullTitle:"DNA Repair - On the Pathways to Fixing DNA Damage and Errors",title:"DNA Repair",subtitle:"On the Pathways to Fixing DNA Damage and Errors",reviewType:"peer-reviewed",abstract:"DNA repair is fundamental to all cell types to maintain genomic stability. A collection of cutting-edge reviews, DNA Repair - On the pathways to fixing DNA damage and errors covers major aspects of the DNA repair processes in a large variety of organisms, emphasizing foremost developments, questions to be solved and new directions in this rapidly evolving area of modern biology. Written by researchers at the vanguard of the DNA repair field, the chapters highlight the importance of the DNA repair mechanisms and their linkage to DNA replication, cell-cycle progression and DNA recombination. Major topics include: base excision repair, nucleotide excision repair, mismatch repair, double-strand break repair, with focus on specific inhibitors and key players of DNA repair such as nucleases, ubiquitin-proteasome enzymes, poly ADP-ribose polymerase and factors relevant for DNA repair in mitochondria and embryonic stem cells.\nThis book is a journey into the cosmos of DNA repair and its frontiers.",isbn:null,printIsbn:"978-953-307-649-2",pdfIsbn:"978-953-51-5160-9",doi:"10.5772/871",price:139,priceEur:155,priceUsd:179,slug:"dna-repair-on-the-pathways-to-fixing-dna-damage-and-errors",numberOfPages:394,isOpenForSubmission:!1,isInWos:1,hash:"962f1357bb182c3d5e01b7cac964f529",bookSignature:"Francesca Storici",publishedDate:"September 9th 2011",coverURL:"https://cdn.intechopen.com/books/images_new/346.jpg",numberOfDownloads:43861,numberOfWosCitations:45,numberOfCrossrefCitations:11,numberOfDimensionsCitations:42,hasAltmetrics:0,numberOfTotalCitations:98,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"November 10th 2010",dateEndSecondStepPublish:"December 8th 2010",dateEndThirdStepPublish:"April 14th 2011",dateEndFourthStepPublish:"May 14th 2011",dateEndFifthStepPublish:"July 13th 2011",currentStepOfPublishingProcess:5,indexedIn:"1,2,3,4,5,6",editedByType:"Edited by",kuFlag:!1,editors:[{id:"40385",title:"Dr.",name:"Francesca",middleName:null,surname:"Storici",slug:"francesca-storici",fullName:"Francesca Storici",profilePictureURL:"https://mts.intechopen.com/storage/users/40385/images/1777_n.jpg",biography:"Francesca Storici was born in Triestre (Italy) in 1968. She received a Biology degree in 1993 from the University of Trieste and a Ph.D. in Molecular Genetics from the International School of Advanced Studies (ISAS), working at the International Center for Genetic Engineering and Biotechnology of Trieste in 1998. From 1999 to 2007, she was a Visiting and then a Research Fellow at the National Institute of Environmental and Health Sciences (NIEHS, NIH) in North Carolina (USA). In 2007, she was a Research Assistant Professor at the Gene Therapy Center of the University of North Carolina at Chapel Hill. In August 2007 she joined the faculty at the School of Biology of the Georgia Institute of Technology in Atlanta, Georgia as Assistant Professor and soon after she received the title of Distinguished Cancer Scholar from the Georgia Cancer Coalition. Her research is on genome stability, DNA repair and gene targeting.",institutionString:null,position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"0",totalChapterViews:"0",totalEditedBooks:"1",institution:null}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"400",title:"Molecular Genetics",slug:"human-genetics-molecular-genetics"}],chapters:[{id:"19294",title:"Lagging Strand Synthesis and Genomic Stability",doi:"10.5772/22007",slug:"lagging-strand-synthesis-and-genomic-stability",totalDownloads:2603,totalCrossrefCites:0,totalDimensionsCites:1,signatures:"Tuan Anh Nguyen, Chul-Hwan Lee and Yeon-Soo Seo",downloadPdfUrl:"/chapter/pdf-download/19294",previewPdfUrl:"/chapter/pdf-preview/19294",authors:[{id:"45828",title:"Dr.",name:"Yeon-Soo",surname:"Seo",slug:"yeon-soo-seo",fullName:"Yeon-Soo Seo"},{id:"46800",title:"Ph.D.",name:"Tuan Anh",surname:"Nguyen",slug:"tuan-anh-nguyen",fullName:"Tuan Anh Nguyen"},{id:"57602",title:"Dr.",name:"Chul-Hwan",surname:"Lee",slug:"chul-hwan-lee",fullName:"Chul-Hwan Lee"}],corrections:null},{id:"19295",title:"Synergy Between DNA Replication and Repair Mechanisms",doi:"10.5772/24164",slug:"synergy-between-dna-replication-and-repair-mechanisms",totalDownloads:2512,totalCrossrefCites:0,totalDimensionsCites:0,signatures:"Maria Zannis-Hadjopoulos and Emmanouil Rampakakis",downloadPdfUrl:"/chapter/pdf-download/19295",previewPdfUrl:"/chapter/pdf-preview/19295",authors:[{id:"55850",title:"Dr.",name:"Maria",surname:"Zannis-Hadjopoulos",slug:"maria-zannis-hadjopoulos",fullName:"Maria Zannis-Hadjopoulos"},{id:"58439",title:"Dr.",name:"Emmanouil",surname:"Rampakakis",slug:"emmanouil-rampakakis",fullName:"Emmanouil Rampakakis"}],corrections:null},{id:"19296",title:"New Insight on Entangled DNA Repair Pathways: Stable Silenced Human Cells for Unraveling the DDR Jigsaw",doi:"10.5772/23681",slug:"new-insight-on-entangled-dna-repair-pathways-stable-silenced-human-cells-for-unraveling-the-ddr-jigs",totalDownloads:2059,totalCrossrefCites:0,totalDimensionsCites:0,signatures:"Biard Denis S.F.",downloadPdfUrl:"/chapter/pdf-download/19296",previewPdfUrl:"/chapter/pdf-preview/19296",authors:[{id:"53173",title:"Dr.",name:"Denis S.F.",surname:"Biard",slug:"denis-s.f.-biard",fullName:"Denis S.F. 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\r\n\tThis book will discuss the mechanisms by which TTM can mitigate the pathophysiologies responsible for secondary brain injury, as well as the available evidence for use of TTM in multiple neurologic injuries (stated above). In addition, this review will also provide information to help guide this treatment with regard to timing, depth, duration, and management of side-effects. It will also address normothermia and fever prevention in brain injury.
\r\n\tThe book will also discuss the pathophysiology and therapeutic approach to shivering during TTM. It will also provide grounds for future directions in the application of and research with TTM.
Iron-nitrogen or Fe-N binary system is essential in the steel design in a similar manner to the iron-carbon system [1]. Since the maximum solubility limit of nitrogen solutes is only 0.1 mass% or 0.3 at%, most of the previous studies concentrated on the solubility of nitrogen into γ-phase at a higher temperature than 1000 K [2]. Under those research circumstances, three important items in the material science were pointed out as findings to be noticed. Nitrogen works as a γ-phase stabilizer so that phase transformation temperature from α/α′- to γ-phase decreases with increasing the nitrogen content, [N] [3]. Mechanical properties significantly improve by themselves also with increasing [N] [4]. Thirdly, a crystalline structure of nitrogen super-saturated iron or Fe (N) resembles with that of iron nitride; for example, α′-Fe (N) with the nitrogen content of 11 at% has the same crystalline structure of α″-Fe16N2 and γ-Fe (N) with 20 at% nitrogen solute content corresponds to γ′-Fe4N as surveyed in the textbook [5]. The first two items stimulated further researches for high-nitrogen steels (HNS) as discussed in [6]. The third item leads to the chemical vapor deposition of Fe16N2 thin films on the template substrate [7].
An pressurized electro-slag remelting (ESR) method has become a standard approach to fabricate an ingot of HNS [8]. Relatively high amount of dissociated nitrogen atoms from N2 gas can diffuse into the depth of γ-phase matrix at 1263 K. This solution nitriding method induced the nitrogen atoms even into high chromium content steels including austenitic stainless steels [9]. Through this process, the nickel resource can be saved by 69 kg only by the addition of nitrogen atoms by 1 kg. The nitrogen works to stabilize the austenitic phase even with less nickel content. These nickel-free HNS have coarse grains, resulting in embrittlement, difficulty in welding, and insufficient stability in working. Although many trials have been made to improve the nitrogen solute content higher than 1 mass%, most of the studies experienced engineering difficulties to find a new alloying effect on the increase of strength and corrosion resistance [10].
In parallel with research on HNS, ion- and radical nitriding processes were developed with the use of the direct current (DC)-plasma and DC-pulse plasma technologies [11]. The TH was held to be higher than 900 K in them; CrN was synthesized as a precipitate in the matrix together with iron nitrides such as Fe2N and γ′-Fe4N [12]. Hence, the stainless steels and Fe-Cr alloys were hardened by fine precipitation of CrN; however, the chromium content in the matrix was reduced by CrN-precipitation reaction to lower the original corrosion resistance [13]. In addition, this high temperature plasma nitriding was mainly governed by the nitrogen diffusion process; the nitrogen solute content exponentially decreases from the maximum nitrogen solid solubility of 0.1 mass% at the surface down to 0 toward the nitriding front-end [14]. Furthermore, when the TH was higher than 1000 K, the chromium also diffuses to form a multi-stripe pattern with layered structure of {- (Cr-rich) - (CrN-rich) -} during nitriding [15]. Most of engineers and companies related to plasma nitriding believe that chemical reaction of chromium with nitrogen should drive the nitrided layer formation and hardening.
British research group [16] first found the nitrogen super-saturated lattices in the austenitic stainless steels by low temperature plasma nitriding. When using the same DC or DC-pulse plasmas, the nitriding process is characterized mainly by CrN precipitation into matrix when TH is higher than 800 K. On the other hand, an original γ-lattice expands to form a peak shift from the original peaks of austenitic stainless steels in X-ray diffraction (XRD) analysis when TH < 800 K. This finding does not mean a formation of new phase, so called by S-phase, but implies that nitrogen super-saturation accompanies with the γ-lattice expansion and that the crystalline structure of this Fe (N) is essentially different from that of original austenitic stainless steel matrix. In addition, various new engineering is expected to start from this nitrogen super-saturated Fe (N) [17].
In the present chapter, this low temperature nitriding (LTN) with nitrogen super-saturation is reconsidered by developing a new tool to drive LTN in the AISI304 stainless steels. First, Radio-frequency(RF)-DC plasma nitriding system is introduced with comments on the essential difference from other plasma nitriding processes such as DC- and DC-pulse plasmas. Quantitative plasma diagnosis equipment is stated to describe the nitrogen-hydrogen plasmas. In particular, the effect of hydrogen content in the mixture gas on the nitriding process is analyzed to determine the optimum condition. A hollow cathode device is proposed to intensify the ion and electron densities.
An austenitic stainless steel type AISI304 specimen is employed for plasma nitriding at 673 K for 14.4 ks by 60 Pa. Each fundamental process in this low temperature inner nitriding is analyzed by XRD, scanning electron microscopy (SEM)-electron dispersive X-ray spectroscopy (EDX), and electron back-scattering diffraction (EBSD). The γ-lattice expansion is analyzed as a peak shift in the XRD diagram. The nitrogen super-saturation is described by SEM-EDX; the elastic distortion is directly calculated by the lattice strain. The phase transformation, the plastic straining as well as the microstructure refinement are analyzed by EBSD. The nitrogen diffusion path is mainly estimated by the grain boundary diffusion process. These processes are mutually related to form a synergetic loop to drive this low temperature inner nitriding. When this loop is sustained during nitriding, the nitriding front-end advances homogeneously into the depth of stainless steel matrix. Once this loop is shut down at any point, the inner nitriding localizes by itself only to form a heterogeneous microstructure.
High-density RF-DC plasma nitriding system is introduced together with comments on the quantitative plasma diagnosis of nitrogen-hydrogen plasmas and on the hollow cathode device to intensify the ion and electron densities.
DC-plasma and DC-pulse plasma [18, 19, 20] have been utilized for nitriding of stainless steel parts, tools and dies at higher hold temperature than 800 K. plasma enhanced chemical vapor deposition (PECVD) has been utilized for nitriding at lower temperature than 800 K. Table 1 compares the difference in their capacity, inner nitriding behavior, and characteristics together with the present high-density RF-DC plasma nitriding. The former two approaches, widely utilized in the market, harden the stainless steels by CrN-precipitation and form thicker nitrided layer than 100 μm after 36 ks or 10 hours. PECVD nitriding works in the low-pressure of 1 to 2 Pa to form a moderate nitrided layer with the thickness of 20–30 μm. Inner nitriding process both in PECVD [21] and RF-DC plasma [22] is governed by nitrogen super-saturation without CrN precipitation. In the following, a detail of RF-DC plasma generation as well as a hollow cathode device is stated together with plasma diagnosis equipment in the present system.
Comparison of DC-plasma, DC-pulse plasma, PECVD, and RF-DC plasma nitriding processes.
A high-density plasma nitriding system [23, 24, 25] consisted of the vacuum chamber, the evacuation system, the DC-RF generators working in the frequency of 2 MHz, the gas supply of N2 and H2, and the heating unit located under the cathode plate as depicted in Figure 1. The nitriding parameters as well as controlling procedure are specified on the panels. All through the nitriding process, the measured pressure, temperature as well as gas pressure is automatically controlled by the process computer. Through the telecommunication, time history of RF- and DC-voltages and currents are also monitored on the panel to recognize the temporal status of RF-DC plasmas.
RF-DC plasma nitriding system. (1) Vacuum chamber, (2) RF-generator, (3) control-panel, (4) RF- and DC-power suppliers, (5) evacuation units, and (6) carrier gas supply.
Figure 2 illustrates an actual experimental setup for plasma nitriding. The thermocouple is inserted into this cathode plate to monitor the TH. In the vacuum chamber, the specimen is placed inside a hollow cathode setup on the cathode plate, which is electrically connected with DC generator. This hollow cathode setup includes a rectangle-shaped tube with the size of 40 × 20 × 70 mm3 and the thickness of 2 mm. To be explained later, the specimen is located at the position with the highest nitrogen ion density, far half from the mixture gas inlet, as shown in Figure 2.
Experimental setup for RF-DC high-density plasma nitriding.
In the standard plasma diagnosis, two methods are often employed to quantitatively describe the nitrogen-hydrogen mixture plasma state; that is, emissive light optical spectroscopy (EOS) and Langmuir probe (LP). A typical setup for EOS is illustrated in Figure 3 as precisely stated in the previous studies [26, 27, 28].
EOS for plasma diagnosis to describe the active species in the ignited plasmas.
Emissive light from plasmas is detected through the optically transparent silica window on the chamber in Figure 1 and analyzed to deduce the spectrum of species in the plasmas. Figure 4 shows the effect of hydrogen content in the gas mixture on the measured spectra together with the spectra for hydrogen plasmas.
Measured spectra for the hydrogen-nitrogen plasmas by EOS.
As seen in the spectra for hydrogen plasmas inserted in Figure 4, hydrogen peak intensity (Hα) at 656 nm increases monotonically with hydrogen content [H]. Pure nitrogen plasma mainly consists of an excited nitrogen molecule (N2*) and a nitrogen molecule ion (N2+) besides for a nitrogen molecule. When [H] = 83%, the whole population of nitrogen species including the NH-radicals significantly decreases. On the other hand, when [H] = 17%, {N2*, N2+, and NH} have high-intensity without peaks for the molecular nitrogen in the range of short wavelength (<300 nm). Although the active species such as N2(A3 ∑u+, ϑ) or N2(X1 ∑g+, ϑ) cannot be observed directly from the EOS spectra, their transitions can be investigated to describe the reaction model on the active species; for example, N2(C3 ∏u → B3 ∏ g*) peaks observed at 337, 358, and 370 nm are related to the N2* and N2+(B2 ∑u+ → X2 ∑g+) at 391 and 427 nm, related to the N2+. These second positive and the first negative bands of nitrogen play an important role in the generation of atomic nitrogen by reaction with N2 and N2+ in parallel with the formation of NH-radicals as detected at 336 nm.
The LP was also utilized in the diagnosis to describe the effect of [H] on the generated plasmas. Figure 5 depicts how to measure the ion and electron densities by using LP.
Experimental setups of the LP for measurement of ion and electron densities.
Through the direct measurement of I-V curves at the probe tip, the electron resistivity as well as the ion and electron densities are analyzed to describe the plasma state. In particular, the electron resistivity is proportional to the enhancement of plasma chemical reaction. Figure 6shows a variation of measured resistivity in the plasmas with increasing the hydrogen content in the mixture gas.
Variation of the measured resistivity in the plasmas with increasing the hydrogen content in the mixture gas.
The measured resistivity has maximum around [H] = 20–30%; a hot spot is formed in the plasmas where the chemical reaction is most enhanced for nitriding by directly controlling the hydrogen content [29].
The hollow cathode device is utilized to intensify the ion density in the nitrogen-hydrogen plasmas. The LP is employed to directly measure the ion density in the hollow. The LP-tip was inserted into the hollow along the X-axis in every 2 cm. In each position, the tip was fixed at the center of hollow. Figure 7 depicts the measured ion density distribution along the X-axis.
Measured ion density by the LP along the X-axis in the hollow.
The ion density increases monotonically with X in Figure 7; in particular, a hot spot with higher ion density than 1.5 × 1018 m−3 is located in the latter half of hollow. This is common to the hollow device effect where the ionization is enhanced at the vicinity of outlet in the hollow [30].
XRD (Rigaku SmartLab) with monochromatic Cu-Kα radiation (λ = 0.1542 nm) and Bragg–Brentano geometry, 40 kV, and 30 mA was utilized for analysis. The 2θ range was set between 30 and 90° with the scanning speed of 10 mm/min and the step angle of 0.02°. EDX device and software were utilized to make element mapping over a specified depth for nitrogen, chromium, iron, and carbon. Its spatial resolution was at most 5 μm. EBSD was utilized with the accelerating voltage of 20 kV, the working distance of 20 mm, the magnification (×2000), and the resolution of 0.1 μm. The inverse pole figure (IPF) was determined for each constituent grain to describe the change in microstructure through the nitriding. In addition, the kernel average misorientation (KAM) and the phase mapping were also measured to explain the plastic straining and phase transformation processes, respectively.
The micro-hardness testing apparatus (Mitsutoyo HM-200) was used by applying the load of 50 g or 0.5 N for hardness measurement on the cross-section in every 10 μm. The matrix hardness of AISI304 was 400 HV.
An austenitic stainless steel type AISI304 was employed as a specimen for high-density plasma nitriding at 673 K for 14.4 ks by 60 Pa with use of the hollow cathode device. Essential processes in this low temperature plasma nitriding are described by chemical analyses.
An austenitic stainless steel type AISI304 was selected for plasma nitriding at lower TH than 723 K. Table 2 summarizes the experimental results in the literature.
Previous studies on the low temperature plasma nitriding of AISI304 stainless steels.
Although detail information is not written in a few papers, relatively high-nitrogen surface content and formation of a nitrided layer with the thickness of 10–20 μm are common to those previous studies [31, 32, 33, 34, 35]. More precise analysis and discussion are needed to investigate the essential processes, governing the inner nitriding behavior at a lower temperature than 700 K. High-density RF-DC plasma systems [36, 37, 38, 39, 40] provides a new way to further analyze this low temperature plasma nitriding by experiments.
In the present study, AISI304 stainless steel plate with the size of 40 × 20 × 2 mm3 was employed as a specimen for RF-DC high-density plasma nitriding at 673 K for 14.4 ks by 60 Pa for the nitrogen and hydrogen mixture gas with the flow rate ratio of 160–30 ml/min. The pre-sputtering only with the use of nitrogen gas was first performed for 1.8 ks to clean the surface condition of the specimen before nitriding. Table 3 lists the whole plasma nitriding condition in this experiment.
RF-DC high-density plasma nitriding conditions.
The nitrided specimen was halved to prepare the test-pieces for SEM-EDX analyses. Figure 8 depicts the cross-sectional SEM image as well as the nitrogen mapping from the surface to the depth of nitrided specimen. The nitrogen content is measured at the surface to be 9 mass% or 26 at%. The nitrided layer thickness reaches to be 66.5 μm.
Cross-section of the plasma nitrided at 673 K for 14.4 ks. (a) SEM cross-sectional image and (b) nitrogen mapping from the surface to the depth.
Compared with Table 2, both the nitrogen solute content at the surface and the nitrided layer thickness become the highest by using this plasma nitriding at 673 K for 14.4 ks. Formation of uniform nitrogen super-saturated layer reveals that inner nitriding advances homogeneously into the depth of matrix.
A nitrogen super-saturated lattice is expected to expand by itself; for example, the previous studies in Table 2 reported a γ-lattice expansion by this nitrogen super-saturation. Figure 9 compares the analyzed XRD diagrams before and after the plasma nitriding. The original austenitic phase is characterized by three peaks for γ (111), γ (200), and γ (220) detected at 2θ = 43.4, 50.82, and 74.5°, respectively.
Comparison of analyzed XRD diagrams before and after plasma nitriding at 673 K.
Through the plasma nitriding process, all the austenitic lattices were elastically distorted to the expanded austenite (γN); for example, the original γ-peaks to AISI304 shifted to the lower 2θ, from 43.4 to 41.1°, from 50.82 to 47.94°, and from 74.5 to 70.08°, respectively. In parallel with these γN phases, the expanded martensitic peaks are also detected at 2θ = 43.7–63.5°. Negligibly small peak was detected at 2θ = 37.5° in trace level, which corresponds to the chromium nitrides. The γ-lattice expansion by this shift in XRD induces the tensile lattice strain by 5.4% for the peak shift from γ (111) to γN (111). This strain slightly increases to be 5.6% for the shift of γ (200) to γN (200) and 5.4% for γ (220) to γN (220), respectively. This elastic distortion in the nitrogen super-saturated lattices just corresponds to the previous report in [41]. The grains housing these elastically distorted lattices are forced to deform plastically to compensate for strain incompatibility between the nitrogen unsaturated and the super-saturated lattices in grains.
EDX as well as the micro-Vickers testing are utilized to investigate the nitrogen content and hardness depth profiles. As depicted in Figure 10, the hardness becomes maximum at the surface by 1550 HV and gradually reduces down to 1300 HV in the depth of d < 40 μm. From d = 40–66.5 μm, this hardness gradually decreases to the matrix hardness of 400 HV. A nitriding front-end is defined by the position in depth where the measured hardness coincides with the substrate hardness; the nitrided layer thickness (E) after nitriding for 14.4 ks is 66.5 μm. The nitrogen content is kept constant to be 15–17 at% in the depth of 5 < d < 60 μm except for the vicinities of surface and nitriding front-end. In the high temperature nitriding, the nitrogen content exponentially decays from the maximum nitrogen solubility limit of 0.1 mass% at the surface and goes to zero at the nitriding front-end. The nitrogen solute content depth profile in Figure 10 is far from the common knowledge on the inner nitriding process in the high temperature nitriding.
Nitrogen content and hardness depth profiles from the surface to the depth.
EBSD provides a tool to describe the interrelation among the phase transformation, the plastic straining, and the microstructure evolution. The measured phase mapping and KAM distribution on the cross-section of the nitrided specimen are shown in Figure 11a and b, respectively. After [42], the measured cross-sectional KAM profile can be identified as an equivalent plastic strain distribution.
EBSD analysis on the cross-section of the nitrided AISI304 specimen at 673 K for 14.4 ks. (a) KAM distribution, (b) phase mapping, and (c) IPF depth profile.
In Figure 11a, the expanded γ-phase and transformed α′-phase finely distribute in the depth of d < 40 μm and form the two-phase microstructure. This homogeneous two-phase structure abruptly changes to a heterogeneous one where α′-phase sparsely distributes in the γ-phase matrix. This autonomous phase mapping change coincides with the onset of hardness reduction in Figure 10. This is because the volume fraction of extended γ-phase and transformed α′-phase zones begins to reduce from d = 40 μm in Figure 11a.
In Figure 11b, the layer of d < 40 μm is plastically strained in all since most of grains house the expanded lattice zones and plastically distort to compensate for the strain incompatibility in each grain. Just as seen in Figure 11a, this homogeneous plastic straining also changes by itself and localizes to specified grains. In fact, plastic strains localize in each grain below d = 40 μm. That is, uniform phase transformation and plastic straining change themselves across this critical depth by their localization to grains. The neighboring lattices to elastically distorted ones by phase transformation are forced to make plastic distortion. The transformed α′-phase zones in Figure 11a correspond to the highly strained zones in Figure 11b.
Phase transformation and plastic straining in the above reflects the microstructure change by the nitrogen super-saturation. Figure 11c depicts the IPF distribution on the cross-section of the nitrided specimen. Each grain with a specified crystallographic orientation is represented by a different color. In correspondence to Figure 11a and b, the layer of d < 40 mm has refined microstructure with the average grains size of 0.1 μm, just near the spatial resolution of EBSD. This gray color for this layer in Figure 11c implies that each grain in this layer is homogeneously refined to have random crystallographic orientation. Just as observed in Figure 11a and b, this homogeneous microstructure changes by itself to heterogeneous one at d = 40 μm; the average grain size comes near to the original grain size before nitriding. To be noticed, the crystallographic orientations with different colors from original one or with graded colors are seen in most of the grains below d = 40 μm. The plastically strained grains are partially decomposed into several or tens of subgrains with different crystallographic orientations.
LTN of austenitic stainless steels is essentially different from the conventional plasma nitriding at higher temperatures. No nitrides are formed in the matrix so that no change in the original chromium content proves less change in the original corrosion resistance of stainless steels. The surface layer is hardened by nitrogen solid-solution where the γ-phase is expanded by nitrogen super-saturation with the occupation of octahedral vacancy sites by nitrogen solutes. Owing to fine grain size in the homogeneously nitrided layer, higher strength is expected to this high-nitrogen stainless steel surface. In addition, the fine-grained two-phase structure has a role to improve the trade-off-balancing between strength and fracture toughness and to increase the fatigue life [2]. How to extend this homogeneously nitrided layer toward the nitriding front-end must be an engineering issue to be discussed further.
Inner nitriding mechanism in this low temperature plasma nitriding of austenitic stainless steels is discussed with importance on the difference between the homogeneous and heterogeneous nitriding processes.
LTN mechanism is described by a synergetic loop as explained by Figure 12. Nitrogen solute, penetrating from the surface under high-nitrogen flux, occupies with an octahedral vacancy sites in the fcc-structured lattice as suggested by [43]. Under this nitrogen super-saturation, the γ-lattice expands, and elastically distorts to drive the γ to α′ phase transformation. The whole γ-lattices neighboring to expanding γ-lattices and transformed α′-lattices, are plastically strained to compensate for the strain incompatibility between two zones. Original grain is distorted and decomposed into fine subgrains by this plastic straining. More nitrogen solutes diffuse to the depth of unsaturated matrix through the refined grain boundaries. Evolution of the nitrided layer accompanies with this loop.
Synergetic loop of processing steps to drive the low temperature inner nitriding of stainless steels.
When this synergetic loop is sustained during the plasma nitriding, every unit process uniformly advances from the surface to the depth of matrix. As seen in Figure 11, the original coarse-grained AISI304 matrix is surface-modified to have fine-grained, two-phase microstructure from the surface to the depth of 40 μm. This homogeneous nitriding is shut down at the critical depth of 40 μm for the nitrided AISI304 at 673 K for 14.4 ks in Figure 11; the above loop only takes place locally below this critical depth. There is no change in the synergetic loop across this criticality. When the loop works uniformly in the matrix, the nitriding advances homogeneously, while it does heterogeneously when the loop localizes in the selected grains. In other words, this autonomous change from heterogeneous nitriding to homogeneous nitriding is driven by the nitrogen super-saturation process into grains. When the nitrogen super-saturated γ-phase zones are closely neighboring to each other in the specified grain, the whole related grains are homogeneously nitrided and refined by the synergetic loop in Figure 12. On the other hand, when each super-saturated γ-phase zones are isolated from each other, every process in the loop works only inside of each grain.
Let us first describe the localization of phase transformation, plastic straining, and micro-refinement below the critical depth in Figure 11. The phase mapping, the plastic strain distribution as well as the IPF mapping for the grain-A at d = 100 μm in Figure 11 are analyzed and shown in Figure 13. Since a grain boundary works as a nitrogen diffusion path, most of the γ-phase zones at its vicinity transform to α′-phase. As pointed by an arrow-a in Figure 13a and b, a series of α′-phase zones are aligned in the alternate order of {- (α′-phase zone) − (highly plastic-strained zone) − (α’-phase) -}. In correspondence to this alignment, an original (001) orientation rotates by the plastic straining as shown in the graded colors in Figure 11c. The transformed zones have (111) orientation as pointed by arrow-b. This local change in phase mapping, plastic straining, and crystallographic orientation distribution in the inside of grain-A proves that the heterogeneous nitriding process is driven by this localization in each grain of matrix below the critical depth.
Localized steps around the grain-a in the heterogeneous nitriding process. (a) Local phase mapping, (b) local plastic straining, and (c) local IPF mapping.
Figure 13 also suggests that each transformed band, pointed by the arrow-a, has a unit size of 0.3–0.5 μm in common and that these bands are isolated by highly strained γ-phase zones. With the enhancement of the nitrogen flux from the surface or with an increase of the nitrogen diffusion path density, those isolated zones overlap with each other to change the heterogeneous nitriding to the homogeneous nitriding. In other words, homogeneous nitriding mode prevails in the low temperature plasma nitriding process with higher activation of nitrogen flux from plasmas or with reduction of the initial grain size to a comparable level of transformed units in Figure 13.
An initial grain size of AISI304 sheet is controlled to decrease by intense rolling with the reduction in thickness by 90 % to demonstrate this mode change from heterogeneous nitriding to homogeneous nitriding. Figure 14 depicts the phase mapping, the plastic straining, and the microstructure refinement on the cross-section of rolled AISI304 before nitriding. Although crystallographic textures are formed along the rolling direction as shown by the arrow-a in Figure 14, the average grain size is uniformly reduced down to 1.5 μm.
Microstructure of intensely rolled AISI304 sheet with the reduction of thickness by 90%. Average grain size is 1.5 μm.
Under the same processing conditions, this fine-grained AISI304 specimen is nitrided at 673 K for 14.4 ks. The nitriding front-end is analyzed to be E = 60 μm, nearly the same as shown in Figure 11. Figure 15 shows the phase mapping, the plastic strain distribution, and the microstructure after nitriding. The heterogeneous microstructure observed above the nitriding front-end as well as the textures by rolling in Figure 14, completely disappears to form two-phase and fine-grained homogeneous nitrided layer. Although the initial fully martensitic phase turns to be γ – α’ two-phase; this two-phase fine microstructure is continuously formed across the nitriding front-end. This homogenization of the heterogeneous microstructure reveals that nitrogen super-saturation process advances homogeneously into the depth of stainless steel matrix under the synergetic loop once the grain size of the matrix is comparable to the nitrogen super-saturated unit size.
Microstructure after nitriding the fine-grained AISI304 at 673 K for 14.4 ks.
LTN of stainless steels is essentially governed by the homogeneous nitrogen super-saturation. When the synergetic loop is sustained during the nitriding, the nitrided layer has two-phase, fine-grained microstructure. Once the nitrogen super-saturation process is localized into the specified grains, the homogeneous nitriding changes itself to heterogeneous nitriding. Refinement of the initial grain size into a comparable size of nitrogen saturated γ-lattice units homogenizes the heterogeneously nitrided layer.
Low temperature plasma nitriding provides a processing tool for the surface treatment of the stainless steels to have a fine two-phase microstructure with the average grain size of 0.1 μm. This homogeneously nitrided layer has higher surface hardness than 1500 HV and higher nitrogen content than 15 at%. Different from the conventional nitriding, (1) no nitrides are formed as a precipitate in the matrix, (2) stainless steel matrix is nitrogen super-saturated to have a nitrogen content plateau of 15–17 at% toward the nitriding front-end, (3) phase transformation and plastic straining take place together with γ-lattice expansion, and (4) original coarse grains are refined. This homogeneous nitriding follows the heterogeneous nitriding process where γ-lattice expands locally in the specified grains with phase transformation to α′-phase and plastic straining. When nitriding the fine-grained stainless steels, their surfaces are homogeneously nitrided to have fine, a two-phase microstructure with high hardness, strength, and corrosion resistance.
The author would like to express his gratitude to Mr. Abdelrahman Farghali (SIT) and late Mr. Y. Sugita (YS-Electric Industry, Co. Ltd.) for their help in experiments. This study was financially supported in part by the Abe-Initiative in Japan Government and the METI-program on the supporting industries, Japan, respectively.
No conflicts of interest were declared.
Extremophile organisms capable of growing in extreme conditions draw considerable attention since they show that life is robust and adaptable and help us understand its limits. In addition, they show a high biotechnological potential [1, 2]. Most of the best-characterized extreme environments on Earth are geophysical constraints (temperature, pressure, ionic strength, radiation, etc.) in which opportunistic microorganisms have developed various adaptation strategies. Deep-sea environments, hot springs and geysers, extreme acid waters, hypersaline environments, deserts, and permafrost or ice are some or the most recurrent examples of extreme environments [3]. However, the atmosphere is rarely thought of as an extreme habitat. In the atmosphere, the dynamics of chemical and biological interactions are very complex, and the organisms that survive in this environment must tolerate high levels of UV radiation, desiccation (wind drying), temperature (extremely low and high temperatures), and atmospheric chemistry (humidity, oxygen radicals, etc.) [4]. These factors turn the atmosphere (especially its higher layers) into one of the most extreme environments described to date and the airborne microorganisms into extremophiles or, at least, multiresistant ones [5].
\nIt is known that airborne cells can maintain viability during their atmospheric residence and can exist in the air as spores or as vegetative cells thanks to diverse molecular mechanisms of resistance and adaptation [2, 6]. The big question is whether some of them can be metabolically active and divide. Bacterial residence times can be several days, which facilitate transport over long distances. This fact, together with the extreme conditions of the atmosphere, has led researchers to think for years that they do not remain active during their dispersion. However, recent studies strongly suggest that atmospheric microbes are metabolically active and were aerosolized organic matter and water in clouds would provide the right environment for metabolic activity to take place. Thus, the role played by microorganisms in the air would not only be passive but could also influence the chemistry of the atmosphere. In any case, only a certain fraction of bacteria in the atmosphere would be metabolically active [2, 7].
\nDespite recognizing its ecological importance, the diversity of airborne microorganisms remains largely unknown as well as the factors influencing diversity levels. Recent studies on airborne microbial biodiversity have reported a diverse assemblage of bacteria and fungi [4, 8, 9, 10, 11, 12], including taxa also commonly found on leaf surfaces [13, 14] and in soil habitats [15]. The abundance and composition of airborne microbial communities are variable across time and space [11, 16, 17, 18, 19]. However, the atmospheric conditions responsible for driving the observed changes in microbial abundances have not been thoroughly established. One reason for these limitations in the knowledge of aerobiology is that until recently, microbiological methods based on culture have been the standard, and it is known that such methods capture only a small portion of the total microbial diversity [20]. In addition, because pure cultures of microorganisms contain a unique type of microbes, culture-based approaches miss the opportunity to study the interactions between different microbes and their environment.
\nAnother limitation for the study of aerial microbial ecology at higher altitudes or in open ocean areas is the difficulty of repeated and dedicated use of airborne platforms (i.e., aircraft or balloons) to sample the air. Most studies to date on the atmospheric microbiome are restricted to samples collected near the Earth’s surface (e.g., top of mountains or buildings). Aircraft, unmanned aerial systems (UASs), balloons or even rockets, and satellites could represent the future in aerobiology knowledge [5, 21, 22]. These platforms could open the door to conducting microbial studies in the stratosphere and troposphere at high altitudes and in open-air masses, where long-range atmospheric transport is more efficient, something that is still poorly characterized today. The main challenge in conducting these kinds of studies stems from the fact that microbial collection systems are not sufficiently developed. There is a need for improvement and implementation of suitable sampling systems for platforms capable of sampling large volumes of air for subsequent analyses using multiple techniques, as this would provide a wide range of applications in the atmospheric, environmental, and health sciences.
\nIn aerobiology, dust storms deserve special mention. Most of them originate in the world’s deserts and semideserts and play an integral role in the Earth system [23, 24]. They are the result of turbulent winds, including convective haboobs [25]. This dust reaches concentrations in excess of 6000 μg m−3 in severe events [26]. Dust and dust-associated bacteria, fungal spores, and pollen can be transported thousands of kilometers in the presence of dust [9].
\nIn this chapter, we approach the atmosphere as an extreme environment and make use of some advanced data from an example of an in situ study of the atmosphere: the analysis of bacterial diversity of the low troposphere of the Iberian Peninsula during an intrusion of Saharan dust using a C-212 aircraft adequately improved for aerobiological sampling.
\nIt is well known that there is a biota in the atmospheric air. The first study dates back to the nineteenth century, which speak about the presence and dispersion of microorganisms and spores in the atmosphere [27, 28]. Although the atmosphere represents a large part of the biosphere, the density of airborne microorganisms is very low. Estimates suggest that from the ground surface up to about 18 km above sea level (troposphere), there is less than a billionth of the number of cells found in the oceans, soils, and subsurface. Between approximately 18 and 50 km above sea level (stratosphere), temperature, oxygen, and humidity decrease and with them the number of cells. Above the ozone layer (between 18 and 35 km into stratosphere), ultraviolet (UV) and cosmic radiation become lethal factors. Once in the mesosphere (above 50 km), life is difficult to imagine; however microorganisms of terrestrial origin could arrive to the stratosphere from lower layers via different phenomena (human activity, thunderstorms, dust storms, or volcanic activity), and bacteria have been found isolated up to 41 km or in dust samples from the International Space Station (\nFigure 1\n) [6, 29]. Therefore, airborne microbes are always present in the atmosphere [11, 30, 31], and their permanence is dynamic, resulting in an environment with enormous variability. Estimates calculate that over 1021 cells are lifted into the atmosphere every year, leading to considerable transport and dispersal around the atmosphere, with a large portion of these cells returning to the surface due to different atmospheric events as part of a feedback cycle. Undoubtedly, airborne microbes play an important role in meteorological processes. They have been linked to the nucleation phenomena that lead to the formation of clouds, rain, and snow and to the alteration of precipitation events [32, 33, 34]. Their presence is essential to understand long-range dispersal of plant and potential pathogens [7, 35, 36] and maintain diversity in ground systems and could interfere with the productivity of natural ecosystems [17, 18]. On the other hand, airborne bacteria can have important effects on human health, being responsible for different phenomena such as seasonal allergies and respiratory diseases. Based on data from terrestrial environments, the global abundance of airborne bacteria has been estimated to range between 104 and 106 m−3 [37]. However, more recent studies incorporating direct counting by microscopy or quantitative PCR have provided more accurate estimates of the number of airborne microbes, which apparently point to a higher number of cells present in the atmosphere [38, 39, 40, 41].
\nDiagram displaying atmosphere layers, temperature and airborne emission sources. Yellow line marks atmospheric temperature. Bottom of the figures shows the common sources of aerosolized bacteria, with special attention to dust storms.
There is a great variety of airborne microorganism sampling systems, allowing us to select the most suitable one depending on our objectives [42]. On the other hand, no standardized protocols exist, which is a major pitfall when developing our objectives. This fact has led some authors to propose the creation of consortiums of interested parties for establishing standardized protocol reproducibility [20], as well as the need to establish global networks of aerobiological studies [11]. Two approaches are proposed: particles or cells can be collected passively or directly from the atmosphere. Passive media usually involves decanting [43] and collecting particles over snow [44] or through the collection of atmospheric water [45]. On the other hand, active methodologies entail three major approaches: filtration, impaction, and liquid impingement. All three approaches are very efficient when developing culture-dependent techniques. In contrast, culture-independent approaches produce some serious problems that make the work difficult: the high variability of the system and the low biomass mean that sampling campaigns are, in many cases, extremely inefficient [20]. Lastly, the use of airborne platforms is not very extended, but they represent a good opportunity to conduct a more direct study of the atmosphere [5, 19, 31].
\nFiltration is a simple and cheap method that is often efficient. It involves pumping air through a filter where the mineral and biological particles are trapped. Filters of different materials and porosity are available made of cellulose, nylon, polycarbonate or fiberglass, or quartz. Sizes used range from 0.2 to 8 μm, depending on the size of the particles to be captured and the capacity of the pump. In many cases, a PM10 filter can give better results when collecting smaller bacteria, as it allows greater airflow. Airflow filtration rates generally range between 300 and 1000 L/minute [4, 46]. Microorganisms trapped in the filter can be cultured, or the filters can be directly used for DNA extraction. In addition, filters are a very suitable support for microscopy, and countless holders for filters are available (an example is shown in \nFigure 2A\n).
\nThree different samplers of airborne microorganisms. (A) Filter holder and a filter (PALL Corporation). (B) Impinger sampling of bioaerosols (BioSampler, SKC, Inc.). (C) Six-stages Andersen Cascade Impactor (Thermo Fisher Scientific).
In impingement, particles are collected in a liquid matrix [20]. Normally a buffer is used such as phosphate buffer saline (PBS) that helps maintain the viability of the cells. One of the more widely used liquid impingers is BioSampler SKC (\nFigure 2B\n). In this case, the tangential movement of the particles inside the flow impinger retains the particles in the collecting liquid. The suspension obtained could be used for culturing or for molecular ecology assays [20]. One of the advantages of impingement collection is that it facilitates quantitative techniques such as flow cytometry or in situ hybridization [47].
\nIn this system, the particles generally impact into a petri dish with an enrichment medium. It is, possibly, the most efficient and most used method to conduct studies based on culture. Airflow impacting onto the plates is controlled by slots that allow the homogeneous distribution of the air. The system can be single stage or several stages in cascade, causing the particles to be distributed by size in the different petri dishes [20]. Some variants replace petri dishes with agarose filters or Vaseline strips, in order to carry out independent culture methodologies, but efficiency is very low. The original and more popular impactor is the Andersen cascade impactor (\nFigure 2C\n) [48].
\nSeveral studies explain and compare sampling methodologies in aerobiology, but most of them focus on the surface of the Earth (e.g., on top of mountains or buildings) or indoors [42, 49, 50, 51, 52, 53, 54]. However, small studies have been conducted at higher altitudes or in open sea areas. The use of airborne platforms (balloons, aircraft, rockets, etc.) for aerobiology sampling would allow conducting a direct study of the microbial ecology of the atmosphere. Another advantage of airborne platforms is the possibility of studying the vertical distribution of airborne microbial communities. In addition, some aircraft allow us to develop studies in the upper troposphere or in the stratosphere. Unfortunately, atmospheric microbial collection instruments have not been developed enough for airborne platforms.
\nAmong the different airborne platforms, aircraft, due to their versatility and access, are particularly interesting. Some studies have been conducted, but not enough samples have been developed yet, and efficiency is still very low. As already mentioned, the efficiency of samplers in soil-level aerobiology faces a series of problems (low biomass, high variability of populations, lack of standardized protocols). In the case of airplanes, in addition to these intrinsic problems associated with atmospheric microbial ecology, other additional ones exist: (1) the high velocity of the aircraft in relation to the relative quiescent air mass. This makes it difficult to obtain an isokinetic sampler and, therefore, one that is sufficiently efficient that would allow us to obtain a correct quantification of the incoming air [55]; (2) the sampler must be in a location on the airplane that avoids chemical contamination from the operation of the device. Previous studies have used wing-mounted air samplers or the roof of the aircraft to reduce the possibility of in-flight contamination [21, 22, 56, 57, 58]. Similarly, it should allow the aseptic collection of samples, avoiding microbiological contamination during the process. This operation, which can be very simple in the laboratory or at ground level, becomes tremendously complicated on an airplane, since air intakes that are part of the fuselage of the aircraft are often difficult to sterilize. It is therefore necessary to develop robust sterilization protocols. The spectacular work of DeLeon-Rodríguez of 2013 has been criticized in this aspect [40, 59]; (3) sampling time. A possible solution to the low biomass of the atmosphere is to increase sampling time, but in the case of flights, we are limited to the flight autonomy of the aircraft. Although scarce, some studies from airplanes have been conducted. The first studies that were conducted in airplanes were carried out by impaction on a petri plate with enrichment means, which allowed isolating microorganisms from the upper troposphere and even from the stratosphere [21, 57, 60]. However, advances in molecular ecology have caused the most recent studies to favor filtration [40, 58].
\nThe European Facility for Airborne Research (EUFAR) program brings together infrastructure operators of both instrumented research aircraft and remote sensing instruments with the scientific user community. However, it lacked aircraft prepared for microbiological sampling. The National Institute for Aerospace Technology (INTA) belonging to the Spanish Ministry of Defence has two CASA C-212-200 aircraft that were suitably modified to be used as flying research platforms. Now, these two aircraft are a unique tool for the study of atmospheric microbial diversity and the different environments of the EUFAR program. Our research group has a CASA-212 aircraft with an air intake located on the roof of the aircraft. A metal tube fits the entrance and is fitted inside the aircraft to a filter holder, a flowmeter, and a pump (\nFigure 3\n). This simple system is easy to sterilize, and both the metal tube and the filter holder can be replaced in flight by other sterile ones if we want to take different samples. Using PM10 fiberglass filters, we can obtain isokinetic conditions and pass 1800 L of air per hour through the filter, as indicated by the flowmeter.
\nAirborne microorganisms sampler installed in INTA’s CASA C-212-200 aircraft.
In a series of recent experiments, we tried to install a multi-sampler system in our aircraft, where we had five systems in parallel and connected to the same intake of the plane: one filter holder, two impingement systems, and two impactors (\nFigure 4\n). The results clearly showed that in the case of our aircraft, filtration was more efficient (data not shown).
\nMulti-sampler system tested in INTA’s CASA C-212-200 aircraft. (A) Impinger sampler, design and manufacture own. (B) Impactor sampler (Impaktor FH6, Markus Klotz GmbH). (C) Coriolis μ (Bertin Technologies SAS) a impinger biological air sampler. (D) Filter holder (PALL Corporation). (E) Six-stages Andersen Cascade Impactor (Thermo Fisher Scientific).
Aerobiology studies have traditionally focused on the collection of bacterial cells and the analysis of samples by total counting and culture-based techniques. It is known that such methods capture only a small portion of the total microbial diversity [61]. The almost exclusive use, for years, of these methodologies is one of the reasons for these limitations in the knowledge of aerobiology. In addition, culture-dependent methods do not allow us to study the interactions between different species of microorganisms. Culture-independent methods have been used to assess microbial diversity, increasing the specificity of microbial identification and the sensitivity of environmental studies, especially in extreme environments. These methods have recently been applied to various areas of airborne microbiology [62, 63, 64, 65] revealing a greater diversity of airborne microorganisms when compared to culture-dependent methods. Some good studies approach the challenges and opportunities of using molecular methodologies to address airborne microbiology [20, 66]. Although molecular ecology methods allow the rapid characterization of the diversity of complex ecosystems, the isolation of the different components is essential for the study of their phenotypic properties in order to evaluate their role in the system and their biotechnological potential. A combination of culture-dependent and culture-independent methods is ideal to address the complete study of the system.
\nModern culture-independent approaches to community analysis, for example, metagenomics and individual cell genomics, have the potential to provide a much deeper understanding of the atmospheric microbiome. However, molecular ecology techniques face several particular challenges in the case of the atmospheric microbiome: (1) very low biomass [20]; (2) inefficient sampling methods [20]; (3) lack of standard protocols [9, 20]; (4) the composition of airborne microbes continuously changes due to meteorological, spatial, and temporal patterns [7, 62, 67, 68, 69, 70]; and (5) avoidance of the presence of foreign DNA in the system [59]. Because these issues are not yet resolved, most of the non-culturing approaches focus on microbial diversity, where they are highly efficient.
\nThe most recurrent techniques are those based on DNA extraction, gene amplification of 16S/18S rRNA, and next-generation sequencing (NGS) technologies. Often, this approach is more efficient due to the greater efficiency and sensitivity of this process, as opposed to gene cloning and Sanger sequencing; thus some authors are inclined toward metagenomics instead of amplification. This provides more information and avoids an intermediate step, but bioinformatic processing is tedious and often only provides data in relation to diversity, making the annotation of the rest of the information very complicated [20]. These approaches can be complemented with quantitative methods such as qPCR, flow cytometry, or fluorescence in situ hybridization (FISH) [41, 47, 66, 71]. FISH is surely the best and most specific cell quantification methodology that exists. However, in the case of aerobiology, it cannot always be used. A minimum number of cells must exist so that we can observe and count them under a fluorescence microscope. Due to the variability of microbial populations in the air, this is not always achieved. In our research group, we have obtained very good results in this regard, optimizing cell concentration. \nFigure 5\n shows epifluorescence micrographs of bacteria from an air sample. On this occasion, sampling was performed using a biological air sampler (Coriolis μ, Bertin Technologies SAS), where biological particles are collected and concentrated in a liquid (PBS). Sampling was conducted for 2 hours at ground level, pumping a total of 36,000 L of air. After this time, the sample was paraformaldehyde fixed and filtered through a 0.2 μm pore size, hydrophilic polycarbonate membrane, 13 mm diameter (GTTP, Millipore). A half sample was hybridized with the universal Bacteria domain probe, EUB338I-III [72], following a conventional protocol [73]. The second half was hybridized with the probe NON338 [74] as negative control. In this case, an average of 140 cells per liter of air was counted. Occasionally, FISH also allows to observe bacteria attached to mineral particles (\nFigure 5C\n–\nD\n).
\nEpifluorescence micrographs of bacteria from an air sample. (A and C) DAPI-stained cells; (B and D) same fields a A, and C, respectively, showing cells hybridized with probes EUB338I-III (Cy3 labeled), specific for Bacteria domain. All micrographs correspond to the same hybridization process, performed with a sample obtained after 4 hours sampling at ground. C and D show microorganisms attaches to a mineral particles (arrow sign). Bars, 5 μm.
DNA gives us much information about the diversity of the system, but if we wish to obtain information about the metabolic activity that is taking place in the ecosystem, metabolomic and metatranscriptomic approaches are needed [50, 66]. In the case of the atmosphere, this is crucial, since we are not fully certain if the cells present are active. Some studies indicate that a part of the microorganisms in the atmosphere are developing an activity [6], but until we conduct RNA-based and metabolite-based studies, we will not have the certainty that this is the case. The big problem is that it is very difficult to carry out these studies using the current microbial capture systems.
\nScanning electron microscopy (SEM) also provides much information of the aerobiology [7]. Specifically, it allows the characterization of eukaryotic cells (e.g., diatoms) and, above all, pollens and fungal spores, from which we can obtain great information with good images alone. \nFigure 6A\n shows pine tree pollen observed via SEM in a sample obtained after a 30 minutes flight of the C-212 aircraft.
\nSEM images of different airborne samples. (A) Pinus pollen. Ground sample after 2 hours sampling. (B) Air sample collected from C-212-200 aircraft during a Saharan dust intrusion (February 24, 2017). Filter appear completely cover of mineral particles. (B and C) Biological particles sampled using C-212-200 aircraft. (E) Diatomea sampled by C-212-200 aircraft in a fligth along the northern coast of Spain (9 March 2017). (F) Cell attached to mineral particles and organic matter.
As mentioned above, factors, such as the shortage of nutrients and substrates, high UV radiation, drying, changes in temperature and pH, or the presence of reactive oxygen species, make the atmosphere an extreme environment. However, it is possible that the high variability of its conditions is the one characteristic that makes this environment more extreme [1, 20]. Among the cells present in the atmosphere, a considerable portion appears in the resistance forms capable of withstanding low-temperature and high-radiation conditions. This is what probably happens with fungi and gram-positive bacteria. Bacillus strains recurrently isolated from the atmosphere have characteristics and a capacity to sporulate very similar to strains isolated from the soil. Undoubtedly, another part of the cells will be in the form of latency and may even suffer modifications of the cell wall and slow down or stop their metabolic activity [75, 76]. These transformations can improve resistance to physical stresses, such as UV radiation [58]. On the other hand, some of the bacteria present in the atmosphere, such as Geodermatophilus, show pigmentation that undoubtedly protects it from excessive radiation. The microorganisms that are usually detected in the atmosphere originate mainly from the soil, which means they will share similar mechanisms of resistance. In some strains, metabolic adaptations have been observed to lack nutrients such as cytochrome bd biosynthesis to survive iron deprivation [77]. Deinococcus is also a recurrent genus in the atmosphere, which, like those in soil, has multiresistance mechanisms based on high DNA-repair efficiency. Bacteria that do not form spores and certain archaea, in contrast, often have genomes rich in G + C, which may increase tolerance to UV rays and overall survival [78].
\nAnother strategy of resistance could be cell clustering and adhesion to particles. Several studies have confirmed the loss of viability and shielding or the reflective properties of the mineral particles as an important role for the protection of UV radiation [19, 31]. In that sense, it is very possible that many cells have mechanisms that promote aggregation. In our samples, we often find the cells adhered to each other or to minerals, which undoubtedly makes them more resistant (\nFigure 6\n).
\nGlobal and regional models have been used to explain bioaerosol emission, transport, and atmospheric impact [17, 18, 79, 80, 81, 82, 83, 84]. Even so, it is not an easy phenomenon to explain, since it depends on a large number of factors. On the one hand, there are numerous sources of tropospheric aerosols, which include sea salt, volcanic dust, cosmic dust, industrial pollutants, and desert and semidesert areas [6, 85]. We must also consider the factors that make the transfer of particles possible, for example, meteorological phenomena, solar radiation, temperature, tides, erosion, etc. [85]. On the other hand, anthropogenic activities can also affect dust emissions indirectly, by changing the climate and the hydrological cycle. In these aerosols, microorganisms will be included in a greater or lesser number. The degree of richness in cells of tropospheric aerosols will depend largely on the source of emission. Thus, the large wooded masses or fields of crops provide the atmosphere with a good number of microorganisms due to the effect of air or the aerosols produced by rain. Similarly, anthropogenic activity contributes large amounts of bacteria to the environment, treatment plants, and composting areas being sources of airborne microorganisms [85].
\nDesert dust storms play a major role in particle emissions and with them that of microorganisms. In this way, most of the material reaching the atmosphere from the surface comes from desert and semidesert areas, which is known as desert dust. The Sahara-Sahel desert, the Middle East, central and eastern Asia, and Australia are the major sources of desert dust, although all the arid zones of the world are emission sources [9, 86]. Dust storms are atmospheric events typically associated with dry lands due to the preponderance of dried and unconsolidated substrates with little vegetation cover. The strong and turbulent winds that blow on these surfaces raise fine-grained material, a large part of which consists of particles the size of silt (4–62.5 μm) and clay (<4 μm), reducing visibility to less than 1 km. The atmospheric concentrations of PM10 dust exceed 15,000 μg/m3 in severe events [87], although the concentrations naturally decrease with the distance from the areas of origin, extending hundreds of kilometers. The dust particles and cells associated with them are transported in this manner and will be deposited finally, by the effect of rain, snow, or other meteorological phenomena. Therefore, there is a continuous transfer of mineral and biological matter through the atmosphere that moves from the air to the terrestrial environment and changes its geographical area [7, 24].
\nThe Sahara-Sahel desert located in northwestern Africa is one of the major sources of windblown dust in the world [9]. This phenomenon has an impact on the Mediterranean coastline, but Saharan dust has been transported toward the north of Europe and has been found on numerous occasions in the Alps [88, 89] or blown toward the Atlantic and Caribbean [8, 90]. It has been estimated that 80–120 tons of dust are transported annually through the Mediterranean toward Europe [23, 91, 92]. In particular, dust transported by the winds can reach an elevation of up to 8 km in the atmosphere over the Mediterranean basin [93]. Because of its geographic position, the Iberian Peninsula is often affected by these dust events. Specifically, the Sahara-Bodele depression, located at the southern edge of the Sahara desert, has been described as the richest dust source reaching the Iberian Peninsula. Southern Spain is the main area affected, but dust can reach the Pyrenees and even France [43]. Different researchers have studied the mineralogical and chemical composition of Saharan dust, which has been observed to contain calcite, dolomite, quartz, different clay minerals, and feldspars as the main mineral components [94]. The intrusion of big amounts of these components is an important influence on nutrient dynamics and biogeochemical cycling in the atmosphere of the Iberian Peninsula.
\nDespite the large number of studies on dispersion, geochemistry, and mineralogy of African dust, few are focused on microbiology. All these studies conclude that there are microbes associated with dust because there are higher concentrations of aerosolized microorganisms during dust events [43, 90, 93, 94, 95, 96]. However, the magnitude of the concentrations and the specific microbes associated with dust events remain the subject of debate. On the other hand, the viability of these microorganisms is another big question. The United States Geological Survey (USGS) develops the Global Dust Program to investigate the viability of microorganisms transported in dust masses. USGS authors using DNA sequencing of the ribosomal gene were able to isolate and identify more than 200 viable bacteria and fungi in St. John’s samples in the USA [8, 36, 90]. Fungi and bacteria associated with atmospheric dust can be recovered and cultivated, but they must be gram-positive bacteria and many spore formers, which makes them resistant to the extreme conditions of the atmosphere.
\nTherefore, fungi and bacteria associated with dust may have been isolated from dust intrusions, but a percentage of the viable ones already remains an unanswered question. Another big question is the activity of these cells in the atmosphere. It is clear that they are resistant to extremophile conditions, but the question is whether they are developing their life cycle in this particular environment. This question could be answered by molecular ecology methodologies based on the isolation and sequencing of mRNA, but low atmospheric biomass and high variability are, once again, the great problem when developing this type of RNA-based methodologies. On the other hand, clinical records point to many of the viable microorganisms identified in the Saharan dust as the cause of respiratory diseases (asthma and lung infections or allergic reactions), cardiovascular diseases, and skin infections [7, 90, 97, 98]. It is known that other microbes associated with dust in the air are pathogenic to humans, including those that cause anthrax and tuberculosis, or to livestock (such as foot and mouth disease) or plants [7, 90, 97, 98]. Characterization, quantification, and feasibility studies are vital to address these problems.
\nIt is common to find fungal spores belonging to the genus Aspergillus, Nigrospora, Arthrinium, and Curvularia associated with Saharan dust. Bacterial taxa comprised a wide range of phyla, including Firmicutes, Proteobacteria, Actinobacteria, and Bacteroidetes. Generators of genus spores such as Clostridium and Bacillus are very common, along with other gram-positive ones such as Geodermatophilus or Streptococcus. Also, Alphaproteobacteria, a very common bacterium class in soils (e.g., the family Sphingomonadaceae), are associated with dust [4, 9]. As regards Archaea, there are few studies of the atmosphere, in general, and of dust, in particular, that focus on this domain. Surely, reduced cases of pathogenic archaea have been studied to a lesser extent. Aeropyrum is the most detected genus of airborne archaea, but it is related to marine aerosols [11]. On the other hand, studies of pollen associated with dust are widespread. An interesting study investigated pollen transported from North Africa to Spain through Saharan dust and found that pollen from five non-native plant species was detected exclusively during dust events [99]. Lastly, viruses and virus-like particles have a great interest in the emission of dust. One study mentions virus-like particles associated with a transoceanic dust event. This report is based on epifluorescent microscopy of filters stained with a specific nucleic acid stain. An increase in the order of magnitude of virus-like particles was observed, from 104 to 2105 m−3 between the baseline condition and dust conditions in the Caribbean [41]. It is speculated that free airborne viruses show worse resistance to high ultraviolet radiation and dry air associated with long-distance transport in dust events resist worse than others [9].
\nFour aerobiology sampling flights took place during February and March 2017 using the CASA C-212-200 aircraft from INTA. The study focused on microbial diversity in the atmosphere of the Iberian Peninsula during and after a Saharan dust intrusion. Flights took place under four different conditions: (1) during a strong Sahara dust storm that reached the north of the Iberian Peninsula, from February 22 to 24, 2017 (February 23, 2017) (\nFigure 7\n); (2) following precipitation (February 28, 2017); (3) following a dry period (March 8, 2017); and (4) along the northern coast of Spain (March 9, 2017). In each flight, samples were collected at different altitudes, and air samples were obtained simultaneously at ground level. A total of 20 samples were collected and are being analyzed. Cell presence was observed by scanning electron microscopy (SEM), and bacterial diversity is being studied by DNA extraction, 16S rRNA gene amplification, and Illumina MiSeq sequencing. Results are being analyzed via bioinformatics and biostatistical software (MOTHUR, SPSS, STAMP, CANOCO, and PAST) which will allow us to compare the results between the different flows and scenarios.
\nSaharan dust intrusion. Dust pours off the northweat Afrincan coast and blankets the Iberian Peninsula, 23 February, 2016. NASA satelital imagen via MODIS.
Although this study is not yet finished, some data can be advanced in this chapter. \nFigure 6\n shows SEM microphotographs obtained from samples in different scenarios. In general, the samples obtained during the days of dust intrusion (flight of February 23) appear completely covered with mineral particles. In these cases, more biological cells were detected than in the rest of the days. In the particular case of samples from the marine coast flight, more diatoms were observed (\nFigure 6E\n).
\nThe analysis of diversity using the Shannon index showed that, in all cases, diversity was greater on days of Saharan dust intrusion, both in the samples taken from the ground and those taken at higher altitudes with the aircraft. This indicates that Saharan dust contributes microorganisms that are not present in the atmosphere on a daily basis. Diversity analysis showed phylum characteristics of soils, being Alpha- and Betaproteobacteria the most abundant classes. All of the analyses performed showed that bacterial diversity detected at ground level and in-flight samples during the dust intrusion event were similar among one another. The genus taxonomic levels of Sphingomonas, Geodermatophilus, Methylobacter, Rhizobiales, Bacillus, or Clostridium were present in every sample, but their sequences were more abundant in the case of ground samples and dust intrusion samples collected during the day flight. However, sequences of the genus Flavobacterium, Streptococcus, or Cupriavidus were most abundant in the case of samples collected during flight.
\nPreliminary conclusions show that bacterial diversity of airborne bacteria during days of dust intrusion is higher and similar to bacterial diversity commonly detected in soil samples. Further analyses are being conducted with these samples to obtain a complete description of the evolution of bacterial diversity during those days.
\nIntense UV radiation, low pressure, lack of water and nutrients, and freezing temperatures turn the atmosphere into an extreme environment, especially its upper layers. However, it is widely known that airborne bacteria, fungal spores, pollen, and other bioparticles exist. Numerous bacteria and fungi have been isolated and can survive even at stratospheric altitudes. Microbial survival in the atmosphere requires extremophilic characteristics, and therefore airborne microbiota is potentially useful for biotechnological applications. The role of airborne microbial communities is vital in the Earth, including interactions among the atmosphere, biosphere, climate, and public health. Airborne microorganisms are involved in meteorological processes and can serve as nuclei for cloud drops and ice crystals that precede precipitation, which influences the hydrological cycle and climate. Furthermore, their knowledge is essential in understanding the reproduction and propagation of organisms through various ecosystems. Furthermore, they can cause or improve human, animal, and plant diseases.
\nAirborne platforms that allow conducting a direct study of microorganisms in the atmosphere and molecular methodologies (e.g., “omics”) could represent a major opportunity for approaching this question. Nevertheless, some challenges must yet be solved, such as low biomass, efficiency of sampling methods, the absence of standard protocols, or the high variability of the atmospheric environment.
\nDeserts and arid lands are one of the most important sources of aerosol emissions. Clouds of dust generated by storms mobilize tons of mineral particles, and it is known that microorganisms remain attached to the particles being transported over long distances. The large number of mineral particles and microorganisms thus placed into the atmosphere has global implications for climate, biochemical cycling, and health. North African soils, primarily the Sahara Desert, are one of the major sources of airborne dust on Earth. Saharan dust is often transported to southern Europe and could even reach high altitudes over the Atlantic Ocean and the European continent. Again, airborne platforms could be a perfect opportunity for conducting a direct study of the microbiology of this kind of events.
\nThis work has been supported by grants from the Spanish government (
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