Probabilities of ensuring integrity, availability, and confidentiality.
\r\n\t
\r\n\tThe authors are cordially invited to express their knowledge and awareness in this domain, to share their unpublished clinical trials pertaining to any type of STT, to analyse any new data emerged from their studies and to display their information in a methodical way, so that we may present an original book with novel and useful medical material.
Information systems are of high importance in organizations, industrial process, banking sector, etc. The “human factor” accounts for approximately 70% of information security breaches. Staff are one of the parts of information system. The influence of the “human factor” on the level of system information security is considered in various articles and standards. In particular, the international standards ISO/IEC 27002 provide recommendations for work with staff at various stages: prior to employment, during employment, termination, and change of employment [14]. The reliability of information system operation and the level of information security depend on different conditions. Wrong actions and inactivity of staff and untimely performance of job duties can lead to violations of integrity, availability, and confidentiality of the information. As a result they influence the level of system information security. The staff of information system have certain characteristics that affect a level of system information security as well as technical and software components. Such characteristics form mental state and psychophysical properties of staff. In addition to attacks on the information system implemented by technical methods, there is also an attack on the staff of the information system. This attack can be carried out by means of information-psychological impact (IPI). In this article, it is proposed to consider mathematical models for predicting and estimating the information security level of information systems, taking into account dependent events and information and psychological impact on staff, methods, and stages of implementing information and psychological impact. The approach to the analysis of staff conditions under the information-psychological impact is considered. A methodical approach is proposed for analyzing the impact of qualification and psychological states of staff on the information security level of the information system. The application of this model is considered.
\nThe boundaries of the conditions for the provision of procedures for modeling secure information systems in terms of compliance with integrity, availability, and confidentiality, and the information circulating in them [9, 12, 25] is estimated by the possibility of realizing their technical characteristics in real devices and conditions [2, 13, 15, 22, 23]. In particular, the ready-made nodes of known information systems are separate technical devices with characteristics corresponding with their passport data. They provide the possibility to choose the topology of the information system within the limits of the compatibility characteristics of the system nodes [2, 4, 13, 15, 22, 23, 24]. At the same time, consideration of this approach to modeling allows to choose the priority of providing information security criteria such as integrity, availability, and confidentiality, which are generally interdependent in the construction of an information system and analysis of the possibility of ensuring maximum levels of values of these criteria. It means that depending on the conditions, tasks, which should be solved, and the purpose of building and information system, first of all, it is more important to ensure integrity; second, if availability comes, then it is confidentiality or in another sequence.
\nThis sequence may be due to the complexity of the information system, its configuration, the characteristics of the individual nodes, which are involved in its composition, and external factors that affect the operating conditions. The opinion of experts [12] who make decisions on estimating the values of the parameters of the safety criteria, based on an analysis of the physical characteristics of the information system under consideration, plays an important role in the implementation of this approach. The theorem on the multiplication of the probabilities of dependent events is at the heart of the approach for estimating the parameters of safety criteria [5]. This is due to the dependence of the safety criteria which is described above, estimated by mutual influence in the analysis of the characteristics of the information system. For example, a separate information system node is a complete single device with specific technical characteristics that are individually responsible for the likely conditions for ensuring either integrity or availability or confidentiality. At the same time, by virtue of the technical implementation, this node cannot be ideal from the point of view of safety criteria and cannot provide only either integrity or availability or confidentiality, since the information that must have a certain level of each criterion will circulate in it. And the characteristics of this node will extend to a certain part of the information system, which also estimates the important conditions for ensuring its security [26]. The security of information, in the sense of analyzing the probability of the existence of safety criteria, in the information system can be represented in the diagram of sets shown in Figure 1.
\nPresentation of integrity, availability, and confidentiality using sets.
If the integrity (I), availability (A), and confidentiality (C) are separate sets, then security (S) is the intersection of these three sets.
\nIt means that it is necessary to ensure both integrity, and availability, and confidentiality to a specific value of the appropriate criterion, estimated for each particular information system in order to ensure security [12, 25]. In its turn, from the point of view of ensuring the probability of the information system security and due to the interdependence described above, integrity, availability, and confidentiality are conditional signs. Then the probability of security should be considered in the following way (Eq. (1)) [12]:
\nThe figure shows a graphical interpretation of the product of the corresponding events I, A, and C for which the following expression is valid (Eq. (2)):
\nSince the events of ensuring integrity, availability, and confidentiality are dependent, then the probability of producing these events according to the multiplication rule for the probabilities of dependent events, is (Eq. (3)):
\nTo describe the case, the probability of coexistence of several dependent events is equal to the product of the probabilities of these events, and the probability of each next event in the order of recording is calculated if all the previous ones also take place.
\nIt means that the probability of ensuring both integrity and availability and confidentiality of information is equal to the product of the probability of ensuring integrity to the probability of providing availability if there is ensuring of integrity and the probability of ensuring of confidentiality while integrity and availability are provided.
\nAs it was mentioned before, the priority of the place of writing in the formula of the corresponding probabilities can be estimated by the experts’ opinion, taking into account the complexity of their calculation, caused by the need to implement the corresponding values of the safety criteria levels, according to the physical expressions which describe these criteria levels [12].
\nThus, the described approach makes it possible to model various information systems based on real physical characteristics that allow to predict and evaluate the levels of safety criteria, taking into account the experts and experts’ opinions, and it is actual and necessary in practical implementation nowadays [12]. The information security level of the information system can be estimated according to the calculated values (1).
\nAlong with the impact on the technical and software components of the information system, there are also effects pointed to the staff of the information system (Figure 2). They are information-psychological impacts (IPI) [6, 7, 8, 9, 10, 11]. They can lead to a change in the characteristics of employees that are the subject of IPI; as a result, the information security level of the information system may change. As a rule, IPI data are usually transmitted through common communication channels.
\nImpacts on the information system.
It is possible to single out the following stages of IPI implementation [6, 7, 8, 9, 10, 11]:
The subject determines the goals to be achieved by IPI.
The subject determines the object of IPI.
The subject collects information about the IPI object and investigates the psychophysical characteristics of the IPI object in order to detect subject matters of the IPI object and their characteristics (the subject is understood to be a component of the IPI object that determines its possible characteristics; one characteristic may belong to several IPI objects).
The subject chooses the most appropriate means of influencing the IPI object and the communication channel, based on the data of points 1–3. Each of the means affects the relevant objects of influence and their characteristics.
The subject forms a message for the IPI object.
The subject implements an impact on the IPI object, with the aim of achieving a sustainable change in characteristics. To do it, the generated message is coded using the selected IPI tools and sent via the selected communication channel to the object.
The IPI object decodes the received message.
The decoded message affects the characteristics of the IPI object; as a result, they change, and there is some possibility of appearing/disappearing new characteristics.
In Figure 3, the scheme of IPI is shown.
\nScheme of IPI.
The formal model of the IPI process is proposed [7, 8, 11]. For the IPI object \n
Each object can have several characteristics. Dependence of objects and their characteristics is estimated in the matrix of properties. In the columns, the subject-matters of the IPI object are indicated; in the lines, characteristics are indicated; at the intersection, their correspondence is denoted (Eq. (5)):
\nThe subject has many means of impact that do not always correspond with articles of the IPI object; this is proposed that the set of means of the subject’s impact is defined as \n
Each of the means of impact \n
Realization of IPI for m-characteristics (Eq. (6)):
\nFor the case when the IPI object possesses articles with characteristics, and the subject has means of impact, this is proposed to obtain the matrix of efficiency of IPI; in the columns, the articles of the IPI object are indicated; in the lines, characteristics are indicated; at the intersection, their correspondence is denoted (Eq. (7)):
\nThe sum of all impacts on the m-characteristic is described by Eq. (8):
\nwhere the efficiency is provided when the matrixes are added in stages, which means that several IPI tools can affect one characteristic. The formal model of IPI implementation can be written in the following form (Eq. (9)):
\nOperation « ⋅ » has the following properties:
\n1. \n
2. \n
3. \n
The result of the malefactor’s attack on the IPI object is a matrix of properties, which will take the changed form (Eq. (11)):
\nSome of the properties resulting from IPI may remain unchanged; others are replaced by \n
The change in the property which undergoes IPI can be described by equation or model [11, 16, 17, 18, 19] (Eq. (12)):
\nwhere P is the characteristics of the IPI object, H is the characteristics of the IPI (means of impact), and K is the response (the level of change). As the characteristic of IPI, we will use H as the effectiveness of implementing the means of influencing the property \n
Eq. (12) makes it possible to evaluate the change in the properties and the response of an object to IPI. In our case, staff are considered as the IPI object. Eq. (13) of the change in the property and the human reaction to the effects is given in articles [11, 16, 17, 18, 19] and has the form (Eq. (14)):
\nwhere F is the frustration; F0 means some value of the level of frustration, considered normal or threshold; A is the aggression; Q means the time parameter; R is the stiffness; X means the effectiveness of information-psychological impact; and Y is the reaction level. These parameters are measured in conditional scores. They can be estimated using psychological tests and an expert method. This is proposed to use Eq. (11) to estimate the change in the property of the IPI object as a result of the action. The transfer equation for Eq. (14) has the form (Eq. (15)):
\nEmployees’ qualifications, mental state, and psychophysical properties can act as their characteristics.
\nThis is a proposed estimate of staff’s qualification in an expert way:
k = 0 if the staff of the information system are idle in the case of vulnerabilities, technical malfunctions are idle in the technical and software components of the information system [27, 28].
k < 1 if the staff of the information system fail to remove vulnerabilities, technical malfunctions fail in the technical and software components of the information system in time [27, 28].
k = 1 if the staff of the information system eliminate vulnerabilities, technical malfunctions eliminate in the technical and software components of the information system in time [27, 28].
k > 1 if the staff of the information system independently detect and fix vulnerabilities (temporary solutions, before the release of the update from the manufacturer) in the technical and software components of the information system, technical malfunctions are prevented [27, 28].
The limiting minimum value for the staff’s qualification k is 0, because staff does not create vulnerabilities and technical malfunctions in the technical and software components of the information system. The maximum value for the staff’s qualification k is 3; in this case the security service includes a large number of highly skilled employees who can increase labor productivity working together.
\nThe estimation should be carried out separately for each component because maintenance of various components of the information system is implemented in different ways. This is proposed to define the malfunction as various malfunctions in the operation of the information system components that require staff intervention to eliminate them. This is proposed to understand vulnerability as a defect of information system that can violate its integrity, availability, and confidentiality and cause a malfunction.
\nDuring the work activity, the staff of the information system may be in different psychological conditions. The effectiveness of the staff depends on what psychological state they are in. The following states can be distinguished as [3, 20, 29]:
Optimum working condition ensures the greatest efficiency of activity. It is characterized by the presence of a conscious goal of activity, high concentration of attention, aggravation of memory, and activation of thinking. The electroencephalogram shows that in this state, the brain rhythms mainly lie in the beta range.
The state of tense activity arises in the course of work in abnormal situations. Mental tension develops directly in proportion to the difficulty of the task. Easy tasks are solved with minimal effort; complex and new actions require a higher degree of mental pressure. Mental tension is a physiological reaction of the organism, mobilizing its resources to perform more difficult tasks. Mental tension stimulates the physical and mental processes of the human body, which increases its adaptive abilities. The tension reaction develops in a responsible environment, as well as when people perform complex production tasks, if they change the stereotype of actions and habitat and if they are under the influence of extreme conditions. Under the influence of mental stress, vital body functions such as metabolism, circulation, and respiration change. If in the behavior of a person, there is some general concentration, the actions become clearer, the speed of motor reactions increases, and physical performance improves. At the same time, perception becomes aggravated, the process of thinking is accelerated, memory is improved, and concentration of attention is increased.
It should be remembered that the dependence of the efficiency of labor activity (working capacity) of employees on the level of tension of its functional systems is parabolic. It was found out that mental stress has a positive effect on the result of labor up to a certain limit. Exceeding the critical level of activation leads to a decrease in the results of labor up to a complete loss of efficiency.
Fatigue is a functional state of a person, temporarily occurring under the influence of prolonged or intensive work, accompanied by a decrease in its effectiveness. Fatigue is caused by the depletion of body resources during prolonged or excessive activity and is characterized by a decrease in motivation to work, a violation of attention and memory. At the physiological level, the appearance of a protective inhibition of the central nervous system is noted. Fatigue may eventually go into the exhaustion, which requires a longer rehabilitation to get it over.
Stress is a state of increased and prolonged pressure associated with the inability to adapt to the requirements of the habitat. This condition is caused by the long-term impact of environmental factors, exceeding the possibilities of the organism adaptation. It is characterized by mental stress, a sense of frustration, anxiety, and worry, and in the last stage, indifference and apathy appear. At the physiological level, there is a depletion of adrenal hormone stores, muscle tension, and a two-phase activation of the autonomic nervous system.
Figure 4 shows the possible dynamics of staff states. The transition between states can occur both as a result of labor activity and under the influence of information-psychological impact.
\nPossible dynamics of staff transitions in the course of labor activity.
The effectiveness of staff for different psychological conditions is a quantity with no dimension and can be estimated in the following way:
For an optimal working condition, the efficiency of labor activity will be estimated as (Eq. (16)) [3, 20, 29]
where k is the qualification of the staff.
For the state of intense activity, the efficiency of labor activity will be estimated as (Eq. (17)) [3, 20, 29]
where \n
For the state of fatigue, the efficiency of labor activity will be estimated as (Eq. (18)) [3, 20, 29]
where k is the qualification of the staff, b [1/h] is the parameter that estimates the rate of staff fatigue, and t [h] is time.
For the state of fatigue, the efficiency of labor activity will be estimated as (Eq. (19)) [3, 20, 29]
where k is the qualification of the staff, b [1/h] is the parameter that estimates the rate of staff fatigue, s is the reaction to information-psychological impact, and t [h] is time.
The efficiency of labor activity is equal to zero for the state of relaxation.
The information system consists of various technical and software components; each of them can have vulnerabilities and fail due to a technical malfunction. Vulnerabilities and technical faults pose a threat to the confidentiality, integrity, and availability of information. This is proposed to represent the information system as a set of queuing systems [26, 27, 28]; each of them simulates the dynamics of vulnerabilities and technical faults that threaten the confidentiality, integrity, and availability of information. The input of the described system receives a non-stationary Poisson stream of requests (vulnerabilities and faults). This model is presented in Figure 5, where \n
Model of changes in the state of security of the information system, taking into account the staff activities.
The average speed of elimination of vulnerabilities and faults of the information system will be described in the following way (Eq. (20)):
\nwhere \n
The assessment of \n
The average number of vulnerabilities and faults in the information system will be the sum of the average number of vulnerabilities and faults that threaten the confidentiality, integrity, and availability of information (Eq. (22)):
\nWhen \n
There is a probability of a number of vulnerabilities and faults (Eq. (24)):
\nThus, the probability of the absence of vulnerabilities and faults is (Eq. (25))
\nIn general, based on the proposed models, it is proposed to estimate the security of the information system \n
where \n
To analyze the influence of the human factor on the properties of each component of the investigated information system, one can consider, as (Eq. (27)) [1]:
\nwhere \n
Let us consider an information system, consisting of an X router and a file server under the management of the operating system Y. Users who are allowed to have an access connect to the router through a Wi-Fi connection and get an access to files according to the permitting access system.
\nIn this information system, confidentiality, integrity, and availability are provided by means of a router and a server running the operating system Y.
\nIt is possible to infringe the security of the information system by violating the performance of one of the components which are responsible for confidentiality, integrity, and availability.
\nAs the experience of practical studies [12] has shown for 802.11 wireless networks in calculating the probability values of safety criteria, it is advisable to take noise immunity coding into account for the estimation of integrity. But it is necessary to take modulation efficiency and bandwidth usage technology into account for the estimation of availability, and it is important to take cryptographic strength of encryption into account for the estimation of confidentiality. Then the expression for the probability of ensuring the security of information takes the form (Eq. (28)):
\nwhere
\nWith a more detailed representation of the parameters (Eq. (32)):
\nwhere \n
Thus, perhaps there are five more options for writing and using the applied expression for multiplying dependent probabilities. Perhaps, because of the complexity of accounting for modeling the network with a great number of parameters in the above expressions, experts believe that in the proposed formula for calculating security, the probability of availability should be put on the first place, the second one should be given to the conditional probability of confidentiality, and then the conditional probability of integrity comes.
\nIf it is possible to ensure security while ensuring integrity and confidentiality considering integrity and availability in the context of integrity and confidentiality, the expression for the probability of network security will take the following form (Eq. (35)):
\nand so on.
\nDifferent variants of writing these expressions are fair to use then; it is more advantageous to calculate safety when taking into account the corresponding described conditions. For different networks, the probabilities of security criteria will be described by different physical expressions and different number of parameters in these physical expressions [5, 12].
\nFor different information systems at different stages of the technological process that they implement, it may be expedient to differentiate the priority of providing information security criteria (integrity, availability, confidentiality), including the exclusion of some of them. For example, in information retrieval systems that provide users with a legislative basis or a database of threats, it is primarily necessary to ensure the integrity and availability of information, while ensuring confidentiality is not required, since information is publicly available.
\nObtaining probability values is a separate research area and requires a separate assessment technique [12]. Values of the probability of ensuring integrity, availability, and confidentiality for various information systems are given in Table 1. These values are obtained on the basis of practical experience [21].
\nProbability \n | \nAvailability | \nConfidentiality | \nIntegrity | \n
---|---|---|---|
For Case 1 | \n0.85 | \n0.88 | \n0.86 | \n
For Case 2 | \n0.74 | \n0.85 | \n0.9 | \n
For Case 3 | \n0.91 | \n0.82 | \n0.64 | \n
Probabilities of ensuring integrity, availability, and confidentiality.
Table 2 shows the average time to resolve vulnerabilities and faults for components of various information systems.
\n\n\n | \nAvailability | \nConfidentiality | \nIntegrity | \n
---|---|---|---|
For Case 1 | \n0.019 | \n0.016 | \n0.023 | \n
For Case 2 | \n0.04 | \n0.021 | \n0.3 | \n
For Case 3 | \n0.01 | \n0.001 | \n0.03 | \n
Average time and speed of vulnerability and malfunction elimination.
Table 3 provides statistics on the intensity of vulnerability and fault detection for components of various information systems.
\n\n\n | \nAvailability | \nConfidentiality | \nIntegrity | \n
---|---|---|---|
For Case 1 | \n0.00366 | \n0.002 | \n0.0077 | \n
For Case 2 | \n0.001 | \n0.0047 | \n0.01781 | \n
For Case 3 | \n0.00146 | \n0.0023 | \n0.00724 | \n
Statistics of the intensity of vulnerability and fault detection for components of the information system.
Let \n
Using Eq. (14), this is proposed to estimate the reaction to the information-psychological impact. Depending on the characteristics of the staff, the reaction can be both sustainable (staff can do their duties; their effectiveness is defined as Eq. (19)) and unstable (staff is incapable). In the case of an unstable reaction, the graph of the reaction level of the staff is periodic; in the case of a stable reaction, the graph of the reaction level of the staff will not be periodic. Figure 6 presents examples of the dependence of the level of staff reaction on the information and psychological impact.
\nThe level of the subject’s reaction to information and psychological impact.
Let the staff in question have the following characteristics, obtained from the results of the psychological tests of Eysenck: \n
Using Eq. (26), this is proposed to estimate the probability of the security of the information system. Figure 7a–c shows the probability of the security of the information system, depending on the coefficient of staff work and their state, for the first, second, and third cases. At first, the results of IPI on staff are not apparent, so the graphics are depicted from 1 hour of the operation of the information system.
\nProbability of the information system security, depending on the employees’ workload and their condition [(1) optimal condition, (2) fatigue status, (3) state of stressful activity, (4) stressful condition (impact on staff)].
It can be seen from the graph that upgrading the skills of staff leads to an increase in the probability of security of the information system. Thus, the high qualification of the staff can compensate the information and psychological effects on the staff and their fatigue from prolonged activities.
\nFigure 8a–c shows the probability of security of the information system for the first, second, and third cases, respectively, if a staff qualification level is equal to one, depending on the condition of staff. Figure 8d shows the probability of the security of the information system for the third case, taking into account the recess for recovery. However, the time for the restoration process itself was not taken into account. Figure 8e shows an enlarged transition fragment after recovery for Figure 8d. A time interval equal to the average working day was taken for consideration.
\nProbability of the information system security at the level of staff qualification is equal to 1, depending on the condition of the staff [(1) optimal condition, (2) state of fatigue, (3) state of tense activity, (4) stressful condition (impact on staff)].
At the initial stage of operation with a stressed state, the probability of ensuring the security of the information system is higher than at the optimal state, but this is a temporary effect; as it can be seen from Figure 8a with prolonged operation in the stressed state, the probability of the information system safety is lower than at the optimal state. With an optimal state, the probability of ensuring the security of the information system is higher than if staff are in a state of fatigue or under the influence of IPI in a stressful state. Figure 8d shows that if the staff use the break to restore their original characteristics, the probability of the information system safety increases.
\nFor example, on December 23, 2015 [1], Ukrainian power companies experienced unscheduled power outages impacting a large number of customers in Ukraine. The outages experienced on December 23, 2015, were caused by external cyber attackers. After extensive reconnaissance of the victim networks, the telephone tdos attack was conducted on staff. As a result staff did not notice that substations disconnected in time. Exemplary actions of cyber malefactors and psychological conditions of staff are shown in the time diagram of Figure 9.
\nTime diagram of exemplary actions of cyber malefactors and psychological conditions of staff.
The received results coincide with the data obtained in the course of practical activity by interviewing the staff and owners of information systems, so it confirms the effectiveness of the proposed model for estimating the level of systems information security based on probabilistic analysis of the impact of their staff qualifications and psychological state.
\nThus, to ensure the security of the information system, it is essential to take into account the abilities of staff. It is necessary to take into account the qualification of staff, which can change the probability of security of the information system characterized by technical and functional construction according to Eq. (1), from values \n
The proposed method allows to use the probabilistic assessment of the system information security, taking into account the technical characteristics of the components of the information system, the qualifications of the staff, the mental state of the employees, and their psychophysical characteristics. Their permanent use in system life cycle helps to increase information security and decrease a potential danger of “human factor.”
\nExtremophile 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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