Actinobacteria is a phylum of gram-positive bacteria with high G+C content. Among gram-positive bacteria, actinobacteria exhibit the richest morphological differentiation, which is based on a filamentous degree of organization like filamentous fungi. The actinobacteria morphological characteristics are basic foundation and information of phylogenetic systematics. Classic actinomycetes have well-developed radial mycelium, which can be divided into substrate mycelium and aerial mycelium according to morphology and function. Some actinobacteria can form complicated structures, such as spore, spore chain, sporangia, and sporangiospore. The structure of hyphae and ultrastructure of spore or sporangia can be observed with microscopy. Actinobacteria have different cultural characteristics in various kinds of culture media, which are important in the classification identification, general with spores, aerial hyphae, with or without color and the soluble pigment, different growth condition on various media as the main characteristics. The morphological differentiation of actinobacteria, especially streptomycetes, is controlled by relevant genes. Both morphogenesis and antibiotic production in the streptomycetes are initiated in response to starvation, and these events are coupled.
- Morphological characteristics
- Cultural characteristics
The history of the classification of prokaryote clearly demonstrates that changes were caused by the availability of new techniques . The development of prokaryotic classification has experienced different stages: (i) the classical or traditional classification mainly based on microbial morphological traits, growth requirements, physiological and biochemical features ; (ii) numerical taxonomy analyzing huge volumes of phenotypic data to derive meaningful relationships amongst a large number of microorganisms can be carried out using computer programs [3, 4]; (iii) chemotaxonomic methods studied the chemical variation in actinobacteria and used chemical characters in classification and identification, and it dealt with the discontinuous distribution of specific chemicals, especially amino acids, lipids, sugars, proteins, and other substances in whole cells, parts of cells or fermentation products, and with enzymes [5, 6]; (iv) genotypic classification based on genetic relatedness, inferred mainly from DNA-DNA hybridization (DDH) and comparative sequence analyses of homologous macromolecules, especially, rRNA [7, 8]. In recent years, more and more genotypic approaches were applied on the classification of actinobacteria, such as multilocus sequence analyses (MLSA) , average nucleotide identity (ANI) [10, 11], and whole genome analysis [10, 12-14]. Recently, the most widely accepted system is the polyphasic approach . This approach combines as many different data as possible, for instance, phenotypic, chemotaxonomic, genotypic, and phylogenetic information. The modern classification method is an important means to understand the biological origin and species diversity. On one hand, the quantitative determination results are more objective; on the other hand, the research results of polyphasic taxonomy not only enrich the taxonomic content greatly, but also enrich the essence of life phenomenon. But the characterization of a strain is a key element in actinobacteria systematics in any period and prokaryotic morphologies are consistent with their phylogenetic reconstructions [16, 17].
Actinobacteria are currently characterized using the polyphasic approach that brings together a variety of phenotypic, chemotaxonomic, and genotypic data that comprise the formal description of a novel taxon. The key elements that should be acquired and analyzed in characterization studies of prokaryotes were outlined : the phenotypic features are the foundation for description of taxa. Most actinobacteria are characterized and classified on the basis of their morphology in the first place. The morphological characteristics are still one of the most basic indexes which provide in-depth information on a taxon.
2. The basic morphological characteristics of actinobacteria
Actinobacteria display the greatest morphological differentiation among gram-positive bacteria; however, the cell structure of actinobacteria are typical prokaryotes and totally different with fungi. The whole structure of a hyphae cell corresponds to bacterial organization: the cytoplasm contains genomic DNA regions, ribosomes, and various inclusions, presumably reserve substances such as polyphosphates, lipids, or polysaccharides. Classic actinomycetes have well-developed radial mycelium. According to the difference of morphology and function, the mycelia can be divided into substrate mycelium and aerial mycelium (Figure 1). Some actinobacteria can form complicated structures, such as spore, spore chain, sporangia, and sporangiospore. The growth and fracture modes of substrate mycelium, the position of spore, the number of spore, the surface structures of spore, the shape of sporangia, and whether sporangiospore have flagella or not are all important morphological characteristics of actinobacteria classification.
2.1. Substrate mycelium
As known as vegetative mycelium or primary mycelium, the substrate mycelium grows into the medium or on the surface of the culture medium. The main function of the substrate mycelium is the absorption of nutrients for the growth of actinobacteria. Under the microscope, the substrate mycelia are slender, transparent, phase-dark, and more branched than aerial hyphae. The single hyphae is about 0.4 to 1.2 µm thick, usually do not form diaphragms and fracture, capable of developing branches. Minority groups (such as
The substrate mycelia are white, yellow, orange, red, green, blue, purple, brown, black, and other colors; some hyphae can produce water-soluble or fat-soluble pigment. The water-soluble pigment can seep into culture medium, which make the medium with the corresponding color. The non-water-soluble (or fat-soluble pigment) make the colony with the corresponding color. The color of the substrate mycelia and whether there are soluble pigments provide important references in the determination of new species.
2.2. Aerial mycelium
Aerial mycelium is the hyphae that the substrate mycelium develops to a certain stage, and grows into the air. Sometimes, aerial hyphae and substrate mycelia are difficult to distinguish. This is easy to distinguish by an impression preparation on a cover slip, viewed in a dry system with a light microscope: substrate hyphae are slender, transparent, and phase-dark; aerial hyphae are coarse, refractive, and phase-bright. The hyphae of the aerial mycelium are characterized by a fibrous sheath, except the genera
2.3. Spore chain
Actinobacteria grow to a certain stage, differentiated in its aerial hyphae, can form reproductive hyphae called spore-bearing mycelium. Indeed, this type of spore formation occurs in most actinobacteria genera. According to observation , spore chains can be divided morphologically respecting their length and number of spore: di- or bisporous with two spores, oligosporous with a few spore, and poly-sporous with many spores. Actinomycete spore chain length, shape, position, color are the important basis for classification.
The monosporous is the mode of single spore production. This form occurs in various suprageneric groups, represented by several well-known genera, such as
The length, shape, position, and color of actinobacteria pore chain are an important basis for classification. Spore chains of the genus
The division of a hyphae and the production of a spore start with the formation of a cross-wall. In general, there are three kinds of methods of actinomycetes sporulation process (Figure 9): (i) when substrate hyphae are fragmented, the septum, which is known as a split septum, may occur and form spore, like the genus
The characteristics of spores have played a very important role in species descriptions for many years. The spores produced individually or in short chains are in general thicker than the hyphae, while those which are developed in long chains usually have the same diameter as the hyphae. Spores are about 1 to 2 µm thick and vary in term of shape and surface characteristics (Figure 10). Common spore morphology is globose, ovoid, coliform, rod-shaped, allantoid, and reniform. The motile spores are equipped with flagella which provide active movement (Figure 11). In some species, like
Many genera of phylogenetically different groups form spores enclosed in sporangia. The sporangium is a sack-like structure, in which the spores are developed and held together until they are released, usually leaving an empty sporangial envelope. Sporangia vary considerably both in terms of size and shape. They measure between 2 to 50 µm in diameter with 10 µm being the most common size. They can be cylindrical, clavate, tubular, bottle-shaped, campanulate, digitate, irregular, lobate, umbelliform, pyriform, or globose (Figure 14, Figure 15). The sporangia arise from the substrate hyphae or aerial hyphae. Sporangia formation is largely divided into two forms: in some genera, sporangia are formed by spore filament winding; in some genera, sporangia are expanded by sporangiophores. Sporangia has sporangial envelope, which has no wall called pseudosporangial. The classical internal structure of latter type of sporangium shows coiled or parallel oriented rows of spores, held together by the sporangial envelope, which continues into the outer layer of the sporangiophore. Sporangiospore is formed by differentiation of protoplasm within sporangia. As spores, sporangial types can be classified on the basis of the number of enclosed spores. Sporangia with few spores may be called oligosporous, with the special consideration given to those with one (monosporous) or two spores (bisporous). Sporangia containing numerous spores are called polysporous. Most sporangiate genera produce motile spore, except for the
In conclusion, sporangia position, sporangia shape, and sporangiospores with or without flagella, are important indications of the genus confirmation, a possible morphological evolutionary series can be observed in the genera with sporangia produced on the aerial mycelium and characterized by a single row of sporangiospores. There is gradation from monosporous, bisporous, tetrasporous, to polysporous sporangia, just like
Some sporulation types are hard to classify according to the traditional scheme of morphological differentiation. These include the genus
2.6. The stability of morphological characteristics
The morphological characteristics of actinobacteria due to gene regulation are generally quite stable, andit is an important basis for classification. The development and formation of some structures, like aerial mycelium, spore, and sporangia, are affected by culture conditions. In some media, strains produce a lot of sporangia or spore, while in other media have little or none. Figure 16 is the diagram of some genera of actinobacteria.
3. Experiment methods of morphological and cultural characteristics
3.1. Cultural characteristics
Cultural characteristics of actinobacteria refer to the growth characteristics and morphology in various kinds of culture media. It is usually determined after incubation for 14 days at 28°C strictly according to methods used in the
Classical taxonomy attaches great importance to the role of culture characteristics in the classification identification, general with spores, aerial hyphae, with or without color and the soluble pigment, different growth condition on various media as the main characteristics (Figure 17). The colors of the mature sporulating aerial mycelium are recorded in a simple way (white, grey, red, green, blue, and violet). When the aerial mass color fell between two colors series, both the colors are recorded. If the aerial mass color of a strain to be studied showed intermediate tints, then both the color series are also noted. The media used are yeast extract-malt extract agar and inorganic-salt starch agar. The groupings are made on the production of melanoid pigments (i.e., greenish brown, brownish black, or distinct brown, pigment modified by other colors) on the medium. The strains are grouped as melanoid pigment produced (+) and not produced (–). In a few cases, the productions of melanoid pigments are delayed or weak, and therefore, it is not distinguishable. This is indicated as variable. This test was carried out on the media ISP-1 and ISP-7, as recommended by International
|ISP Medium 1|
(Tryptone-yeast extract broth agar)
pH 7.0 to 7.2
|ISP Medium 2|
(Yeast extrac-malt extract agar)
|ISP Medium 3|
|ISP Medium 4|
(Inorganic salts-starch agar)
Trace salt solution2pH 7.0 to 7.4
|ISP Medium 5|
Trace salts solution
pH 7.0 to 7.4
|ISP Medium 6|
(Peptone-yeast extract iron agar)
|Peptic digest of animal tissue|
pH 7.0 to 7.2
|ISP Medium 7|
L- aspar agine
Trace salt s solution
As the result of cultivation characteristics that are susceptible to cultural conditions (factors such as culture medium, temperature, pH, and light), the influence of culture characteristics was declining in importance. Usually, only use it as one of many indicators of polyphasic taxonomy. And the cultivating characteristic experiment must be in strict accordance with the International
3.2. Morphological observation
Microscopes are the traditional instruments used for assessing actinobacteria, and they remain as indispensable tools for exploring the morphological, physiological, and genetic diversity present in actinobacteria. Usually, the basic morphology of hyphae and spores is observed by light microscopy, and the microscopic structures of hyphae and spores on the surface are observed by scanning electron microscope (SEM), and the ultramicroscopic structure of the spore flagella and cell is observed by transmission electron microscopes (TEM) (Figure 18).
Transplantation embedding method is usually used in morphological observation of actinobacteria . The selected appropriate agar flat (2 to 4 media) were dug into 1 cm wide rectangular hole, inoculated at the edge of hole, and then covered with sterile coverslip. The flat is cultivated at proper temperature. The coverslips are taken out at different times (usually 5, 10, 14, and 20 days) and observed using light microscopy. According to the graph of light microscopy, the good area is chosen, which is cut into 1 x 1 cm pieces, sprayed directly on the cover sheet, taken pictures using scanning electron microscopy (Figure 19). In order to prevent shape deformation, fixation is usually performed by incubation in a solution of a buffered chemical fixative, such as glutaraldehyde (2.5%, 1.5 h), sometimes in combination with formaldehyde and other fixatives and optionally followed by post fixation with osmium tetroxide. The fixed tissue is then dehydrated. Because air-drying causes collapse and shrinkage, this is commonly achieved by replacement of water in the cells with organic solvents such as ethanol (respectively 30, 50, 70, 90, 100%, dehydration each 15 min) or acetone, and replacement of these solvents in turn with a transitional fluid such as liquid carbon dioxide by critical point drying. The carbon dioxide is finally removed while in a supercritical state, so that no gas–liquid interface is present within the sample during drying. The dry specimen is usually mounted on a specimen stub using an adhesive such as epoxy resin or electrically conductive double-sided adhesive tape, and sputter-coated with gold or gold/palladium alloy before examination in the microscope.
4. The molecular mechanisms of morphological differentiation
Filamentous microorganisms involved two main groups, filamentous fungi and filamentous actinomycetes, particularly the
The actinomycetes developmental life cycle is uniquely complex and involves coordinated multicellular development with both physiological and morphological differentiation of several cell types, culminating in the production of secondary metabolites and dispersal of mature spores [45, 46].
Growth of actinomycetes is from the hyphal, which is similar with filamentous fungi . Using the modern fluorescence microscopy,
In general, when nutrients become limiting, a developmental switch occurs during which hyphae start to escape the moist environment and grow into the air. These so-called aerial hyphae can further differentiate into long chains of spores, which can withstand the adverse conditions. Following their dispersal, these spores will reinitiate growth in suitable environments. Some of the key processes involved in the formation of aerial hyphae by streptomycetes and fungi appear to be very similar. Both groups secrete highly surface-active molecules that lower the surface tension of their aqueous environment enabling hyphae to grow into the air. In the case of filamentous actinomyces, small peptides (i.e., SapB and streptofactin) are secreted, while filamentous fungi use proteins known as hydrophobins to decrease the water surface tension. Although these fungal and bacterial molecules are not structurally related, they can, at least partially, functionally substitute for each other (Figure 22) . The
When hyphal growth is limited, much of the biomass becomes converted into spores through the extraordinary parasitic growth of a fluffy white aerial mycelium. The syncytial aerial hyphal tips (which may contain more than 50 copies of the genome) undergo multiple cell divisions to generate a string of unigenomic compartments, destined to become tough, desiccation-resistant spores . Thus, substantial growth is interpolated between the first sporulation related decisions, made in the substrate mycelium, and the decisions involved in the formation and maturation of the spore compartments themselves (Figure 24) . Additionally, the
Morphological differentiation, which coincides with the production of various secondary metabolites, including antibiotics antitumor drugs and enzyme inhibitors, is initiated, when partial nutrient limitation is encountered. Both morphogenesis and antibiotic production in the streptomycetes are initiated in response to starvation. Upon sensing starvation, the substrate mycelia release small molecules that act as signals for the initiation of aerial hyphal growth, as well as for the production of antibiotics. Besides sensing of the nutritional situation, quorum sensing and other environmental stress signals are also involved and controlled by the hierarchical cascade of
Benefited from recent advances in determining prokaryotic phylogeny, our understanding of actinobacteria taxonomy is constantly improving. The early assumption that the evolution of actinobacteria went from simple to complex in morphology and that the morphological similarities reflect phylogenetic relationship must have been wrong. It is common to see convergence in morphology between totally different organisms as a result of adoption to environmental factors during evolution. The phylum actinobacteria is a large and ancient group of bacteria with many interesting features. Various members represent a gradient of morphological and developmental complexity, from simple coccoid cells like the
This project was supported by the National Natural Science Foundation of China (No. 31270001, and N0. 31460005), Yunnan Provincial Society Development Project (2014BC006), National Institutes of Health USA (1P 41GM 086184 -01A 1). We are grateful to Ms. Chun-hua Yang and Mr. Yong Li for excellent technical assistance.
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