Actinobacteria

Nodules on alder roots containing Frankia alni, copyright Cwmhiraeth.

Belongs within: Actinobacteriota.
Contains: Microbacteriaceae, Kineosporiaceae, Dermabacteraceae, MicrococcaceaeBrevibacterium, Bifidobacteriaceae, Actinomycetaceae, Demequina, Cellulomonas, Jonesiaceae, Promicromonosporaceae, Bogoriellaceae, Glycomycetaceae, Micromonosporaceae, Geodermatophilaceae, Pseudonocardiaceae, Corynebacteriales, Streptosporangiales, Catenulisporales, Streptomycetaceae, Priopionibacteriales.

The Actinobacteria are a diverse clade of mostly terrestrial, Gram-positive bacteria united by molecular analysis. Members of the clade are morphologically diverse, varying from cocci to rod-shaped taxa to taxa forming complex mycelia (Nouioui et al. 2018). Within Actinobacteria, members of the order Micrococcales have isoprenoid quinone systems composed of menaquinones with 6–14 isoprenoid units in the side chain; one or two subunits may be saturated (Nouioui et al. 2018). The Beutenbergiaceae are aerobic and facultatively anaerobic, irregular rods and cocci that utilise a broad range of carbon sources. Tropheryma whipplei is a poorly known pathogen of humans causing the chronic illness Whipple’s disease.

Cryptosporangium is a genus of aerobic, soil-dwelling bacteria forming branching hyphae with sporangia and aerial mycelia aggregating, and sporangiospores exhibiting motility in water (Goodfellow et al. 2012). Frankia species are often capable of fixing nitrogen and form symbiotic associations with the roots of various angiosperms (Goodfellow et al. 2012).

Actinobacteria: from monads to moulds
Published 8 April 2020

Perhaps no field of biology was revolutionised more by the advent of molecular phylogenetics in the 1990s than bacteriology. Previously, the higher classification of bacteria and their analysis from an evolutionary perspective had mostly an unattainable dream. Though some major groups such as cyanobacteria and spirochetes possessed biochemical and ultrastructural features that had already set them apart, most bacterial lineages could not be robustly associated with each other much above about the genus level. Molecular phylogenetics changed that, allowing the recognition of a number of genetically supported diverse lineages that, between them, divvied up the greater number of described bacterial species. One of the first of these lineages to be formally recognised was the Actinobacteria.

Colour-enhanced SEM of Streptomyces griseus hyphae, from the Actinomycetes Society of Japan.

Actinobacteria are one of the major lineages of what had already been recognised as the Gram-positive bacteria, so called because they can be stained with crystal violet using the technique developed by Hans Christian Gram. The absorption of this stain is not a mere sartorial manner: it relates to the structure of the cell wall which in typical Gram-positive bacteria has a thick layer of peptidoglycan outside the cell membrane (standard Gram-negative bacteria have a thinner peptidoglycan layer and a second cell membrane overlaying it). In some texts from the 1990s, you may encounter the Actinobacteria being referred to as the ‘high G+C Gram-positive bacteria’, in reference to a tendency for the genomes of these bacteria to have a relatively high proportion of cytosine and guanine. As it turns out, this feature is not universal within the actinobacterial lineage, but this group remains recognisable by phylogenetic analysis, gene arrangements, and the presence of distinctive indels and inserts in certain genes (Goodfellow et al. 2012).

Many Actinobacteria have a filamentous growth habit and an assemblage of these forms had been recognised even before the molecular revolution as the ‘actinomycetes’. However, the diversity of cell forms among the Actinobacteria ranges from spherical cocci to complex branching hyphae forming a fungus-like mycelium. Mycelial forms may form complex sporulating structures, sometimes distinctive enough to make them among the relatively few bacteria that may be identified by their external morphology alone. Their selections of habitat run the gamut but the highest diversity of species may be found in soils under aerobic conditions. Thermophilic and anaerobic Actinobacteria are much less numerous. Most are chemo-organotrophs, obtaining energy from the break-down of organic compounds.

Goodfellow et al. (2012) recognised a division of the phylum Actinobacteria between six classes. The largest of these classes includes by far the majority of actinobacterian species and goes by the name of…wait for it…Actinobacteria. Yes, apparently bacterial nomenclature sees no problem with having ‘phylum Actinobacteria’ and ‘class Actinobacteria’ co-existing in the same classification but not referring to the same assemblage of organisms. This. Is. Insane. Even a scan of Goodfellow et al.‘s own text provides examples of the name being referred to without the rank explicitly specified. Seriously, how could anyone even begin to consider this acceptable? The remaining classes–Acidimicrobiia, Coriobacteriia, Nitriliruptoria, Rubrobacteria, Thermoleophilia–each contain only a handful of descried species but, as always with bacterial taxonomy, doubtless countless more remain to be described. Members of one of these classes, the Nitriliruptoria, were not described at all before 2009.

It is hardly surprising that a group as diverse as Actinobacteria should include many representatives of significance to humans. For a start, their status as one of the most diverse groups of soil-living bacteria means that they play a major role in decay processes. A number of species are pathogens of plants and animals; perhaps the most notorious of these are Mycobacterium species such as the tuberculosis-causing M. tuberculosis and the leprosy-causing M. leprae. Members of the genus Frankia are found living in nodules on the roots of certain plants where they provide the host with nitrates by fixing nitrogen from the air. Actinobacteria are also massively significant from a biochemical point of view. Actinobacteria species produce close to half of the known microbial bioactive secondary metabolites (Goodfellow e tal. 2012) and about two-thirds of all known antibiotics (Barka et al. 2016). Particularly significant (providing over 80% of all known actinobacterial antibiotics) in this regard are the various species of Streptomyces, which are also among the most morphologically complex Actinobacteria. When conditions under which Streptomyces mycelia are growing begin to decline, cells within the terrestrial vegetative hyphae will begin to die off in order to provide nutrients to support the growth of spore-producing aerial hyphae. As noted by Barka et al. (2016), production of antibiotics at this time would help to prevent other micro-organisms from swooping in to take advantage of this flood of suddenly released nutrients. I hardly need point out how much the discovery of antibiotics changed the pace of medical progress; it might be argued that our modern society simply could not exist without them. Without Actinobacteria, you might not be alive to read this today.

Systematics of Actinobacteria
Actinobacteria (see below for synonymy)
    |  i. s.: Actinomycites Ellis 1916KC01
    |         Ampullaria Couch 1963 nec Ampullaria Lamarck 1799 (ICZN) nec Werneck in Ehrenberg 1872 (ICZN) nec Sm. 1903 (ICBN)KC01
    |         Myceliochytrium Johanson 1946KC01
    |         Waksmania Lechev. & Lechev. 1957KC01
    |         Actinorhabdospora filicisNC18
    |         Planktophila [Nanopelagicaceae, Nanopelagicales]CD21
    |--Micrococcales [Cellulomonadaceae, Micrococcineae]GH01
    |    |--+--MicrobacteriaceaeNC18
    |    |  `--Tropheryma [TropherymataceaeNC18
    |    |       `--*T. whipplei La Scola et al. 2001NC18
    |    `--+--KineosporiaceaeNC18
    |       `--+--+--DermabacteraceaeNC18
    |          |  `--+--MicrococcaceaeNC18
    |          |     `--+--Sediminivirga luteolaNC18
    |          |        `--+--Spelaeicoccus albusNC18
    |          |           `--BrevibacteriumNC18
    |          `--+--+--BifidobacteriaceaeNC18
    |             |  `--ActinomycetaceaeNC18
    |             `--+--+--‘Luteimicrobium’ albumNC18
    |                |  `--‘Luteimicrobium’ xylanilyticumNC18
    |                `--+--DemequinaNC18
    |                   `--+--+--CellulomonasNC18
    |                      |  `--+--JonesiaceaeNC18
    |                      |     `--PromicromonosporaceaeNC18
    |                      `--+--+--BogoriellaceaeNC18
    |                         |  `--RuaniaceaeNC18
    |                         |       |--*Ruania albidiflavaNC18
    |                         |       `--*Halocatinobacterium albumNC18
    |                         `--BeutenbergiaceaeNC18
    |                              |--*Beutenbergia cavernae Groth et al. 1999NC18
    |                              `--+--Salana multivoransNC18
    |                                 `--+--Miniimonas arenaeNC18
    |                                    `--SerinibacterNC18
    |                                         |--*S. salmoneusNC18
    |                                         `--S. tropicusNC18
    `--+--+--+--+--GlycomycetaceaeNC18
       |  |  |  `--MicromonosporaceaeNC18
       |  |  `--Cryptosporangium [Cryptosporangiaceae, Cryptosporangiales]NC18
       |  |       |--C. mongolienseNC18
       |  |       `--+--C. aurantiacum (ex Ruan et al. 1976) Tamura & Hatano 2001NC18, JC08
       |  |          `--+--C. minutisporangiumNC18
       |  |             `--+--C. japonicumNC18
       |  |                `--+--*C. arvum Tamura et al. 1998NC18
       |  |                   `--C. cibodasenseNC18
       |  `--+--+--+--GeodermatophilaceaeNC18
       |     |  |  `--Antricoccus [Antricoccaceae]NC18
       |     |  |       `--*A. suffuscus Lee 2015NC18
       |     |  `--Jatrophihabitans [Jatrophihabitandaceae]NC18
       |     |       |--+--*J. endophyticus Madhaiyan et al. 2013NC18
       |     |       |  `--J. fulvusNC18
       |     |       `--+--J. huperziaeNC18
       |     |          `--J. soliNC18
       |     `--+--+--PseudonocardiaceaeNC18
       |        |  `--CorynebacterialesNC18
       |        `--+--+--Humicoccus flavidusL13
       |           |  `--Saxeibacter lacteusL13
       |           `--Nakamurella [Nakamurellaceae, Nakamurellales]NC18
       |                |--N. silvestrisNC18
       |                `--+--N. endophyticaNC18
       |                   `--+--N. flavidaNC18
       |                      |--N. lacteaNC18
       |                      `--+--*N. multipartita (Yoshimi et al. 1996) Tao et al. 2004NC18
       |                         `--N. panacisegetisNC18
       `--+--FrankiaNC18
          |    |--F. elaeagniNC18
          |    `--+--F. alniNC18
          |       |    |--F. a. ssp. alniE92
          |       |    |--F. a. ssp. pommeriiE92
          |       |    `--F. a. ssp. vandijkiiE92
          |       `--F. casuarinaeNC18
          `--+--+--+--StreptosporangialesNC18
             |  |  `--Fodinicola feengrottensisNC18
             |  `--+--+--Acidothermus [Acidothermaceae, Acidothermales]NC18
             |     |  |    `--*A. cellulolyticus Mohagheghi et al. 1986NC18
             |     |  `--Sporichthya Lechevalier, Lechev. & Holbert 1968NC18, K-WK92 [Sporichthyaceae, Sporichthyales]
             |     |       |--*S. polymorpha Lechevalier et al. 1968NC18
             |     |       `--S. brevicatenaL13
             |     `--+--CatenulisporalesNC18
             |        `--+--StreptomycetaceaeNC18
             |           `--Motilibacter Lee 2012NC18, L13 [Motilibacteraceae]
             |                |--*M. peucedani Lee 2012L13, NC18
             |                `--M. rhizosphaerae Lee 2013L13
             `--+--PropionibacterialesNC18
                `--+--PhytoactinopolysporaNC18
                   |    |--P. alkaliphilaNC18
                   |    `--P. endophyticaNC18
                   `--Jiangellaceae [Jiangellales]NC18
                        |--HaloactinopolysporaNC18
                        |    |--*H. albaNC18
                        |    `--H. alkaliphilaNC18
                        `---JiangellaNC18
                              |--*J. gansuensisNC18
                              |--J. mangroviNC18
                              `--+--J. alkaliphilaNC18
                                 `--+--J. albaNC18
                                    `--J. muralis Kämpfer et al. 2011NC18

Actinobacteria [Actinobacteridae, Actinomycetales, Actinomycetes, Arabobacteria, Arthrobacteria, Frankiaceae, Frankiales, Frankineae]

*Type species of generic name indicated

References

Barka, E. A., P. Vatsa, L. Sanchez, N. Gaveau-Vaillant, C. Jacquard, J. P. Meier-Kolthoff, H.-P. Klenk, C. Clément, Y. Ouhdouch & G. P. van Wezel. 2016. Taxonomy, physiology, and natural products of Actinobacteria. Microbiology and Molecular Biology Reviews 80 (1): 1–43.

[CD21] Coleman, G. A., A. A. Davín, T. A. Mahendrarajah, L. L. Szánthó, A. Spang, P. Hugenholtz, G. J. Szöllősi & T. A. Williams. 2021. A rooted phylogeny resolves early bacterial evolution. Science 372: 588.

[E92] Eady, R. R. 1992. The dinitrogen-fixing bacteria. In: Balows, A., H. G. Trüper, M. Dworkin, W. Harder & K.-H. Schleifer (eds) The Prokaryotes: A handbook on the biology of bacteria: Ecophysiology, isolation, identification, applications 2nd ed. vol. 1 pp. 534–553. Springer-Verlag: New York.

[GH01] Garrity, G. M., & J. G. Holt. 2001. The road map to the Manual. In: Boone, D. R., R. W. Castenholz & G. M. Garrity (eds) Bergey’s Manual of Systematic Bacteriology 2nd ed. vol. 1. The Archaea and the Deeply Branching and Phototrophic Bacteria pp. 119–166. Springer.

Goodfellow, M., P. Kämpfer, H.-J. Busse, M. E. Trujillo, K. Suzuki, W. Ludwig & W. B. Whitman (eds) 2012. Bergey’s Manual of Systematic Bacteriology 2nd ed. vol. 5. The Actinobacteria, Part A and B. Springer.

[JC08] Judicial Commission of the International Committee on Systematics of Prokaryotes. 2008. Status of strains that contravene Rules 27 (3) and 30 of the International Code of Nomenclature of Bacteria. Opinion 81. International Journal of Systematic and Evolutionary Microbiology 58: 1755–1763.

[KC01] Kirk, P. M., P. F. Cannon, J. C. David & J. A. Stalpers. 2001. Ainsworth & Bisby’s Dictionary of the Fungi 9th ed. CAB International: Wallingford (UK).

[K-WK92] Korn-Wendisch, F., & H. J. Kutzner. 1992. The family Streptomycetaceae. In: Balows, A., H. G. Trüper, M. Dworkin, W. Harder & K.-H. Schleifer (eds) The Prokaryotes: A handbook on the biology of bacteria: Ecophysiology, isolation, identification, applications 2nd ed. vol. 1 pp. 921–995. Springer-Verlag: New York.

[L13] Lee, S. D. 2013. Proposal of the Motilibacteraceae fam. nov., with the description of Motilibacter rhizosphaerae sp. nov. International Journal of Systematic and Evolutionary Microbiology 63 (10): 3818–3822.

[NC18] Nouioui, I., L. Carro, M. García-López, J. P. Meier-Kolthoff, T. Woyke, N. Kyrpides, C., R. Pukall, H.-P. Klenk, M. Goodfellow & M. Göker. 2018. Genome-based taxonomic classification of the phylum Actinobacteria. Frontiers in Microbiology 9: 2007.

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