Bacteroidota

Microbial mats containing Chlorobium tepidum, from the Lunar and Planetary Institute.

Belongs within: Gracilicutes.
Contains: Bacteroidetes.

The green sulphur bacteria
Published 19 January 2017

There was a time when we really didn’t know what to make of bacterial systematics. We knew that there were a lot of different species out there (not, it turns out, any near as many as there actually are, but still…) but prior to the molecular revolution of the last few decades we lacked the facilities to tell how many of them were related to each other. Nevertheless, there are some bacterial groupings that are distinctive enough to have been recognised even before the advent of regular genetic sequencing. One such group is the green sulphur bacteria.

Culture of Chlorobium phaeobacteroides, from here.

Two things must you know of green sulphur bacteria. One, they are (commonly) green. Two, they are associated with sulphur. Like the more familiar blue-green algae, green sulphur bacteria are photosynthetic, using light energy collected by coloured pigments to assimilate carbon dioxide. In some species the photosynthetic pigments are bacteriochlorophyll c or d, giving the cells a grass green coloration. In others, the pigment is bacteriochlorophyll e, and the cells are a chocolate brown. In contrast to blue-green algae, green sulphur bacteria are anaerobic: instead of using water as an electron donor to produce oxygen, they oxidise sulphide or sulphur to produce sulphur or sulphate (a single species, C. ferrooxidans, uses ferrous iron instead of sulphur). As a result, they are found growing in habitats that light reaches but oxygen doesn’t. Many species are found in thermally stratified lakes or brackish lagoons with little mixing between upper and lower water layers, and form a distinct planktonic layer at the optimum intersection between light and sulphide gradients. They are also common in sulphur-rich hot springs. The cell’s bacteriochlorophylls are concentrated into structures referred to as chlorosomes attached to the cytoplasmic membrane, maximising their ability to gather light at the low intensities. A number of species contain gas vacuoles to improve buoyancy. Most green sulphur bacteria are non-motile, though one species Chloroherpeton thalassium has long, filamentous cells with gliding motility. Molecular phylogenetic analyses have placed this species as the sister taxon to all other described green sulphur bacteria.

Scanning electron micrograph of ‘Chlorochromatium aggregatum’, showing the green sulphur bacteria wrapped around a central (concealed) non-photosynthetic partner. Copyright American Society for Microbiology.

An interesting characteristic of many green sulphur bacteria is their propensity for forming close symbiotic relationships with other, non-photosynthetic bacteria. These associations (referred to as consortia) are so closely integrated that many were described as formal bacterial species before their composite nature was realised, and are commonly still referred to by their old ‘species’ names for convenience (especially as none of the bacteria involved can yet be cultured independently). In the majority of consortia, referred to as ‘Chlorochromatium’ and ‘Pelochromatium’, the non-motile green sulphur bacteria form a layer around the surface of a larger flagellated, non-photosynthetic bacterium. The motile bacterium is able to swim towards sulphide concentrations that are used for energy by the green sulphur bacteria. The oxidised sulphur or sulphate produced by the sulphur bacteria is then believed to be used by the non-photosynthetic partner for its own metabolic purposes. A slightly different type of consortium, referred to as “Chloroplana vacuolata”, grows as non-motile films made up of alternating rows of the green sulphur bacteria and their colourless partners, with the one converting sulphides to sulphur or sulphates and the other converting them back again.

Short and long individuals of the non-green, not-always-sulphur bacterium Ignavibacterium album, from here.

In 2010, a group of researchers described Ignavibacterium album, currently the closest known non-photosynthetic relative of the green sulphur bacteria, from a sulphide-rich hot spring in Japan (Liu, Frigaard et al. 2012). Unlike the green sulphur bacteria, Ignavibacterium is only a facultative anaerobe, being also capable of growing in the presence of oxygen. It uses a number of electron donors including sulphide (though not elemental sulphur) and also has limited abilities to fix carbon dioxide. However, it cannot use carbon dioxide as its only carbon source in the way that the green sulphur bacteria can; as it lacks the ability to synthesise some vital amino acids, it still depends on being able to obtain those compounds from external sources. When first described, Ignavibacterium was believed to be non-motile; however, further study of its genome has identified complete versions of the genes used in flagella production. It is not unknown for motile bacteria to lose their flagella in the process of being cultured, and its seems likely that this happened to the original Ignavibacterium isolate.

A further link between Ignavibacterium and the green sulphur bacteria is provided by an organism that currently goes by the label ‘Candidatus Thermochlorobacter aerophilum’ (Liu, Klatt et al. 2012). As indicated by the term ‘Candidatus‘, Thermochlorobacter has not been cultured in the laboratory. Instead, it is one of an ever-increasing number of bacterial taxa that have been identified from genetic samples extracted directly from the environment, in this case from hot springs in Yellowstone National Park. Even though these organisms have, in a sense, never been directly ‘seen’, we can still infer a great deal from their genomic data about what their characters are likely to be. We know that Thermochlorobacter is photosynthetic like the green sulphur bacteria, able to produce chlorosomes containing bacteriochlorophyll (probabably bacteriochlorophyll d) to obtain energy from sunlight. However, unlike the green sulphur bacteria, Thermochlorobacter lacks the ability to meet all its carbon needs by fixing carbon dioxide; like Ignavibacterium, it depends on external sources of nutrients. It is also aerobic rather than anaerobic, and lacks the ability to oxidise sulphides or sulphur. It does resemble the green sulphur bacteria in lacking the ability to produce flagella. Interestingly, however, it retains some genes that are associated in Ignavibacterium with movement towards nutrient sources; as these genes are also present in Chloroherpeton, I find myself wondering if Thermochlorobacter may be capable of gliding motility in the way that Chloroherpeton is.

Systematics of Bacteroidota
<==Bacteroidota [Sphingobacteria]CD21
    |  i. s.: Leeuwenhoekiella blandensisWK13
    |--ChlorobiRS13
    |    |--+--Kryptonium [Kryptonia, Kryptoniaceae, Kryptoniales]CD21
    |    |  |    `--K. thompsoniCD21
    |    |  `--+--Kapabacteriales [Kapabacteria]CD21
    |    |     `--Ignavibaterium [Ignavibacteria, Ignavibacteriaceae, Ignavibacteriae, Ignavibacteriales]BG-M11
    |    |          `--I. albumBG-M11
    |    `--Chlorobiaceae [Chlorobea, Chlorobia, Chlorobiales, Chlorobibacteria]MK03
    |         |  i. s.: Ancalochloris Gorlenko & Lebedeva 1971AL GH01c
    |         |           `--A. perfilievii Gorlenko & Lebedeva 1971AL GH01c
    |         |--Chloroherpeton Gibson, Pfennig & Waterbury 1985VP GH01c
    |         |    `--*C. thalassium Gibson, Pfennig & Waterbury 1985VP GH01c
    |         `--+--Prosthecochloris Gorlenko 1970AL GH01c
    |            |    `--*P. aestuarii Gorlenko 1970AL GH01c
    |            |--Pelodictyon Laterborn 1913AL GH01c
    |            |    |--*P. clathratiforme (Szafer) Lauterborn 1913AL [=Aphanothece clathratiformis Szafer 1911]GH01c
    |            |    |--P. luteolum (Schmidle) Pfennig & Trüper 1971AL (see below for synonymy)GH01c
    |            |    |--P. phaeoclathratiforme Overmann & Pfennig 1990VP GH01c
    |            |    `--P. phaeum Gorlenko 1972AL GH01c
    |            `--Chlorobium Nadson 1906AL GH01c
    |                 |  i. s.: C. chlorovibrioides Gorlenko, Chebotarev & Kachalkin 1974AL GH01c
    |                 |--C. vibrioforme Pelsh 1936AL (see below for synonymy)GH01c
    |                 `--+--C. tepidum Wahlund, Woese et al. 1996VP GH01c
    |                    `--+--*C. limicola Nadson 1906AL (see below for synonymy)GH01c
    |                       `--+--C. phaeovibrioides Pfennig 1968AL GH01c
    |                          `--C. phaeobacteroides Pfennig 1968AL GH01c
    `--+--+--Dyadobacter fermentansWK13
       |  |--Candidatus Amoebophilus asiaticusWK13
       |  `--Runella slithyformisYC04
       `--+--BacteroidetesRS13
          `--Rhodothermaeota [Rhodothermia]AK17
               |--RhodothermalesAK17
               |    |--Rubricoccus [Rubricoccaceae]AK17
               |    |    `--R. marinusAK17
               |    `--+--RhodothermusGH01a [RhodothermaceaeAK17]
               |       |    `--R. marinusHP98
               |       `--SalinibacterMO03 [SalinibacteraceaeAK17]
               |            `--S. ruberMO03
               `--Balneolales [Balneolia]AK17
                    |--Soortia Amoozegar, Khansha et al. 2017 [Soortiaceae]AK17
                    |    `--S. roseihalophila Amoozegar, Khansha et al. 2017AK17
                    `--BalneolaceaeAK17
                         |--+--Fodinibius salinusAK17
                         |  `--AliifodinibiusAK17
                         |       |--A. roseusAK17
                         |       `--A. sediminisAK17
                         `--+--BalneolaAK17
                            |    |--B. alkaliphilaAK17
                            |    `--B. vulgarisAK17
                            `--GracilimonasAK17
                                 |--G. mengyeensisAK17
                                 |--G. roseaAK17
                                 `--G. tropicaAK17
Nomina invalida: Chlorobium clathratiforme (Szafer 1911) Imhoff 2003JC08
                 Chlorobium luteolum (Schmidle 1901) Imhoff 2003JC08
                 Chloroherpeton limnophilumGH01c
                 Prosthecochloris phaeoasteroidea Puchkova & Gorlenko 1976GH01c
                 Prosthecochloris vibrioformis (Pelsh 1936) Imhoff 2003JC08

*Chlorobium limicola Nadson 1906AL [incl. C. limicola f.sp. thiosulfatophilum (Larsen 1952) Pfennig & Trüper 1971]GH01b

Chlorobium vibrioforme Pelsh 1936AL [incl. C. vibrioforme f.sp. thiosulfatophilum (Larsen 1952) Pfennig & Trüper 1971 non C. limicola f.sp. thiosulfatophilum (Larsen 1952) Pfennig & Trüper 1971]GH01b

Pelodictyon luteolum (Schmidle) Pfennig & Trüper 1971AL [=Aphanothece luteola Schmidle 1901; incl. Clathrochloris sulfurica]GH01b

*Type species of generic name indicated

References

[AK17] Amoozegar, M. A., J. Khansha, M. Mehrshad, S. A. S. Fazeli, M. Ramezani, R. R. de la Haba, C. Sánchez-Porro & A. Ventosa. 2017. Soortia roseihalophila gen. nov., sp. nov., a new taxon in the order Balneolales isolated from a travertine spring, and description of Soortiaceae fam. nov. International Journal of Systematic and Evolutionary Microbiology 67 (1): 113–120.

[BG-M11] Borgonie, G., A. García-Moyano, D. Litthauer, W. Bert, A. Bester, E. van Heerden, C. Möller, M. Erasmus & T. C. Onstott. 2011. Nematoda from the terrestrial deep subsurface of South Africa. Nature 474: 79–82.

[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.

[GH01a] Garrity, G. M., & J. G. Holt. 2001a. 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.

[GH01b] Garrity, G. M., & J. G. Holt. 2001b. Phylum BXI. Chlorobi phy. nov. 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. 601–623. Springer.

[HP98] Hugenholtz, P., C. Pitulle, K. L. Hershberger & N. R. Pace. 1998. Novel division level bacterial diversity in a Yellowstone hot spring. Journal of Bacteriology 180 (2): 366–376.

[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.

Liu, Z., N.-U. Frigaard, K. Vogl, T. Iino, M. Ohkuma, J. Overmann & D. A. Bryant. 2012. Complete genome of Ignavibacterium album, a metabolically versatile, flagellated, facultative anaerobe from the phylum Chlorobi. Frontiers in Microbiology 3: 185. doi: 10.3389/fmicb.2012.00185.

Liu, Z., C. G. Klatt, M. Ludwig, D. B. Rusch, S. I. Jensen, M. Kühl, D. M. Ward & D. A. Bryant. 2012. ‘Candidatus Thermochlorobacter aerophilum:’ an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics. ISME Journal 6: 1869–1882. doi:10.1038/ismej.2012.24.

[MK03] Miroshnichenko, M. L., N. A. Kostrikina, N. A. Chernyh, N. V. Pimenov, T. P. Tourova, A. N. Antipov, S. Spring, E. Stackebrandt & E. A. Bonch-Osmolovskaya. 2003. Caldithrix abyssi gen. nov., sp. nov., a nitrate-reducing, thermophilic, anaerobic bacterium isolated from a Mid-Atlantic Ridge hydrothermal vent, represents a novel bacterial lineage. International Journal of Systematic and Evolutionary Microbiology 53: 323–329.

[MO03] Müller, V., & A. Oren. 2003. Metabolism of chloride in halophilic prokaryotes. Extremophiles 7: 261–266.

[RS13] Rinke, C., P. Schwientek, A. Sczyrba, N. N. Ivanova, I. J. Anderson, J.-F. Cheng, A. Darling, S. Malfatti, B. K. Swan, E. A. Gies, J. A. Dodsworth, B. P. Hedlund, G. Tsiamis, S. M. Sievert, W.-T. Liu, J. A. H. Eisen, S. J., N. Kyrpides, C., R. Stepanauskas, E. M. Rubin, P. Hugenholtz & T. Woyke. 2013. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499: 431–437.

[WK13] Williams, K. P., & D. P. Kelly. 2013. Proposal for a new class within the phylum Proteobacteria, Acidithiobacillia classis nov., with the type order Acidithiobacillales, and emended description of the class Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology 63 (8): 2901–2906.

[YC04] Yi, H., & J. Chun. 2004. Hongiella mannitolivorans gen. nov., sp. nov., Hongiella halophila sp. nov. and Hongiella ornithinivorans sp. nov., isolated from tidal flat sediment. International Journal of Systematic and Evolutionary Microbiology 54: 157–162.

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