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The versatile ε-proteobacteria: key players in sulphidic habitats

Key Points

  • The ε-proteobacteria represent a unique assemblage of microorganisms that have had little defined taxonomic or ecological consideration, despite the attention given to the pathogenic members, and despite the recent explosion in the number of unclassified and unaffiliated ε-proteobacterial 16S rRNA sequences deposited into the public databases.

  • Because most lineages are without cultured representatives or are only known from environmentally retrieved 16S rRNA gene sequences from PCR-based studies, an evaluation of class taxonomic structure serves as a frame of reference for placing the environmental ε-proteobacterial sequences in an evolutionary context. For each of the phylogenetic clusters identified in this study, sequence affinities strongly correlate with ecotype distribution and metabolic diversity and capabilities.

  • Our taxonomy reveals a large cluster of environmentally relevant groups, representing the largest increase in 16S rRNA gene-sequence diversity throughout the ε-proteobacteria. We have provisionally termed this cluster the Thiovulgaceae fam. nov.

  • Thiovulgaceae fam. nov. includes several recently described genera, and the diversity within this cluster is being revealed, particularly in terrestrial habitats.

  • The ε-proteobacteria are metabolically versatile and are well suited to environmental variability and extreme habitat conditions. As such, they are ecologically and biogeochemically significant in modern symbioses with metazoans, or in anaerobic or microaerophilic, sulphur-rich, marine and terrestrial aquatic habitats, many of which are deemed 'extreme' environments.

  • Many of the ε-proteobacteria, and specifically those affiliated with the Thiovulgaceae fam. nov., are chemolithoautotrophs, and might have had an important ecological and biogeochemical role throughout much of Earth's history.

Abstract

The ε-proteobacteria have recently been recognized as globally ubiquitous in modern marine and terrestrial ecosystems, and have had a significant role in biogeochemical and geological processes throughout Earth's history. To place this newly expanded group, which consists mainly of uncultured representatives, in an evolutionary context, we present an overview of the taxonomic classification for the class, review ecological and metabolic data in key sulphidic habitats and consider the ecological and geological potential of the ε-proteobacteriain modern and ancient systems. These integrated perspectives provide a framework for future culture- and genomic-based studies.

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Figure 1: Phylogeny of 1,037 near full-length (>1,200 bp) ε-proteobacterial sequences collected from public databases and published research.
Figure 2: The provisional Thiovulgaceae fam. nov. clade.
Figure 3: The reductive or reverse TCA (rTCA) cycle of carbon fixation.

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Acknowledgements

B.J.C was partially supported by the National Science Foundation. A.S.E was partially supported by the College of Basic Sciences at Louisiana State University, USA. The authors thank T.E. Hanson for his valuable input in to this review.

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Correspondence to Barbara J. Campbell or Annette Summers Engel.

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DATABASES

Entrez Genome Project

Helicobacter pylori

Chlorobium limicola

Nautilia sp. strain AmH

Persephonella marina

Aquifex aeolicus

FURTHER INFORMATION

Barbara Campbell's web page

Annette Summers Engel's laboratory

A Metagenome of Alvinella pompejana symbiont database link

DDBJ

EMBL

Epsilonproteobacteria sequence data files and alignments

GenBank

RDPII

Glossary

Thermophile

An organism that grows optimally at high temperatures, usually above 45°C.

Autotroph

An organism that can use carbon dioxide as the sole source of carbon for growth.

Heterotroph

An organism that uses organic compounds as nutrients to produce energy for growth.

Chemocline

A chemical gradient from high to low concentrations, often consisting of a relatively small stratum where the concentration changes rapidly between the two endpoints.

Mesophile

An organism that grows optimally at moderate temperatures, ranging between 20°C and 45°C.

Chemolithoautotroph

An organism that obtains energy from inorganic compounds and carbon from CO2.

Calvin?Benson pathway

Also known as the Calvin?Benson cycle. A series of biochemical, enzyme-mediated reactions in which CO2 is reduced and incorporated into organic molecules.

Reductive TCA cycle

(rTCA cycle). The TCA cycle in reverse, leading to the fixation of CO2. Represents a putatively ancient metabolic pathway in which autotrophic carbon fixation occurs under anaerobic conditions.

Mixotroph

An organism that can use both heterotrophic and autotrophic metabolic processes.

Phylotype

A group of sequences that show some threshold of sequence similarity, usually >97%, and that also form a monophyletic clade.

Epibiont

An organism that lives attached to a host organism without apparent consequence (benefit or detriment) to the host.

Push cores

Soft sediment collected using a hollow plastic collection tube that is pushed into the sediment, after which the ends are closed.

Methane cold seeps

Areas of the deep ocean floor where oil and methane gas bubble up from under sea-sediment layers at ambient temperatures, providing an energy source that can sustain deep-sea microbial communities.

Wood?Ljungdahl pathway

Also known as the acetyl-coenzyme A pathway. An ancient carbon-fixation pathway found in bacteria and archaea in which CO2 is converted to acetate; the key enzyme is acetyl-coenzyme A synthase/CO dehydrogenase.

Aphotic

Receiving no light or energy from the sun.

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Campbell, B., Engel, A., Porter, M. et al. The versatile ε-proteobacteria: key players in sulphidic habitats. Nat Rev Microbiol 4, 458–468 (2006). https://doi.org/10.1038/nrmicro1414

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