Nonpathogenic Epsilonproteobacteria

Satoshi Nakagawa, Hokkaido University, Hakodate, Japan
Yoshihiro Takaki, Japan Agency for Marine‐Earth Science and Technology (JAMSTEC), Yokosuka, Japan

Published online: September 2009

DOI: 10.1002/9780470015902.a0021895

The Epsilonproteobacteria is a class within the phylum Proteobacteria and has been primarily recognized as a group of pathogenic microorganisms. However, nonpathogenic Epsilonproteobacteria has been increasingly of great biological importance. They represent bacteria with the highest metabolic versatility. Nonpathogenic Epsilonproteobacteria occurs dominantly in various redoxclines such as deep-sea vents, stratified ocean, terrestrial sulfidic caves, and oil fields as both epi- or endosymbionts and free-living microorganisms. Recent genome analysis has revealed that some virulence determinants and the genomic plasticity of the pathogenic Epsilonproteobacteria appear to have roots in nonpathogenic, chemoautotrophic Epsilonproteobacteria. These work advantageously for pathogenic Epsilonproteobacteria to be efficiently and persistently infectious and for nonpathogenic Epsilonproteobacteria to thrive in extreme habitats. In the genomic era, previously unrecognized evolutionary links are emerging between important human/animal pathogens and their nonpathogenic, symbiotic, chemoautotrophic relatives.

Key concepts

  • The Epsilonproteobacteria is the class within the phylum Proteobacteria and represented by important human/animal pathogens.
  • The perception of the class Epsilonproteobacteria has recently changed dramatically.
  • The Epsilonproteobacteria comprise numerous nonpathogenic bacteria with diverse ecophysiology and phylogeny.
  • Nonpathogenic Epsilonproteobacteria play key roles in biogeochemical cycles in various extreme environments on earth.
  • Nonpathogenic Epsilonproteobacteria provide new insights into the origin of animal/human pathogens.

Keywords: Epsilonproteobacteria; nonpathogenic; diversity; chemoautotroph; deep-sea vents

Figure 1. Phylogenetic tree of 16S rRNA gene sequences. Branch colours indicate origins of nonpathogenic Epsilonproteobacteria as follows: red, deep-sea vents; blue, other marine habitats and green, terrestrial environments. Scale bar represents the expected number of changes per position. *, Whole-genome sequence is available and , whole genome is being sequenced.
Figure 2. Deep-sea vents as one of the largest reservoirs of nonpathogenic Epsilonproteobacteria. Host animals (polychaete, Paralvinella; shrimp, Alvinocaris and squat crab, Shinkaia) are shown.
Figure 3. Conservation of gene content across proteobacterial genomes in relation to phylogenetic distance. Each dot represents a pair of species within each class of Proteobacteria (96 genomes, 1126 pairs). Conservation of gene contents was calculated by dividing the number of genes shared between two genomes by the number of genes in the smaller genome. Phylogenetic distance was calculated according to Jukes–Cantor's model using the SSU rRNA gene sequences. In addition to pairs of epsilonproteobacterial species (red), pairs of endosymbionts (green) and parasites (blue) are highlighted.
Figure 4. 16S rRNA tree, with the predicted number for protein families at each node displayed (green), and the number of families gained (upper in red) or lost (lower in blue) for each branch. Some representatives of gained or lost genes are shown in parentheses. The inference of gene content was performed using the GeneTRACE algorithm (Kunin and Ouzounis, 2003). Protein families were assigned using the InParanoid/MultiParanoid (Remm et al., 2001; O'Brien et al., 2005). Two Deltaproteobacteria (Geobacter sulfurreducens PCA and Desulfovibrio vulgaris Hildenborough) were used as outgroup (not shown). NLG, N-linked glycosylation system.
close
 References
    Alain K, Querellou J, Lesongeur F et al. (2002) Caminibacter hydrogeniphilus gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing bacterium isolated from an East Pacific Rise hydrothermal vent. International Journal of Systematic and Evolutionary Microbiology 52: 1317–1323.
    Baar C, Eppinger M, Raddatz G et al. (2003) Complete genome sequence and analysis of Wolinella succinogenes. Proceedings of the National Academy of Sciences of the USA 100: 11690–11695.
    Campbell B and Cary S (2001) Characterization of a novel spirochete associated with the hydrothermal vent polychaete annelid, Alvinella pompejana. Applied and Environmental Microbiology 67: 110–117.
    Campbell B and Cary S (2004) Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep-sea hydrothermal vents. Applied and Environmental Microbiology 70: 6282–6289.
    Campbell B, Engel A, Porter M and Takai K (2006) The versatile -proteobacteria: key players in sulphidic habitats. Nature Reviews. Microbiology 4: 458–468.
    Campbell B, Smith J, Hanson T et al. (2009) Adaptation to submarine hydrothermal environments exemplifed by the genome of Nautilia profundicola. PLoS Genetics 5: e1000362.
    Corre E, Reysenbach A and Prieur D (2001) -proteobacterial diversity from a deep-sea hydrothermal vent on the Mid-Atlantic Ridge. FEMS Microbiology Letters 205: 329–335.
    Donachie S, Bowman J, On S and Alam M (2005) Arcobacter halophilus sp. nov., the first obligate halophile in the genus Arcobacter. International Journal of Systematic and Evolutionary Microbiology 55: 1271–1277.
    Engel A, Porter M, Stern L, Quinlan S and Bennett P (2004a) Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic ‘Epsilonproteobacteria’. FEMS Microbiology Ecology 51: 31–53.
    Engel A, Stem L and Bennett P (2004b) Microbial contributions to cave formation: new insights into sulfuric acid speleogenesis. Geology 32: 369–372.
    Fenchel T and Glud R (1998) Veil architecture in a sulphide-oxidizing bacterium enhances contercurrent flux. Nature 394: 367–369.
    Garcia-Pichel F (1989) Rapid bacterial swimming measured in swarming cells of Thiovulum majus. Journal of Bacteriology 171: 3560–3563.
    book Garrity G, Bell J and Lilburn T (2005) "Class V. Epsilonproteobacteria class nov". In: Brenner D, Krieg N and Staley J (eds) Bergey's Manual of Systematic Biology, 2nd edn, vol. 2, pp. 1145–1194. New York: Springer.
    Gevertz D, Telang A, Voordouw G and Jenneman G (2000) Isolation and characterization of strains CVO and FWKO B, two novel nitrate-reducing, sulfide-oxidizing bacteria isolated from oil field brine. Applied and Environmental Microbiology 66: 2491–2501.
    Goffredi S, Jones W, Erhlich H, Springer A and Vrijenhoek R (2008) Epibiotic bacteria associated with the recently discovered Yeti crab, Kiwa hirsuta. Environmental Microbiology 10: 2623–2634.
    Grzymski J, Murray A, Campbell B et al. (2008) Metagenome analysis of an extreme microbial symbiosis reveals eurythermal adaptation and metabolic flexibility. Proceedings of the National Academy of Sciences of the USA 105: 17516–17521.
    Haddad A, Camacho F, Durand P and Cary S (1995) Phylogenetic characterization of the epibiotic bacteria associated with the hydrothermal vent polychaete Alvinella pompejana. Applied and Environmental Microbiology 61: 1679–1687.
    Hongoh Y, Ohkuma M and Kudo T (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiology Ecology 44: 231–242.
    Huber J, Butterfield D and Baross J (2003) Bacterial diversity in a subseafoor habitat following a deep-sea volcanic eruption. FEMS Microbiology Ecology 43: 393–409.
    Hügler M, Wirsen C, Fuchs G, Taylor C and Sievert S (2005) Evidence for autotrophic CO2 fixation via the reductive tricarboxylic acid cycle by members of the epsilon subdivision of proteobacteria. Journal of Bacteriology 187: 3020–3027.
    Kodama Y, Ha L, Watanabe K (2007) Sulfurospirillum cavolei sp. nov., a facultatively anaerobic sulfur-reducing bacterium isolated from an underground crude oil storage cavity. International Journal of Systematic and Evolutionary Microbiology 57: 827–831.
    Kodama Y and Watanabe K (2004) Sulfuricurvum kujiense gen. nov., sp. nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity. International Journal of Systematic and Evolutionary Microbiology 54: 2297–2300.
    Kunin V and Ouzounis CA (2003) GeneTRACE-reconstruction of gene content of ancestral species. Bioinformatics 19: 1412–1416.
    Linz B and Schuster SC (2007) Genomic diversity in Helicobacter and related organisms. Research in Microbiology 158: 737–744.
    Miller WG, Parker CT, Rubenfield M et al. (2007) The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri. PLoS ONE 2: e1358.
    Moyer C, Dobbs F and Karl D (1995) Phylogenetic diversity of the bacterial community from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii. Applied and Environmental Microbiology 61: 1555–1562.
    Nakagawa S and Takai K (2008) Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiology Ecology 65: 1–14.
    Nakagawa S, Takai K, Inagaki F et al. (2005a) Variability in microbial community and venting chemistry in a sediment-hosted backarc hydrothermal system: Impacts of subseafloor phase-separation. FEMS Microbiology Ecology 54: 141–155.
    Nakagawa S, Takai K, Inagaki F et al. (2005b) Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field. Environmental Microbiology 7: 1619–1632.
    Nakagawa S, Takai K, Inagaki F, Horikoshi K and Sako Y (2005c) Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the -Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa Trough. International Journal of Systematic and Evolutionary Microbiology 55: 925–933.
    Nakagawa S, Takaki Y, Shimamura S et al. (2007) Deep-sea vent -proteobacterial genomes provide insights into emergence of pathogens. Proceedings of the National Academy of Sciences of the USA 104: 12146–12150.
    O'Brien KP, Remm M and Sonnhammer EL (2005) Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Research 33: D476–D480.
    On S (2001) Taxonomy of Campylobacter, Arcobacter, Helicobacter and related bacteria: current status, future prospects and immediate concerns. Journal of Applied Microbiology 90: 1S–15S.
    Polz M and Cavanaugh C (1995) Dominance of one bacterial phylotype at a Mid-Atlantic Ridge hydrothermal vent site. Proceedings of the National Academy of Sciences of the USA 92: 7232–7236.
    Porter M and Engel A (2008) Diversity of uncultured Epsilonproteobacteria from terrestrial sulfidic caves and springs. Applied and Environmental Microbiology 74: 4973–4977.
    Remm M, Storm CE and Sonnhammer EL (2001) Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. Journal of Molecular Biology 314: 1041–1052.
    Römling U and Amikam D (2006) Cyclic di-GMP as a second messenger. Current Opinion in Microbiology 9: 218–228.
    Sievert S, Scott K, Klotz M et al. (2008) The genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Applied and Environmental Microbiology 74: 1145–1156.
    Simon J (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiology Reviews 26: 285–309.
    Suzuki Y, Kojima S, Sasaki T et al. (2006) Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Applied and Environmental Microbiology 72: 1388–1393.
    Suzuki Y, Sasaki T, Suzuki M et al. (2005) Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Applied and Environmental Microbiology 71: 5440–5450.
    Takai K, Campbell B, Cary S et al. (2005) Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of Epsilonproteobacteria. Applied and Environmental Microbiology 71: 7310–7320.
    Takai K, Inagaki F, Nakagawa S et al. (2003) Isolation and phylogenetic diversity of members of previously uncultivated -Proteobacteria in deep-sea hydrothermal fields. FEMS Microbiology Letters 218: 167–174.
    Taylor CD and Wirsen CO (1997) Microbiology and ecology of filamentous sulfur formation. Science 277: 1483–1485.
    Thar R and Kühl M (2002) Conspicuous veils formed by vibrioid bacteria on sulfidic marine sediment. Applied and Environmental Microbiology 68: 6310–6320.
    Tokuda G, Yamada A, Nakano K, Arita N and Yamasaki H (2008) Colonization of Sulfurovum sp. on the gill surfaces of Alvinocaris longirostris, a deep-sea hydrothermal vent shrimp. Marine Ecology 29: 106–114.
    Urakawa H, Dubilier N, Fujiwara Y et al. (2005) Hydrothermal vent gastropods from the same family (Provannidae) harbour - and -proteobacterial endosymbionts. Environmental Microbiology 7: 750–754.
    Vignais P, Billoud B and Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiology Reviews 25: 455–501.
    Wirsen C, Sievert S, Cavanaugh C et al. (2002) Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Applied and Environmental Microbiology 68: 316–325.
 Further Reading
    book Christie DM, Fisher CR, Lee SM and Givens S (2006) Back-arc Spreading Systems: Geological, Biological, Chemical, and Physical Interactions. Washington DC: American Geophysical Union.
    book Dahl C and Friedrich CG (2008) Microbial Sulfur Metabolisms. New York: Springer.
    book Nachamkin I, Szymanski CM and Blaser MJ (2008) Campylobacter, 3rd edn, Washington DC: ASM Press.
    Nakagawa S and Takai K (2006) Methods for the isolation of thermophiles from deep-sea hydrothermal environments. Methods in Microbiology 35: 55–91.
    book Overmann J (2006) Molecular Basis of Symbiosis. New York: Springer.
    book Schlegel HG and Bowien B (1989) Autotrophic Bacteria. New York: Springer.
    book Van Dover CL (2000) The Ecology of Deep-sea Hydrothermal Vents. Princeton: Princeton University Press.
    book Yamaoka Y (2008) Helicobacter pylori. Norfolk, UK: Caister Academic Press.

Related Sub-Topics:

Physiological Ecology | Biomes and Ecosystems | Organisms and the Physical Environment | Bacteria | Environmental Microbiology | Microbial Evolution and Taxonomy | Extremophiles
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Nonpathogenic Epsilonproteobacteria
 
How to Cite close
Nakagawa, Satoshi, and Takaki, Yoshihiro(Sep 2009) Nonpathogenic Epsilonproteobacteria. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021895]