Epsilon of the Deeps – Coming to an Organ System near You

The Pompeii worm (Alvinella pompejana), an inhabitant of deep-sea hydrothermal vents, with a covering of filaments composed of symbiotic ε-proteobacteria. Photo by Alison Murray.

The can be no denying that the direct analysis of DNA sequence data sparked a revolution in bacterial systematics. Previously-recognised taxa were reinforced or struck down, while entirely new groups were raised to recognition. The Proteobacteria were definitely one of the most significant of these new groups. By far the largest of the commonly-recognised major bacterial subdivisions, the Proteobacteria encompass a wide variety of taxa, including photosynthetic, colonial and heterotrophic forms. Indeed, the very name "Proteobacteria" reflects this diversity, naming the group after the shape-shifting Greek sea-god Proteus (the inclusion in the Proteobacteria of the the genus Proteus, named after the same polymorphic god, seems to have been purely a coincidence). Within the Proteobacteria, molecular data distinguished five major subdivisions, which have been rather prosaically dubbed the Alpha, Beta, Gamma, Delta and (surprise, surprise) Epsilon groups. Recent analyses have generally continued to support the distinction of these groups (though the boundary between the β and γ groups may sometimes be a little fuzzy), but it is with the last group, the Epsilonproteobacteria, that we are concerned today.

In terms of recognised species, the ε group is by far the smallest class of the proteobacteria, with only about fourteen described genera. The most-studied members of the group are mammalian pathogens such as Campylobacter and Helicobacter, species of the first of which can cause food poisoning, while species of Helicobacter have become famous for their role in the production of stomach ulcers and potentially increasing the risk of gastric and liver cancers. Other genera are also animal-associated - Wolinella succinogenes, for instance, is a non-pathogenic inhabitant of the cattle gut. However, the isolation of environmental DNA samples, as with so many other bacterial groups, demonstrated that our understanding of ε-proteobacterial diversity has been significantly biased by our ability to culture only a relatively small proportion of species. Epsilonproteobacteria, it turns out, are one of the predominant groups of extremophiles in marine systems. In one environmental DNA sample taken from a hydrothermal vent, Epsilonproteobacteria represented nearly 50% of the inferred diversity (Sogin et al., 2006). As I mentioned previously in a post on another group of extremophilic bacteria, the Aquificae, members of the Epsilonproteobacteria and Aquificae include the only known bacteria that are able to oxidise hydrogen in energy production (Takai et al., 2003). Epsilonproteobacteria have also been shown to be abundant in anaerobic hydrogen sulphide-rich cave springs (figure below from Engel et al., 2003).



Those few members of the Epsilonproteobacteria that have been cultured from hydrothermal vents don't appear to reach quite the thermophilic heights of Aquificae - Sulfurimonas is a mesophile (Inagaki et al., 2003), while Caminibacter and Hydrogenimonas showed optimum growth at 55°C (enough to kill a human with long-term exposure, but still small apples compared to the 100°C-plus temperatures reached by some hyperthermophiles – Miroshnichenko et al., 2004; Takai et al., 2004). A number of undescribed species are ectosymbionts of hydrothermal vent animals, such as the tube worms Alvinella pompejana and Riftia pachyptila or the shrimp Rimicaris exoculata.

Inasmuch as all bacterial phylogenies should be trusted as much as a grinning lunatic with one hand behind their back, the terrestrial Epsilonproteobacteria do appear to be nested within the extremophilic taxa, and the question of how deep-sea extremophiles potentially gave rise to terrestrial animal endosymbionts would be an interesting one. Do the Campylobacter and Helicobacter groups form a single clade, with the animal gut being colonised only the once, or where there multiple invasions? Lines are now open.

REFERENcES

Engel, A. S., N. Lee, M. L. Porter, L. A. Stern, P. C. Bennett & M. Wagner. 2003. Filamentous “Epsilonproteobacteria” dominate microbial mats from sulfidic cave springs. Applied and Environmental Microbiology 69 (9): 5503-5511.

Inagaki, F., K. Takai, H. Kobayashi, K. H. Nealson & K. Horikoshi. 2003. Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing ε-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. International Journal of Systematic and Evolutionary Microbiology 43: 1801-1805.

Miroshnichenko, M. L., S. L’Haridan, P. Schumann, S. Spring, E. A. Bonch-Osmolovskaya, C. Jeanthon & E. Stackebrandt. 2004. Caminibacter profundus sp. nov., a novel thermophile of Nautiliales ord. nov. within the class ‘Epsilonproteobacteria’, isolated from a deep-sea hydrothermal vent. International Journal of Systematic and Evolutionary Microbiology 54: 41-45.

Sogin, M. L., H. G. Morrison, J. A. Huber, D. M. Welch, S. M. Huse, P. R. Neal, J. M. Arrieta & G. J. Herndl. 2006. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proceedings of the National Academy of Sciences of the USA 103 (32): 12115-12120.

Takai, K., S. Nakagawa, Y. Sako & K. Horikoshi. 2003. Balnearium lithotrophicum gen. nov., sp. nov., a novel thermophilic, strictly anaerobic, hydrogen-oxidizing chemolithoautotroph isolated from a black smoker chimney in the Suiyo Seamount hydrothermal system. International Journal of Systematic and Evolutionary Microbiology 53: 1947-1954.

Takai, K., K. H. Nealson & K. Horikoshi. 2004. Hydrogenimonas thermophila gen. nov., sp. nov., a novel thermophilic, hydrogen-oxidizing chemolithoautotroph within the ε-proteobacteria, isolated from a black smoker in a Central Indian Ridge hydrothermal field. International Journal of Systematic and Evolutionary Microbiology 54: 25-32.