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Published online on July 5, 2007, 10.1073/pnas.0700687104
PNAS | July 17, 2007 | vol. 104 | no. 29 | 12146-12150
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BIOLOGICAL SCIENCES / MICROBIOLOGY
Deep-sea vent {varepsilon}-proteobacterial genomes provide insights into emergence of pathogens

Satoshi Nakagawa{dagger},{ddagger}, Yoshihiro Takaki§, Shigeru Shimamura§, Anna-Louise Reysenbach, Ken Takai{dagger}, and Koki Horikoshi{dagger},§

{dagger}Subground Animalcule Retrieval (SUGAR) Program and §Extremophiles Research Program, Extremobiosphere Research Center (XBR), Japan Agency for Marine–Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan; and Department of Biology, Portland State University, Portland, OR 97201

Edited by Rita R. Colwell, University of Maryland, College Park, MD, and approved June 7, 2007 (received for review January 25, 2007)

Deep-sea vents are the light-independent, highly productive ecosystems driven primarily by chemolithoautotrophic microorganisms, in particular by {varepsilon}-Proteobacteria phylogenetically related to important pathogens. We analyzed genomes of two deep-sea vent {varepsilon}-Proteobacteria strains, Sulfurovum sp. NBC37-1 and Nitratiruptor sp. SB155-2, which provide insights not only into their unusual niche on the seafloor, but also into the origins of virulence in their pathogenic relatives, Helicobacter and Campylobacter species. The deep-sea vent {varepsilon}-proteobacterial genomes encode for multiple systems for respiration, sensing and responding to environment, and detoxifying heavy metals, reflecting their adaptation to the deep-sea vent environment. Although they are nonpathogenic, both deep-sea vent {varepsilon}-Proteobacteria share many virulence genes with pathogenic {varepsilon}-Proteobacteria, including genes for virulence factor MviN, hemolysin, invasion antigen CiaB, and the N-linked glycosylation gene cluster. In addition, some virulence determinants (such as the H2-uptake hydrogenase) and genomic plasticity of the pathogenic descendants appear to have roots in deep-sea vent {varepsilon}-Proteobacteria. These provide ecological advantages for hydrothermal vent {varepsilon}-Proteobacteria who thrive in their deep-sea habitat and are essential for both the efficient colonization and persistent infections of their pathogenic relatives. Our comparative genomic analysis suggests that there are previously unrecognized evolutionary links between important human/animal pathogens and their nonpathogenic, symbiotic, chemolithoautotrophic deep-sea relatives.

{varepsilon}-Proteobacteria | comparative microbial genomics | deep-sea hydrothermal vent | pathogenesis | symbiosis


Freely available online through the PNAS open access option.

Author contributions: S.N. and Y.T. designed research; S.N., Y.T., and S.S. performed research; S.N., Y.T., and S.S. analyzed data; and S.N., A.-L.R., K.T., and K.H. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

Data deposition: Genome sequences of Sulfurovum sp. NBC37-1 and Nitratiruptor sp. SB155-2 have been deposited in DDBJ/EMBL/GenBank databases under the project accession nos. AP009179 and AP009178, respectively.

This article contains supporting information online at www.pnas.org/cgi/content/full/0700687104/DC1.

{ddagger}To whom correspondence should be addressed. E-mail: nakagawas{at}jamstec.go.jp

© 2007 by The National Academy of Sciences of the USA


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