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      Sequence Divergence and Conservation in Genomes of Helicobacter cetorum Strains from a Dolphin and a Whale

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          Abstract

          Background and Objectives

          Strains of Helicobacter cetorum have been cultured from several marine mammals and have been found to be closely related in 16 S rDNA sequence to the human gastric pathogen H. pylori, but their genomes were not characterized further.

          Methods

          The genomes of H. cetorum strains from a dolphin and a whale were sequenced completely using 454 technology and PCR and capillary sequencing.

          Results

          These genomes are 1.8 and 1.95 mb in size, some 7–26% larger than H. pylori genomes, and differ markedly from one another in gene content, and sequences and arrangements of shared genes. However, each strain is more related overall to H. pylori and its descendant H. acinonychis than to other known species. These H. cetorum strains lack cag pathogenicity islands, but contain novel alleles of the virulence-associated vacuolating cytotoxin ( vacA) gene. Of particular note are (i) an extra triplet of vacA genes with ≤50% protein-level identity to each other in the 5′ two-thirds of the gene needed for host factor interaction; (ii) divergent sets of outer membrane protein genes; (iii) several metabolic genes distinct from those of H. pylori; (iv) genes for an iron-cofactored urease related to those of Helicobacter species from terrestrial carnivores, in addition to genes for a nickel co-factored urease; and (v) members of the slr multigene family, some of which modulate host responses to infection and improve Helicobacter growth with mammalian cells.

          Conclusions

          Our genome sequence data provide a glimpse into the novelty and great genetic diversity of marine helicobacters. These data should aid further analyses of microbial genome diversity and evolution and infection and disease mechanisms in vast and often fragile ocean ecosystems.

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          Most cited references45

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          Helicobacter pylori evolution and phenotypic diversification in a changing host.

          Helicobacter pylori colonizes the stomachs of more than 50% of the world's population, making it one of the most successful of all human pathogens. One striking characteristic of H. pylori biology is its remarkable allelic diversity and genetic variability. Not only does almost every infected person harbour their own individual H. pylori strain, but strains can undergo genetic alteration in vivo, driven by an elevated mutation rate and frequent intraspecific recombination. This genetic variability, which affects both housekeeping and virulence genes, has long been thought to contribute to host adaptation, and several recently published studies support this concept. We review the available knowledge relating to the genetic variation of H. pylori, with special emphasis on the changes that occur during chronic colonization, and argue that H. pylori uses mutation and recombination processes to adapt to its individual host by modifying molecules that interact with the host. Finally, we put forward the hypothesis that the lack of opportunity for intraspecies recombination as a result of the decreasing prevalence of H. pylori could accelerate its disappearance from Western populations.
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            Partitioning of bacterial communities between seawater and healthy, black band diseased, and dead coral surfaces.

            Distinct partitioning has been observed in the composition and diversity of bacterial communities inhabiting the surface and overlying seawater of three coral species infected with black band disease (BBD) on the southern Caribbean island of Curaçao, Netherlands Antilles. PCR amplification and sequencing of bacterial 16S rRNA genes (rDNA) with universally conserved primers have identified over 524 unique bacterial sequences affiliated with 12 bacterial divisions. The molecular sequences exhibited less than 5% similarity in bacterial community composition between seawater and the healthy, black band diseased, and dead coral surfaces. The BBD bacterial mat rapidly migrates across and kills the coral tissue. Clone libraries constructed from the BBD mat were comprised of eight bacterial divisions and 13% unknowns. Several sequences representing bacteria previously found in other marine and terrestrial organisms (including humans) were isolated from the infected coral surfaces, including Clostridium spp., Arcobacter spp., Campylobacter spp., Cytophaga fermentans, Cytophaga columnaris, and Trichodesmium tenue.
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              Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens.

              Deep-sea vents are the light-independent, highly productive ecosystems driven primarily by chemolithoautotrophic microorganisms, in particular by epsilon-Proteobacteria phylogenetically related to important pathogens. We analyzed genomes of two deep-sea vent epsilon-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 epsilon-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 epsilon-Proteobacteria share many virulence genes with pathogenic epsilon-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 H(2)-uptake hydrogenase) and genomic plasticity of the pathogenic descendants appear to have roots in deep-sea vent epsilon-Proteobacteria. These provide ecological advantages for hydrothermal vent epsilon-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.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                17 December 2013
                : 8
                : 12
                : e83177
                Affiliations
                [1 ]Department of Molecular Microbiology, Washington University Medical School, St Louis, Missouri, United States of America
                [2 ]Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland
                University of Münster, Germany
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DK DB. Performed the experiments: DK DB. Analyzed the data: DK MR DB. Contributed reagents/materials/analysis tools: DK MR DB. Wrote the paper: DK MR DB.

                [¤]

                Current address: Division of Infectious Disease, Department of Medicine, University of California, La Jolla, California, United States of America

                Article
                PONE-D-13-09160
                10.1371/journal.pone.0083177
                3866246
                24358262
                41faef3a-7667-48d7-be6e-406ec0506ca7
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 March 2013
                : 8 November 2013
                Page count
                Pages: 15
                Funding
                This research was supported by grants from the US National Institutes of Health R21 AI078237 and R21 AI088337. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Research Article

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