Insights into the genome of large sulfur bacteria revealed by analysis of single filaments
Marine sediments are frequently covered by mats of the filamentous Beggiatoa and other large nitrate-storing bacteria that oxidize hydrogen sulfide using either oxygen or nitrate, which they store in intracellular vacuoles. Despite their conspicuous metabolic properties and their biogeochemical impo...
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| Veröffentlicht in: | PLoS biology 2007-09, Vol.5 (9), p.e230-e230 |
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| creator | Mussmann, Marc Hu, Fen Z Richter, Michael de Beer, Dirk Preisler, André Jørgensen, Bo B Huntemann, Marcel Glöckner, Frank Oliver Amann, Rudolf Koopman, Werner J H Lasken, Roger S Janto, Benjamin Hogg, Justin Stoodley, Paul Boissy, Robert Ehrlich, Garth D |
| description | Marine sediments are frequently covered by mats of the filamentous Beggiatoa and other large nitrate-storing bacteria that oxidize hydrogen sulfide using either oxygen or nitrate, which they store in intracellular vacuoles. Despite their conspicuous metabolic properties and their biogeochemical importance, little is known about their genetic repertoire because of the lack of pure cultures. Here, we present a unique approach to access the genome of single filaments of Beggiatoa by combining whole genome amplification, pyrosequencing, and optical genome mapping. Sequence assemblies were incomplete and yielded average contig sizes of approximately 1 kb. Pathways for sulfur oxidation, nitrate and oxygen respiration, and CO2 fixation confirm the chemolithoautotrophic physiology of Beggiatoa. In addition, Beggiatoa potentially utilize inorganic sulfur compounds and dimethyl sulfoxide as electron acceptors. We propose a mechanism of vacuolar nitrate accumulation that is linked to proton translocation by vacuolar-type ATPases. Comparative genomics indicates substantial horizontal gene transfer of storage, metabolic, and gliding capabilities between Beggiatoa and cyanobacteria. These capabilities enable Beggiatoa to overcome non-overlapping availabilities of electron donors and acceptors while gliding between oxic and sulfidic zones. The first look into the genome of these filamentous sulfur-oxidizing bacteria substantially deepens the understanding of their evolution and their contribution to sulfur and nitrogen cycling in marine sediments. |
| doi_str_mv | 10.1371/journal.pbio.0050230 |
| format | Article |
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Despite their conspicuous metabolic properties and their biogeochemical importance, little is known about their genetic repertoire because of the lack of pure cultures. Here, we present a unique approach to access the genome of single filaments of Beggiatoa by combining whole genome amplification, pyrosequencing, and optical genome mapping. Sequence assemblies were incomplete and yielded average contig sizes of approximately 1 kb. Pathways for sulfur oxidation, nitrate and oxygen respiration, and CO2 fixation confirm the chemolithoautotrophic physiology of Beggiatoa. In addition, Beggiatoa potentially utilize inorganic sulfur compounds and dimethyl sulfoxide as electron acceptors. We propose a mechanism of vacuolar nitrate accumulation that is linked to proton translocation by vacuolar-type ATPases. Comparative genomics indicates substantial horizontal gene transfer of storage, metabolic, and gliding capabilities between Beggiatoa and cyanobacteria. These capabilities enable Beggiatoa to overcome non-overlapping availabilities of electron donors and acceptors while gliding between oxic and sulfidic zones. 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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: Mußmann M, Hu FZ, Richter M, de Beer D, Preisler A, et al. (2007) Insights into the Genome of Large Sulfur Bacteria Revealed by Analysis of Single Filaments. PLoS Biol 5(9): e230. doi:10.1371/journal.pbio.0050230</rights><rights>2007 Mußmann et al. 2007</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c763t-2d79a00e3bbc4b4fe45e5433184c8d25651354f83ccfb7fd6749dacb255118913</citedby><cites>FETCH-LOGICAL-c763t-2d79a00e3bbc4b4fe45e5433184c8d25651354f83ccfb7fd6749dacb255118913</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC1951784/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC1951784/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17760503$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mussmann, Marc</creatorcontrib><creatorcontrib>Hu, Fen Z</creatorcontrib><creatorcontrib>Richter, Michael</creatorcontrib><creatorcontrib>de Beer, Dirk</creatorcontrib><creatorcontrib>Preisler, André</creatorcontrib><creatorcontrib>Jørgensen, Bo B</creatorcontrib><creatorcontrib>Huntemann, Marcel</creatorcontrib><creatorcontrib>Glöckner, Frank Oliver</creatorcontrib><creatorcontrib>Amann, Rudolf</creatorcontrib><creatorcontrib>Koopman, Werner J H</creatorcontrib><creatorcontrib>Lasken, Roger S</creatorcontrib><creatorcontrib>Janto, Benjamin</creatorcontrib><creatorcontrib>Hogg, Justin</creatorcontrib><creatorcontrib>Stoodley, Paul</creatorcontrib><creatorcontrib>Boissy, Robert</creatorcontrib><creatorcontrib>Ehrlich, Garth D</creatorcontrib><title>Insights into the genome of large sulfur bacteria revealed by analysis of single filaments</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Marine sediments are frequently covered by mats of the filamentous Beggiatoa and other large nitrate-storing bacteria that oxidize hydrogen sulfide using either oxygen or nitrate, which they store in intracellular vacuoles. 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These capabilities enable Beggiatoa to overcome non-overlapping availabilities of electron donors and acceptors while gliding between oxic and sulfidic zones. 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| ispartof | PLoS biology, 2007-09, Vol.5 (9), p.e230-e230 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Public Library of Science (PLoS) |
| subjects | Actin Cytoskeleton - genetics Analysis Bacteria Base Sequence Beggiatoa - genetics Deoxyribonucleic acid DNA Eubacteria Genes Genetic aspects Genome, Bacterial Genomes Genomics Hydrogen Sulfide - metabolism Life sciences Metabolic Networks and Pathways - genetics Microbiology Motility Nitrates Nitrates - metabolism Oxidation-Reduction Oxygen - metabolism Prokaryotes Sulfur-oxidizing bacteria |
| title | Insights into the genome of large sulfur bacteria revealed by analysis of single filaments |
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