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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Main Authors: Marc Mussmann, Fen Z Hu, Michael Richter, Dirk de Beer, André Preisler, Bo B Jørgensen, Marcel Huntemann, Frank Oliver Glöckner, Rudolf Amann, Werner J H Koopman, Roger S Lasken, Benjamin Janto, Justin Hogg, Paul Stoodley, Robert Boissy, Garth D Ehrlich
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-09-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.0050230
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spelling doaj-8d6e290729054f6eabf6463e1f80dd962021-07-02T17:10:22ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852007-09-0159e23010.1371/journal.pbio.0050230Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.Marc MussmannFen Z HuMichael RichterDirk de BeerAndré PreislerBo B JørgensenMarcel HuntemannFrank Oliver GlöcknerRudolf AmannWerner J H KoopmanRoger S LaskenBenjamin JantoJustin HoggPaul StoodleyRobert BoissyGarth D EhrlichMarine 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.https://doi.org/10.1371/journal.pbio.0050230
collection DOAJ
language English
format Article
sources DOAJ
author Marc Mussmann
Fen Z Hu
Michael Richter
Dirk de Beer
André Preisler
Bo B Jørgensen
Marcel Huntemann
Frank Oliver Glöckner
Rudolf Amann
Werner J H Koopman
Roger S Lasken
Benjamin Janto
Justin Hogg
Paul Stoodley
Robert Boissy
Garth D Ehrlich
spellingShingle Marc Mussmann
Fen Z Hu
Michael Richter
Dirk de Beer
André Preisler
Bo B Jørgensen
Marcel Huntemann
Frank Oliver Glöckner
Rudolf Amann
Werner J H Koopman
Roger S Lasken
Benjamin Janto
Justin Hogg
Paul Stoodley
Robert Boissy
Garth D Ehrlich
Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
PLoS Biology
author_facet Marc Mussmann
Fen Z Hu
Michael Richter
Dirk de Beer
André Preisler
Bo B Jørgensen
Marcel Huntemann
Frank Oliver Glöckner
Rudolf Amann
Werner J H Koopman
Roger S Lasken
Benjamin Janto
Justin Hogg
Paul Stoodley
Robert Boissy
Garth D Ehrlich
author_sort Marc Mussmann
title Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
title_short Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
title_full Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
title_fullStr Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
title_full_unstemmed Insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
title_sort insights into the genome of large sulfur bacteria revealed by analysis of single filaments.
publisher Public Library of Science (PLoS)
series PLoS Biology
issn 1544-9173
1545-7885
publishDate 2007-09-01
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.
url https://doi.org/10.1371/journal.pbio.0050230
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