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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2007-09-01
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Online Access: | https://doi.org/10.1371/journal.pbio.0050230 |
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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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