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Insights into the genome of large sulfur bacteria revealed by analysis of single filaments

Insights into the genome of large sulfur bacteria revealed by analysis of single filaments
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 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.
e230
Mussmann, Marc
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Hu, Fen Z.
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Richter, Michael
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de Beer, Dirk
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Preisler, André
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Jørgensen, Bo B.
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Huntemann, Marcel
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Glöckner, Frank Oliver
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Amann, Rudolf
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Koopman, Werner J.H.
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Lasken, Roger S.
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Janto, Benjamin
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Hogg, Justin
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Stoodley, Paul
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Boissy, Robert
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Ehrlich, Garth D.
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Mussmann, Marc
b848dff4-9d37-4bfc-bbcf-50bfd7e0590b
Hu, Fen Z.
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Richter, Michael
f0acb344-7651-4c1d-b401-7e1f46b92d6b
de Beer, Dirk
cb8d8130-86eb-4ecb-9496-41543e1fe536
Preisler, André
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Jørgensen, Bo B.
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Huntemann, Marcel
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Glöckner, Frank Oliver
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Amann, Rudolf
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Koopman, Werner J.H.
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Lasken, Roger S.
ec8ad94b-bcd9-4ddd-bb2d-e937b8d45e8b
Janto, Benjamin
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Hogg, Justin
a046be1a-2be9-4b2f-96a3-b0e83b817c26
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f
Boissy, Robert
305ae798-afc8-4123-9a07-889aa1d41dd4
Ehrlich, Garth D.
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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 and Ehrlich, Garth D. (2007) Insights into the genome of large sulfur bacteria revealed by analysis of single filaments. PLoS Biology, 5 (9), e230. (doi:10.1371/journal.pbio.0050230).

Record type: Article

Abstract

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.

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Published date: September 2007
Organisations: Engineering Mats & Surface Engineerg Gp

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Local EPrints ID: 157167
URI: http://eprints.soton.ac.uk/id/eprint/157167
PURE UUID: 03aab1d3-f320-4511-b832-82f203cebb0f
ORCID for Paul Stoodley: ORCID iD orcid.org/0000-0001-6069-273X

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Date deposited: 03 Jun 2010 13:45
Last modified: 14 Mar 2024 02:55

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Contributors

Author: Marc Mussmann
Author: Fen Z. Hu
Author: Michael Richter
Author: Dirk de Beer
Author: André Preisler
Author: Bo B. Jørgensen
Author: Marcel Huntemann
Author: Frank Oliver Glöckner
Author: Rudolf Amann
Author: Werner J.H. Koopman
Author: Roger S. Lasken
Author: Benjamin Janto
Author: Justin Hogg
Author: Paul Stoodley ORCID iD
Author: Robert Boissy
Author: Garth D. Ehrlich

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