Genomic analysis reveals versatile heterotrophic capacity of a potentially symbiotic sulfur-oxidizing bacterium in sponge

Handle URI:
http://hdl.handle.net/10754/563720
Title:
Genomic analysis reveals versatile heterotrophic capacity of a potentially symbiotic sulfur-oxidizing bacterium in sponge
Authors:
Tian, Renmao; Wang, Yong; Bougouffa, Salim ( 0000-0001-9218-6452 ) ; Gao, Zhaoming; Cai, Lin; Bajic, Vladimir B. ( 0000-0001-5435-4750 ) ; Qian, Peiyuan
Abstract:
Sulfur-reducing bacteria (SRB) and sulfur-oxidizing bacteria (SOB) play essential roles in marine sponges. However, the detailed characteristics and physiology of the bacteria are largely unknown. Here, we present and analyse the first genome of sponge-associated SOB using a recently developed metagenomic binning strategy. The loss of transposase and virulence-associated genes and the maintenance of the ancient polyphosphate glucokinase gene suggested a stabilized SOB genome that might have coevolved with the ancient host during establishment of their association. Exclusive distribution in sponge, bacterial detoxification for the host (sulfide oxidation) and the enrichment for symbiotic characteristics (genes-encoding ankyrin) in the SOB genome supported the bacterial role as an intercellular symbiont. Despite possessing complete autotrophic sulfur oxidation pathways, the bacterium developed a much more versatile capacity for carbohydrate uptake and metabolism, in comparison with its closest relatives (Thioalkalivibrio) and to other representative autotrophs from the same order (Chromatiales). The ability to perform both autotrophic and heterotrophic metabolism likely results from the unstable supply of reduced sulfur in the sponge and is considered critical for the sponge-SOB consortium. Our study provides insights into SOB of sponge-specific clade with thioautotrophic and versatile heterotrophic metabolism relevant to its roles in the micro-environment of the sponge body. © 2014 Society for Applied Microbiology and John Wiley & Sons Ltd.
KAUST Department:
Computational Bioscience Research Center (CBRC); Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division; Applied Mathematics and Computational Science Program
Publisher:
Wiley-Blackwell
Journal:
Environmental Microbiology
Issue Date:
29-Aug-2014
DOI:
10.1111/1462-2920.12586
Type:
Article
ISSN:
14622912
Sponsors:
This study was supported by grants from the Nature Science Foundation of China (U1301232), the 'Strategic Priority Research Program' of the Chinese Academy of Sciences (XDB06010100 and XDB06010200), the SKLMP Seed Collaborative Research fund (CITYU12SC01) and an award from King Abdullah University of Science and Technology (SA-C0040/UK-C0016).
Appears in Collections:
Articles; Applied Mathematics and Computational Science Program; Computational Bioscience Research Center (CBRC); Computer, Electrical and Mathematical Sciences and Engineering (CEMSE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorTian, Renmaoen
dc.contributor.authorWang, Yongen
dc.contributor.authorBougouffa, Salimen
dc.contributor.authorGao, Zhaomingen
dc.contributor.authorCai, Linen
dc.contributor.authorBajic, Vladimir B.en
dc.contributor.authorQian, Peiyuanen
dc.date.accessioned2015-08-03T12:07:43Zen
dc.date.available2015-08-03T12:07:43Zen
dc.date.issued2014-08-29en
dc.identifier.issn14622912en
dc.identifier.doi10.1111/1462-2920.12586en
dc.identifier.urihttp://hdl.handle.net/10754/563720en
dc.description.abstractSulfur-reducing bacteria (SRB) and sulfur-oxidizing bacteria (SOB) play essential roles in marine sponges. However, the detailed characteristics and physiology of the bacteria are largely unknown. Here, we present and analyse the first genome of sponge-associated SOB using a recently developed metagenomic binning strategy. The loss of transposase and virulence-associated genes and the maintenance of the ancient polyphosphate glucokinase gene suggested a stabilized SOB genome that might have coevolved with the ancient host during establishment of their association. Exclusive distribution in sponge, bacterial detoxification for the host (sulfide oxidation) and the enrichment for symbiotic characteristics (genes-encoding ankyrin) in the SOB genome supported the bacterial role as an intercellular symbiont. Despite possessing complete autotrophic sulfur oxidation pathways, the bacterium developed a much more versatile capacity for carbohydrate uptake and metabolism, in comparison with its closest relatives (Thioalkalivibrio) and to other representative autotrophs from the same order (Chromatiales). The ability to perform both autotrophic and heterotrophic metabolism likely results from the unstable supply of reduced sulfur in the sponge and is considered critical for the sponge-SOB consortium. Our study provides insights into SOB of sponge-specific clade with thioautotrophic and versatile heterotrophic metabolism relevant to its roles in the micro-environment of the sponge body. © 2014 Society for Applied Microbiology and John Wiley & Sons Ltd.en
dc.description.sponsorshipThis study was supported by grants from the Nature Science Foundation of China (U1301232), the 'Strategic Priority Research Program' of the Chinese Academy of Sciences (XDB06010100 and XDB06010200), the SKLMP Seed Collaborative Research fund (CITYU12SC01) and an award from King Abdullah University of Science and Technology (SA-C0040/UK-C0016).en
dc.publisherWiley-Blackwellen
dc.titleGenomic analysis reveals versatile heterotrophic capacity of a potentially symbiotic sulfur-oxidizing bacterium in spongeen
dc.typeArticleen
dc.contributor.departmentComputational Bioscience Research Center (CBRC)en
dc.contributor.departmentComputer, Electrical and Mathematical Sciences and Engineering (CEMSE) Divisionen
dc.contributor.departmentApplied Mathematics and Computational Science Programen
dc.identifier.journalEnvironmental Microbiologyen
dc.contributor.institutionDivison of Life Science, Hong Kong University of Science and Technology, Hong Kongen
dc.contributor.institutionSanya Institute of Deep Sea Science and Engineering, Chinese Academy of SciencesSan Ya, Hai Nan, Chinaen
kaust.authorBougouffa, Salimen
kaust.authorBajic, Vladimir B.en
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