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

Renmao Tian, Yong Wang, Salim Bougouffa, Zhaoming Gao, Lin Cai, Vladimir B. Bajic, Pei-Yuan Qian

Research output: Contribution to journalArticlepeer-review

39 Scopus citations

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.
Original languageEnglish (US)
Pages (from-to)3548-3561
Number of pages14
JournalEnvironmental Microbiology
Volume16
Issue number11
DOIs
StatePublished - Aug 29 2014

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: 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).

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Microbiology

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