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Bacterial communities associated with the Southern Ocean vent gastropod, Gigantopelta chessoia: indication of horizontal symbiont transfer

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Abstract

Recently discovered hydrothermal vents of the East Scotia Ridge (ESR) in the Southern Ocean host unique faunal communities that depend on microbial chemosynthetic primary production. These highly abundant invertebrates gain energy from either grazing on free-living microbes or via hosting symbiotic chemoautotrophic microorganisms. The main objective of this study was to characterise microbes associated with a newly discovered species of hydrothermal vent gastropod and therefore increase knowledge of ecosystem functioning in this largely unknown Antarctic hydrothermal vent system. We investigated the phylogenetic composition of bacteria associated with the gills and oesophageal gland of the ESR peltospirid gastropod, Gigantopelta chessoia by molecular cloning and terminal restriction fragment length polymorphism (T-RFLP). 16S rRNA gene clone libraries revealed host tissue-specific combinations of bacteria. The oesophageal gland contained one Gammaproteobacteria OTU whereas a more diverse community of Gamma, Epsilon and Deltaproteobacteria was isolated from the gills. T-RFLP analysis revealed that juvenile bacterial communities were more closely related to adult gill-associated bacterial communities than oesophageal gland bacteria. Oesophageal gland Gammaproteobacteria exhibited a higher sequence similarity with sulphur-oxidising bacteria isolated from cold seep sediments and with thioautotrophic endosymbionts than with bacteria found in the surrounding water column, suggesting that these endosymbionts were not acquired directly from the water column. Juvenile G. chessoia were located within the mantle cavity of adults and we speculate that Gammaproteobacterial endosymbionts in the oesophageal gland could be transmitted horizontally from adults to juveniles via the gills due to the close contact of juveniles with adults’ gills.

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Acknowledgements

The authors would like to thank the principal scientist of JC80 Prof. P. Tyler, the Master and crew of the RRS James Cook as well as the team of technicians of the ROV Isis. The Natural Environment Research Council (NERC) funded the study through the ChEsSO—Chemosynthetically driven ecosystems south of the Polar Front: biogeography and ecology consortium grant (grant number NE/D01249x/1).

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Author notes

  1. Jane L. Heywood

    Present address: Kent and Essex Inshore Fisheries and Conservation Authority, The Sail Loft, Brightlingsea, Essex, CO7 0AR, UK

  2. David A. Pearce

    Present address: Northumbria University, Newcastle City Campus, Newcastle upon Tyne, NE1 8ST, UK

Authors and Affiliations

  1. British Antarctic Survey, High Cross, Cambridge, CB3 0ET, UK

    Jane L. Heywood, David A. Pearce & Katrin Linse

  2. Department of Subsurface Geobiological Analysis and Research, Japan Agency for Marine-Earth Science and Technology, Yokosuka, Kanagawa, 237-0061, Japan

    Chong Chen

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  1. Jane L. Heywood
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Correspondence to Jane L. Heywood.

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Online Resource 1 Taxonomic classification of 16S rRNA gene sequences from gill and oesophageal gland-associated bacterial clone libraries as determined by RDP Classifier (Wang et al. 2007). Classifications with a confidence estimate of above 80% were used

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Heywood, J.L., Chen, C., Pearce, D.A. et al. Bacterial communities associated with the Southern Ocean vent gastropod, Gigantopelta chessoia: indication of horizontal symbiont transfer. Polar Biol 40, 2335–2342 (2017). https://doi.org/10.1007/s00300-017-2148-6

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  • DOI: https://doi.org/10.1007/s00300-017-2148-6

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