Advertisement

Polar Biology

, Volume 40, Issue 11, pp 2335–2342 | Cite as

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

  • Jane L. Heywood
  • Chong Chen
  • David A. Pearce
  • Katrin Linse
Original Paper

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.

Keywords

Symbiont Hydrothermal vent Gastropod Antarctic Chemosynthesis Microbial diversity 

Notes

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).

Supplementary material

300_2017_2148_MOESM1_ESM.xlsx (15 kb)
Supplementary material 1 (XLSX 15 kb) 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

References

  1. Arango CP, Linse K (2015) New Sericosura (Pycnogonida: Ammotheidae) from deep-sea hydrothermal vents in the Southern Ocean. Zootaxa 3995:037–050. doi: 10.11646/zootaxa.3995.1.5 CrossRefGoogle Scholar
  2. Buckeridge JS, Linse K, Jackson JA (2013) Vulcanolepas scotiaensis sp. Nov., a new deep-sea scalpelliform barnacle (Eolepadidae: Neolepadinae) from hydrothermal vents in the Scotia Sea, Antarctica. Zootaxa 3745:551–568. doi: 10.11646/zootaxa.3745.5.4 CrossRefPubMedGoogle Scholar
  3. Campbell BJ, Cary SC (2004) Abundance of reverse tricarboxylic acid cycle genes in free-living microorganisms at deep sea hydrothermal vents. Appl Environ Microbiol 70(10):6282–6289. doi: 10.1128/AEM.70.10.6282-6289.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Campbell BJ, Stein JL, Cary SC (2003) Evidence of chemolithoautotrophy in the bacterial community associated with Alvinella pompejana, a hydrothermal vent polychaete. Appl Environ Microbiol 69(9):5070–5080. doi: 10.1128/AEM.69.9.5070-5078.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch JW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342. doi: 10.1126/science.213.4505.340 CrossRefPubMedGoogle Scholar
  6. Cavanaugh CM, McKiness ZP, Newton ILG, Stewart FJ (2006) Marine chemosynthetic symbioses. In: Dworkin M et al (ed) The prokaryotes. A handbook on the biology of Bacteria. Vol 1 symbiotic associations, biotechnology and applied microbiology, 3rd Ed. Springer, New York, pp 475–507. doi:  10.1007/0-387-30741-9_18
  7. Chen C, Copley JT, Linse K, Rogers AD, Sigwart JD (2015a) The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system. Front Zool 12:13. doi: 10.1186/s12983-015-0105-1 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chen C, Linse K, Copley JT, Rogers AD (2015b) The ‘scaly-foot gastropod’: a new genus and species of hydrothermal vent-endemic gastropod (Neomphalina: Peltospiridae) from the Indian Ocean. J Mollus Stud 81:322–334. doi: 10.1093/mollus/eyv013 CrossRefGoogle Scholar
  9. Chen C, Linse K, Roterman CN, Copley JT, Rogers AD (2015c) A new genus of large hydrothermal vent-endemic gastropod (Neomphalina: Peltospiridae). Zool J Linn Soc Lond 175:319–335. doi: 10.1111/zoj.12279 CrossRefGoogle Scholar
  10. Chen C, Uematsu K, Linse K, Sigwart JD (2017) By more ways than one: rapid convergence at hydrothermal vents shown by 3D anatomical reconstruction of Gigantopelta (Mollusca: Neomphalina). BMC Evol Biol 17:62. doi: 10.1186/s12862-017-0917-z CrossRefPubMedPubMedCentralGoogle Scholar
  11. Collins RE, Rocap G (2007) REPK: an analytical web server to select restriction endonucleases for terminal restriction fragment length polymorphism analysis. Nucleic Acids Res 35:W58–W62. doi: 10.1093/nar/gkm384 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0Google Scholar
  13. Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740. doi: 10.1038/nrmicro1992 CrossRefPubMedGoogle Scholar
  14. Felbeck H, Childress JJ, Somero GN (1981) Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature 293:291–293. doi: 10.1038/293291a0 CrossRefGoogle Scholar
  15. Goffredi SK, Waren A, Orphan VJ, Van Dover CL, Vrijenhoek RC (2004) Novel forms of structural integration between microbes and a hydrothermal vent gastropod from the Indian Ocean. Appl Environ Microbiol 70(5):3082–3090. doi: 10.1128/AEM.70.5.3082-3090.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  17. Marsh L, Copley JT, Huvenne VAI, Linse K, Reid WDK, Rogers AD, Sweeting CJ, Tyler PA (2012) Microdistribution of faunal assemblages at deep-sea hydrothermal vents in the Southern Ocean. PLoSOne 7(10):e48348. doi: 10.1371/journal.pone.0048348 CrossRefGoogle Scholar
  18. Nakagawa S, Shimamura S, Takaki Y, Suzuki Y, Murakami S, Watanabe T, Fujiyoshi S, Mino S, Sawabe T, Maeda T, Makita H, Nemoto S, Nishimura S, Watanabe H, Watsuji T, Takai K (2014) Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont. ISME J 8:40–51. doi: 10.1038/ismej.2013.131 CrossRefPubMedGoogle Scholar
  19. Reid WDK, Sweeting CJ, Wigham BD, Zwirglmaier K, Hawkes JA, McGill RAR, Linse K, Polunin NVC (2013) Spatial differences in East Scotia Ridge hydrothermal vent food webs: influences of chemistry, microbiology and predation on trophodynamics. PLoS ONE 9(6):e65553. doi: 10.1371/journal.pone.006553 CrossRefGoogle Scholar
  20. Rogers AD, Tyler PA, Connelly DP, Copley JT, James R, Later RD, Linse K, Mills RA, Garabato AN, Pancost RD, Pearce DA, Polunin NV, German CR, Shank T, Boersch-Supan PH, Alker BJ, Aquilina A, Bennett SA, Clarke A, Dinley RJ, Graham AG, Green DR, Hawkes JA, Hepburn L, Hilario A, Huvenne VA, Marsh L, Ramirez-Llodra E, Reid WD, Roterman CN, Sweeting CJ, Thatje S, Zwirglmaier K (2012) The discovery of new deep-sea hydrothermal vent communities in the Southern Ocean and implications for biogeography. PLoS Biol 10(1):e1001234. doi: 10.1371/journal.pbio.1001234 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. doi: 10.1128/AEM.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Stein JL, Cary C, Hessler RR, Ohta S, Vetter RD, Childress JJ, Felbeck H (1988) Chemoautotrophic symbiosis in a hydrothermal vent gastropod. Biol Bull 174:373–378. doi: 10.2307/1541963 CrossRefGoogle Scholar
  23. Suzuki Y, Sasaki T, Susuki M, Nogi Y, Miwa T, Takai K, Nealson KH, Horikoshi K (2005) Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl Environ Microbiol 71(9):5440–5450. doi: 10.1128/AEM.71.9.5440-5450.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Suzuki Y, Kojima S, Sasaki T, Suzuki M, Utsumi T, Watanabe H, Urakawa H, Tsuchida S, Nunoura T, Hirayama H, Takai K, Nealson KH, Horikoshi K (2006) Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Appl Environ Microbiol 72(2):1388–1393. doi: 10.1128/AEM.72.2.1388-1393.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi: 10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Thatje S, Marsh L, Roterman CN, Mavrogordato MN, Linse K (2015) Adaptations to hydrothermal vent life in Kiwa tyleri, a new species of yeti crab from the East Scotia Ridge, Antarctica. PLoS ONE 10(6):e0127621. doi: 10.1371/journal.pone.0127621 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267. doi: 10.1128/AEM.00062-07 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Warén A, Bengtson S, Goffredi SK, Van Dover CL (2003) A hot-vent gastropod with iron sulfide dermal sclerites. Science 302:1007. doi: 10.1126/science.1087696 CrossRefPubMedGoogle Scholar
  29. Zwirglmaier K, Reid W, Heywood J, Sweeting CJ, Wigham BD, Polunin NV, Hawkes JA, Connelly DP, Pearce D, Linse K (2015) Linking regional variation of epibiotic bacterial diversity and trophic ecology in a new species of Kiwaidae (Decapoda, Anomura) from East Scotia Ridge (Antarctica) hydrothermal vents. Microbiol Open 4(1):136–150. doi: 10.1002/mbo3.227 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Jane L. Heywood
    • 1
    • 3
  • Chong Chen
    • 2
  • David A. Pearce
    • 1
    • 4
  • Katrin Linse
    • 1
  1. 1.British Antarctic SurveyCambridgeUK
  2. 2.Department of Subsurface Geobiological Analysis and ResearchJapan Agency for Marine-Earth Science and TechnologyYokosukaJapan
  3. 3.Kent and Essex Inshore Fisheries and Conservation AuthorityEssexUK
  4. 4.Northumbria UniversityNewcastle upon TyneUK

Personalised recommendations