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Polar Biology

, Volume 42, Issue 12, pp 2305–2312 | Cite as

Bacterial endosymbiont of Oligobrachia sp. (Frenulata) from an active mud volcano in the Canadian Beaufort Sea

  • Yung Mi LeeEmail author
  • Hyun-Ju Noh
  • Dong-Hun Lee
  • Jung-Hyun Kim
  • Young Keun Jin
  • Charles Paull
Short Note
  • 55 Downloads

Abstract

Siboglinid tubeworms of the genus Oligobrachia that thrive in obligatory association with endosymbionts have been predominantly observed in Arctic and high-latitude Atlantic cold seeps. Metabolic features of endosymbionts provide fundamental understanding for the survival strategy of tubeworms in cold seeps. However, no information on the bacterial endosymbionts of tubeworms from the Canadian Beaufort Sea has been available until now. In this study, we investigated the phylogeny and metabolic potential of a bacterial endosymbiont of siboglinid tubeworms from an active mud volcano in the Canadian Beaufort Sea using Illumina MiSeq sequencing of 16S rRNA gene amplicons. The siboglinid tubeworm shared 99.9% 18S rRNA gene sequence similarity with Oligobrachia haakonmosbiensis and 99.7–99.8% mitochondrial cytochrome C oxidase subunit I gene similarity with members of Oligobrachia sp. CPL-clade and was designated ‘Oligobrachia sp. BS1.’ The endosymbiont of Oligobrachia sp. BS1, which belongs to the Gammaproteobacteria, was most closely related to endosymbionts of Oligobrachia sp. CPL-clade, revealing the close relationships between the endosymbionts and their hosts. The bacterial endosymbiont of Oligobrachia sp. BS1 contained the key gene required for sulfur oxidation, aprA gene encoding the α-subunit of adenosine 1,5-phosphosulfate reductase, suggesting that this endosymbiont is capable of using sulfide as an energy source. The bacterial endosymbiont of an Oligobrachia species from an active mud volcano in the Canadian Beaufort Sea presented here expands our knowledge of the identities and thiotrophic metabolism of endosymbionts that are associated with hosts that dominate a wide range of methane seep habitats in the Arctic.

Keywords

Siboglinid tubeworm Oligobrachia Endosymbiont Canadian Beaufort Sea Arctic aprA gene 

Notes

Acknowledgements

This research was supported by the Korea Polar Research Institute (Grant Nos. PM17050 and PM19050), the Korea Institute of Marine Science and Technology Promotion (Grant No. 20160247), and the David and Lucile Packard Foundation. We thank the captain and crew of RV ARAON for their support at sea. We are very grateful to Dale Graves, Frank Flores, and Roberto Gwiazda at Monterey Bay Aquarium Research Institute for the operation of the remotely operated vehicle and sample collection. We also thank Yeonjin Choi, Sang-Hee Kim, and Binu M. Tripathi of the Korea Polar Research Institute for providing maps, help in removing the worms from tubes, and stimulating discussions. We thank Janine Miller, PhD, from Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript.

Compliance with ethical standards

Conflict of interests

There are no conflicts of interest to declare.

Supplementary material

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References

  1. Blazejak A, Kuever J, Erséus C, Amann R, Dubilier N (2006) Phylogeny of 16S rRNA, ribulose 1,5-bisphosphate carboxylase/oxygenase, and adenosine 5′-phosphosulfate reductase genes from gamma- and alphaproteobacterial symbionts in gutless marine worms (Oligochaeta) from Bermuda and the Bahamas. Appl Environ Microbiol 72:5527–5536.  https://doi.org/10.1128/aem.02441-05 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Cavanaugh CM (1985) Symbioses of chemoautotrophic bacteria and marine invertebrates from hydrothermal vents and reducing sediments. Biol Soc Wash Bull 6:373–388Google Scholar
  3. Cavanaugh CM, Wirsen CO, Jannasch HW (1992) Evidence for methylotrophic symbionts in a hydrothermal vent mussel (Bivalvia: Mytilidae) from the mid-Atlantic ridge. Appl Environ Microbiol 58:3799–3803PubMedPubMedCentralGoogle Scholar
  4. Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074PubMedPubMedCentralGoogle Scholar
  5. Dando PR, Southward AJ, Southward EC, Barrett RL (1986) Possible energy sources for chemoautotrophic prokaryotes symbiotic with invertebrates from a Norwegian fjord. Ophelia 26:135–150.  https://doi.org/10.1080/00785326.1986.10421984 CrossRefGoogle Scholar
  6. Dando PR, Southward AJ, Southward EC, Lamont P, Harvey R (2008) Interactions between sediment chemistry and frenulate pogonophores (Annelida) in the north-east Atlantic. Deep-Sea Res PT I 55:966–996CrossRefGoogle Scholar
  7. Duperron S, Beer DD, Zbinden M, Boetius A, Schipani V, Kahil N, Gaill F (2009) Molecular characterization of bacteria associated with the trophosome and the tube of Lamellibrachia sp., a siboglinid annelid from cold seeps in the eastern Mediterranean. FEMS Microbiol Ecol 69:395–409.  https://doi.org/10.1111/j.1574-6941.2009.00724.x CrossRefPubMedGoogle Scholar
  8. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200.  https://doi.org/10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Felbeck H (1981) Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera). Science 213:336–338CrossRefGoogle Scholar
  10. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376.  https://doi.org/10.1007/bf01734359 CrossRefPubMedGoogle Scholar
  11. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  12. Halanych KM (2005) Molecular phylogeny of siboglinid annelids (a.k.a. pogonophorans): a review. Hydrobiologia 535:297–307.  https://doi.org/10.1007/s10750-004-1437-6 CrossRefGoogle Scholar
  13. Halanych KM, Feldman RA, Vrijenhoek RC (2001) Molecular evidence that Sclerolinum brattstromi is closely related to vestimentiferans, not to frenulate pogonophorans (Siboglinidae, Annelida). Biol Bull 201:65–75.  https://doi.org/10.2307/1543527 CrossRefPubMedGoogle Scholar
  14. Hilário A, Capa M, Dahlgren TG, Halanych KM, Little CTS, Thornhill DJ, Verna C, Glover AG (2011) New perspectives on the ecology and evolution of siboglinid tubeworms. PLoS ONE 6(2):e16309.  https://doi.org/10.1371/journal.pone.0016309 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Kimura H, Sato M, Sasayama Y, Naganuma T (2003) Molecular characterization and in situ localization of endosymbiotic 16S ribosomal RNA and RuBisCO genes in the Pogonophoran tissue. Mar Biotechnol 5:261–269.  https://doi.org/10.1007/s10126-002-0073-2 CrossRefPubMedGoogle Scholar
  16. Kubota N, Kanemori M, Sasayama Y, Aida M, Fukumori Y (2007) Identification of endosymbionts in Oligobrachia mashikoi (Siboglinidae, Annelida). Microbes Environ 22:136–144.  https://doi.org/10.1264/jsme2.22.136 CrossRefGoogle Scholar
  17. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549CrossRefGoogle Scholar
  18. Lee D-H, Kim J-H, Lee YM, Jin YK, Paull C, Kim D, Shin K-H (2019) Chemosynthetic bacterial signatures in Frenulata tubeworm Oligobrachia sp. in an active mud volcano of the Canadian Beaufort Sea. Mar Ecol Prog Ser 628:95–104.  https://doi.org/10.3354/meps13084 CrossRefGoogle Scholar
  19. López-García P, Gaill F, Moreira D (2002) Wide bacterial diversity associated with tubes of the vent worm Riftia pachyptila. Environ Microbiol 4:204–215.  https://doi.org/10.1046/j.1462-2920.2002.00286.x CrossRefPubMedGoogle Scholar
  20. Lösekann T, Robador A, Niemann H, Knittel K, Boetius A, Dubilier N (2008) Endosymbioses between bacteria and deep-sea siboglinid tubeworms from an Arctic cold seep (Haakon Mosby Mud Volcano, Barents Sea). Environ Microbiol 10:3237–3254.  https://doi.org/10.1111/j.1462-2920.2008.01712.x CrossRefPubMedGoogle Scholar
  21. Masella AP, Bartram AK, Truszkowski JM, Brown DG, Neufeld JD (2012) PANDAseq: paired-end assembler for illumina sequences. BMC Bioinform 13:31.  https://doi.org/10.1186/1471-2105-13-31 CrossRefGoogle Scholar
  22. Naganuma T, Elsaied HE, Hoshii D, Kimura H (2005) Bacterial endosymbioses of gutless tube-dwelling worms in nonhydrothermal vent habitats. Mar Biotechnol 7:416–428.  https://doi.org/10.1007/s10126-004-5089-3 CrossRefPubMedGoogle Scholar
  23. Nikolenko SI, Korobeynikov AI, Alekseyev MA (2013) BayesHammer: Bayesian clustering for error correction in single-cell sequencing. BMC Genomics 14:S7.  https://doi.org/10.1186/1471-2164-14-s1-s7 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Paull CK, Dallimore SR, Caress DW, Gwiazda R, Melling H, Riedel M, Jin YK, Hong JK, Kim Y-G, Graves D, Sherman A, Lundsten E, Anderson K, Lundsten L, Villinger H, Kopf A, Johnson SB, Hughes-Clarke J, Blasco S, Conway K, Neelands P, Thomas H, Côté M (2015) Active mud volcanoes on the continental slope of the Canadian Beaufort Sea. Geochem Geophys Geosyst 16:3160–3181.  https://doi.org/10.1002/2015gc005928 CrossRefGoogle Scholar
  25. Rodrigues CF, Hilário A, Cunha MR, Weightman AJ, Webster G (2011) Microbial diversity in Frenulata (Siboglinidae, Polychaeta) species from mud volcanoes in the Gulf of Cadiz (NE Atlantic). Antonie Van Leeuwenhoek 100:83–98.  https://doi.org/10.1007/s10482-011-9567-0 CrossRefPubMedGoogle Scholar
  26. Schirmer M, Ijaz UZ, D'Amore R, Hall N, Sloan WT, Quince C (2015) Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform. Nucleic Acids Res 43:e37.  https://doi.org/10.1093/nar/gku1341 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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 75:7537–7541.  https://doi.org/10.1128/aem.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Sen A, Duperron S, Hourdez S, Piquet B, Léger N, Gebruk A, Le Port A-S, Svenning MM, Andersen AC (2018) Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps. PLoS ONE 13:e0209273.  https://doi.org/10.1371/journal.pone.0209273 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Smirnov RV (2000) Two new species of Pogonophora from the Arctic mud volcano off northwestern Norway. Sarsia 85:141–150.  https://doi.org/10.1080/00364827.2000.10414563 CrossRefGoogle Scholar
  30. Southward AJ, Southward EC, Dando PR, Barrett RL, Ling R (1986) Chemoautotrophic function of bacterial symbionts in small Pogonophora. J Mar Biol Assoc UK 66:415–437.  https://doi.org/10.1017/S0025315400043046 CrossRefGoogle Scholar
  31. Stewart FJ, Newton ILG, Cavanaugh CM (2005) Chemosynthetic endosymbioses: adaptations to oxic–anoxic interfaces. Trends Microbiol 13:439–448.  https://doi.org/10.1016/j.tim.2005.07.007 CrossRefPubMedGoogle Scholar
  32. Thornhill DJ, Wiley AA, Campbell AL, Bartol FF, Teske A, Halanych KM (2008) Endosymbionts of Siboglinum fiordicum and the phylogeny of bacterial endosymbionts in Siboglinidae (Annelida). Biol Bull 214:135–144.  https://doi.org/10.2307/25066670 CrossRefPubMedGoogle Scholar
  33. Wada H, Satoh N (1994) Phylogenetic relationships among extant classes of echinoderms, as inferred from sequences of 18S rDNA, coincide with relationships deduced from the fossil record. J Mol Evol 38:41–49.  https://doi.org/10.1007/bf00175494 CrossRefPubMedGoogle Scholar
  34. Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, Gilbert JA, Jansson JK, Caporaso JG, Fuhrman JA, Apprill A, Knight R (2016) Improved bacterial 16S rRNA gene (V4 and V4–5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1:e00009–e000015.  https://doi.org/10.1128/mSystems.00009-15 CrossRefPubMedGoogle Scholar
  35. Winnepenninckx B, Backeljau T, Wachter RD (1995) Phylogeny of protostome worms derived from 18S rRNA sequences. Mol Biol Evol 12:641–649.  https://doi.org/10.1093/oxfordjournals.molbev.a040243 CrossRefPubMedGoogle Scholar
  36. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617.  https://doi.org/10.1099/ijsem.0.001755 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yung Mi Lee
    • 1
    Email author
  • Hyun-Ju Noh
    • 1
    • 2
  • Dong-Hun Lee
    • 3
  • Jung-Hyun Kim
    • 1
  • Young Keun Jin
    • 1
  • Charles Paull
    • 4
  1. 1.Division of Polar Life SciencesKorea Polar Research InstituteIncheonRepublic of Korea
  2. 2.Inha UniversityIncheonRepublic of Korea
  3. 3.Hanyang UniversityAnsanRepublic of Korea
  4. 4.Monterey Bay Aquarium Research InstituteMoss LandingUSA

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