Skip to main content
SpringerLink
Log in

Phylogenetic relationship between symbionts of tubeworm Lamellibrachia satsuma and the sediment microbial community in Kagoshima Bay

  • Article
  • Published:
Ocean Science Journal Aims and scope Submit manuscript

Abstract

Vestimentiferan tubeworms acquire their symbionts through horizontal transmission from the surrounding environment. In the present study, we constructed a 16S rRNA gene clone library to investigate the phylogenetic relationship between diverse microbes in the sediment and symbiotic bacteria in the trophosome of the tubeworm, Lamellibrachia satsuma, from Kagoshima Bay, Japan. Two symbiotic bacterial phylotypes belonging to the classes γ- and ε-Proteobacteria were found from this tubeworm trophosome. They were very closely related to the symbionts of several other marine invertebrates. The most predominant bacteria in the sediment were ε-Proteobacteria. A broad diversity of bacteria belonged to non-proteobacterial phyla such as Planctomycetes, Acidobacteria, and Chloroflexi was observed. The presence of sulfur oxidizers (i.e., ε-Proteobacteria and γ-Proteobacteria) and sulfur reducers (i.e., δ-Proteobacteria) may play a significant role in the sulfur cycle in these habitats and provide multiple sources of nutrition to the cold-seep communities. Closely related clones of ε-Proteobacteria symbiont in the species level and of γ-Proteobacteria symbiont in the genus level were found in the surrounding sediment. The similarity of symbiont clones of L. satsuma with other symbionts and free-living bacteria suggests the possibility of opportunistic symbiosis in ε-Proteobacteria and the co-evolution of γ-Proteobacteria having occurred after symbiosis with the tubeworms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Acosta GA, Rosselló MR, Marqués S (2013) Characterization of the anaerobic microbial community in oil polluted subtidal sediments: aromatic biodegradation potential after the Prestige oil spill. Environ Microbiol 15:77–92

    Article  Google Scholar 

  • Arakawa S, Sato T, Yoshida Y, Usami R, Kato C (2006) Comparison of the microbial diversity in cold seep sediments from different depths in the Nankai Trough. J Gen Appl Microbiol 52:47–54

    Article  Google Scholar 

  • Barns SM, Fundyga RE, Jeffries MW, Pace NR (1994) Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. P Natl Acad Sci USA 91:1609–1613

    Article  Google Scholar 

  • Beal EJ, House CH, Orpan VJ (2009) Manganese- and iron-dependent marine methane oxidation. Science 325:184–187

    Article  Google Scholar 

  • Beatty JT, Overmann J, Lince MT, Manske AK, Lang AS, Blankenship RE, Van Dover CL, Martinson TA, Plumley FG (2005) An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. P Natl Acad Sci USA 102:9306–9310

    Article  Google Scholar 

  • Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8:218–230

    Article  Google Scholar 

  • Byrne N, Lesongeur F, Bienvenu N, Geslin C, Alain K, Prieur D, Godfroy A (2009) Effect of variation of environmental conditions on the microbial communities of deep-sea vent chimneys, cultured in a bioreactor. Extremophiles 13:595–608

    Article  Google Scholar 

  • Campbell BJ, Jeanthon C, Kostka JE, Luther GW, Cary SC (2001) Growth and phylogenetic properties of novel bacteria belonging to the epsilon subdivision of the Proteobacteria enriched from Alvinella pompejana and deep-sea hydrothermal vents. Appl Environ Microb 67:4566–4572

    Article  Google Scholar 

  • Chao A, Chazdon RL, Colwell RK, Shen TJ (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:361–371

    Article  Google Scholar 

  • Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  • Chao LSL, Davis RE, Moyer CL (2007) Characterization of bacterial community structure in vestimentiferan tubeworm Ridgeia piscesae trophosomes. Mar Ecol 28:72–85

    Article  Google Scholar 

  • Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6:725–740

    Article  Google Scholar 

  • Duhaime, M (2003) Phylogenetics of vestimentiferan symbionts from Guaymas Basin using the 16S and RuBisCO genes. https://www.researchgate.net/publication/237408396 Accessed 26 July 2016

    Google Scholar 

  • Duperron S, Bergin C, Zielinski F, Blazejak A, Pernthaler A, McKiness ZP, DeChaine E, Cavanaugh CM, Dubilier N (2006) A dual symbiosis shared by two mussel species, Bathymodiolus azoricus and Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), from hydrothermal vents along the northern Mid-Atlantic Ridge. Environ Microbiol 8:1441–1447

    Article  Google Scholar 

  • Duperron S, Rodrigues CF, Léger N, Szafranski K, Decker C, Olu K, Gaudron SM (2012) Diversity of symbioses between chemosynthetic bacteria and metazoans at the Guiness cold seep site (Gulf of Guinea, West Africa). Microbiologyopen 1:467–480

    Article  Google Scholar 

  • Elsaied H, Kimura H, Naganuma T (2002) Molecular characterization and endosymbiotic localization of the gene encoding D-ribulose 1,5-bisphosphate carboxylase-oxygenase (RuBisCO) form II in the deep-sea vestimentiferan trophosome. Microbiology 148:1947–1957

    Article  Google Scholar 

  • Fang J, Arakawa S, Kato C, Schouten S (2006) Microbial diversity of cold seep sediments in Sagami Bay, Japan, as determined by 16S rRNA gene and lipid analyses. FEMS Microbiol Ecol 57:429–441

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome oxidase c subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299

    Google Scholar 

  • Forget NL, Kim Juniper S (2013) Free-living bacterial communities associated with tubeworm (Ridgeia piscesae) aggregations in contrasting diffuse flow hydrothermal vent habitats at the Main Endeavour Field, Juan de Fuca Ridge. Microbiologyopen 2:259–275

    Article  Google Scholar 

  • Frank KL, Rogers DR, Olins HC, Vidoudez C, Girguis PR (2013) Characterizing the distribution and rates of microbial sulfate reduction at Middle Valley hydrothermal vents. ISME J 7:1391–1401

    Article  Google Scholar 

  • Gardebrecht A, Markert S, Sievert S M, Felbeck H, Thürmer A, Albrecht D, Daniel R (2012) Physiological homogeneity among the endosymbionts of Riftia pachyptila and Tevnia jerichonana revealed by proteogenomics. ISME J 6:766–776

    Article  Google Scholar 

  • Gaudron SM, Demoyencourt E, Duperron S (2012) Reproductive traits of the cold seep symbiotic mussel Idas modiolaeformis: gametogenesis and larval biology. Biol Bull 222:6–16

    Article  Google Scholar 

  • Gorny N, Schink B (1994) Anaerobic degradation of catechol by Desulfobacterium sp. strain Cat2 proceeds via carboxylation to protocatechuate. Appl Environ Microb 60:3396–3400

    Google Scholar 

  • Hashimoto J, Miura T, Fujikura K, Ossaka J (1993) Discovery of vestimentiferan tube-worms in the euphotic zone. Zool Sci 10:1063–1067

    Google Scholar 

  • Hodges TW, Olson JB (2009) Molecular comparison of bacterial communities within iron-containing flocculent mats associated with submarine volcanoes along the Kermadec Arc. Appl Environ Microb 75:1650–1657

    Article  Google Scholar 

  • Huber JA, Butterfield DA, Baross JA (2003) Bacterial diversity in a subseafloor habitat following a deep-sea volcanic eruption. FEMS Microbiol Ecol 43:393–409

    Article  Google Scholar 

  • Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJM (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microb 67:4399–4406

    Article  Google Scholar 

  • Hügler M, Petersen JM, Dubilier N, Imhoff JF, Sievert SM (2011) Pathways of carbon and energy metabolism of the epibiotic community associated with the deep-sea hydrothermal vent shrimp Rimicaris exoculata. PLoS One 6:e16018

    Article  Google Scholar 

  • JAMSTEC (2005) Cruise report of NT05-01 Leg 2 (R/V Natsushima & ROV Hyper-Dolphin)-Research for tagiri & tubeworm site in Kinko Bay, Kagoshima. Japan Agency for Marine Earth Science and Technology Center, 97 p

    Google Scholar 

  • Kimura H, Higashide Y, Naganuma T (2003) Endosymbiotic microflora of the vestimentiferan tubeworm (Lamellibrachia sp.) from a bathyal cold seep. Mar Biotechnol 5:593–603

    Article  Google Scholar 

  • Kojima S, Murakami S, Nemoto S, Watanabe H, Miyake H, Tsuchida S (2012) Genetic diversity and population structure of a vestimentiferan annelid Lamellibrachia satsuma in Japanese and northern Mariana waters. Plank Benth Res 7:146–150

    Article  Google Scholar 

  • Laming SR, Duperron S, Cunha MR, Gaudron SM (2014) Settled, symbiotic, then sexually mature: adaptive developmental anatomy in the deep-sea, chemosymbiotic mussel Idas modiolaeformis. Mar Biol 161:1319–1333

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lyimo TJ, Pol1 A, Harhangi1 HR, Jetten MSM, Op den Camp HJM (2009) Anaerobic oxidation of dimethylsulfide and methanethiol in mangrove sediments is dominated by sulfate-reducing bacteria. FEMS Microbiol Ecol 70:483–492

    Article  Google Scholar 

  • Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton, 192 p

    Book  Google Scholar 

  • Miura T, Nedachi M, Hashimoto J (2002) Sulphur sources for chemoautotrophic nutrition of shallow water vestimentiferan tubeworms in Kagoshima Bay. J Mar Biol Assoc UK 82:537–540

    Article  Google Scholar 

  • Miyake H, Kitada M, Tsuchida S, Okuyama Y, Nakamura K (2007) Ecological aspects of hydrothermal vent animals in captivity at atmospheric pressure. Mar Ecol 28:86–92

    Article  Google Scholar 

  • Naganuma T, Elsaied H, Hoshii D, Kimura H (2005) Bacterial endosymbioses of gutless tube-dwelling worms in nonhydrothermal vent habitats. Mar Biotechnol 7:416–428

    Article  Google Scholar 

  • Naganuma T, Kato C, Hirayama H, Moriyama N, Hashimoto J, Horikoshi K (1997) Intracellular occurrence of ε-Proteobacterial 16S rDNA sequences in the vestimentiferan trophosome. J Oceanogr 53:193–197

    Google Scholar 

  • Nakagawa S, Takai K, Inagaki F, Chiba H, Ishibashi J, Kataoka S, Hirayama H, Nunoura T, Horikoshi K, Sako Y (2005) Variability in microbial community and venting chemistry in a sediment-hosted backarc hydrothermal system: impacts of subseafloor phase-separation. FEMS Microbiol Ecol 54:141–155

    Article  Google Scholar 

  • Nakagawa S, Takaki Y, Shimamura S, Reysenbach A-L, Takai K, Horikoshi K (2007) Deep-sea vent ε-proteobacterial genomes provide insights into emergence of pathogens. P Natl Acad Sci USA 104:12146–12150

    Article  Google Scholar 

  • Nakagawa S, Takai K (2008) Deep-sea vent chemoautotrophs: diversity, biochemistry and ecological significance. FEMS Microbiol Ecol 65:1–14

    Article  Google Scholar 

  • Newton ILG, Girguis PR, Cavanaugh CM (2008) Comparative genomics of vesicomyid clam (Bivalvia: Mollusca) chemosynthetic symbionts. BMC Genomics 9:585

    Article  Google Scholar 

  • Nunoura T, Oida H, Nakaseama M, Kosaka A, Ohkubo SB, Kikuchi T, Kazama H, Hosoi-Tanabe S, Nakamura K, Kinoshita M, Hirayama H, Inagaki F, Tsunogai U, Ishibashi J, Takai K (2010) Archaeal diversity and distribution along thermal and geochemical gradients in hydrothermal sediments at the Yonaguni Knoll IV hydrothermal field in the Southern Okinawa Trough. Appl Environ Microb 76:1198–1211

    Article  Google Scholar 

  • Nussbaumer AD, Fisher CR, Bright M (2006) Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441:345–348.

    Article  Google Scholar 

  • Pachiadaki MG, Kallionaki A, Dählmann A, Lange GJ, Kormas KA (2011) Diversity and spatial distribution of prokaryotic communities along a sediment vertical profile of a deepsea mud volcano. Microb Ecol 62:655–668

    Article  Google Scholar 

  • Raggi L, Schubotz F, Hinrichs KU, Dubilier N, Petersen JM (2013) Bacterial symbionts of Bathymodiolus mussels and Escarpia tubeworms from Chapopote, an asphalt seep in the southern Gulf of Mexico. Environ Microbiol 15:1969–1987

    Article  Google Scholar 

  • Redmond MC, Valentine DL, Sessions AL (2010) Identification of novel methane-, ethane-, and propane-oxidizing bacteria at marine hydrocarbon seeps by stable isotope probing. Appl Environ Microb 76:6412–6422

    Article  Google Scholar 

  • Rodrigues CF, Cunha MR, Génio L, Duperron S (2013) A complex picture of associations between two host mussels and symbiotic bacteria in the Northeast Atlantic. Naturwissenschaften 100:21–31

    Article  Google Scholar 

  • Ruehland C, Blazejak A, Lott C, Loy A, Erséus C, Dubilier N (2008) Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean sea grass sediments. Environ Microbiol 10:3404–3416

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Sekar R, Mills DK, Remily ER, Voss JD, Richardson LL (2006) Microbial communities in the surface mucopolysaccharide layer and the black band microbial mat of black band-diseased Siderastrea siderea. Appl Environ Microb 72:5963–5973

    Article  Google Scholar 

  • Suzuki Y, Sasaki T, Suzuki 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 Microb 71:5440–5450

    Article  Google Scholar 

  • Takai K, Miyazaki M, Hirayama H, Nakagawa S, Querellou J, Godfroy A (2009) Isolation and physiological characterization of two novel, piezophilic, thermophilic chemolithoautotrophs from a deep-sea hydrothermal vent chimney. Environ Microbiol 11:1983–1997

    Article  Google Scholar 

  • Takishita K, Yubuki N, Kakizoe N, Inagaki Y, Maruyama T (2007) Diversity of microbial eukaryotes in sediment at a deep-sea methane cold seep: surveys of ribosomal DNA libraries from raw sediment samples and two enrichment cultures. Extremophiles 11:563–576

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  Google Scholar 

  • Walsh DA, Zaikova E, Howes CG, Song YC, Wright JJ, Tringe SG, Tortell PD, Hallam SJ (2009) Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science 326:578–582

    Article  Google Scholar 

  • Yan T, Ye Q, Zhou Z, Zhang CL (2006) Diversity of functional genes for methanotrophs in sediments associated with gas hydrates and hydrocarbon seeps in the Gulf of Mexico. FEMS Microbiol Ecol 57:251–259

    Article  Google Scholar 

  • Yanagibayashi M, Nogi Y, Li L, Kato C (1999) Changes in the microbial community in Japan Trench sediment from a depth of 6292 m during cultivation without decompression. FEMS Microbiol Lett 170:271–279

    Article  Google Scholar 

  • Zbinden M, Shillito B, Le Bris N, de Villardi de Montlaur C, Roussel E, Guyot F, Gaill F, Cambon-Bonavita M-A (2008) New insights on the metabolic diversity among the epibiotic microbial community of the hydrothermal shrimp Rimicaris exoculata. J Exp Mar Biol Ecol 359:131–140

    Article  Google Scholar 

  • Zimmermann J, Lott C, Weber M, Ramette A, Bright M, Dubilier N, Petersen JM (2014) Dual symbiosis with co-occurring sulfur-oxidizing symbionts in vestimentiferan tubeworms from a Mediterranean hydrothermal vent. Environ Microbiol 16:3638–3656

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Marine Biotechnology Research Center, KIOST, Ansan, 15627, Korea

    Ajit Kumar Patra, Hyun Hee Cho, Yong Min Kwon, Kae Kyoung Kwon, Sung Gyun Kang & Sang-Jin Kim

  2. Department of Marine Biotechnology, Korea University of Science and Technology, Daejeon, 34113, Korea

    Ajit Kumar Patra, Kae Kyoung Kwon, Sung Gyun Kang & Sang-Jin Kim

  3. Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology, Yokosuka, 247-0061, Japan

    Takako Sato & Chiaki Kato

  4. Marine Biodiversity Institute of Korea, Seocheon, 33662, Korea

    Sang-Jin Kim

Authors
  1. Ajit Kumar Patra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hyun Hee Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yong Min Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kae Kyoung Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takako Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chiaki Kato
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sung Gyun Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sang-Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sang-Jin Kim.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Patra, A.K., Cho, H.H., Kwon, Y.M. et al. Phylogenetic relationship between symbionts of tubeworm Lamellibrachia satsuma and the sediment microbial community in Kagoshima Bay. Ocean Sci. J. 51, 317–332 (2016). https://doi.org/10.1007/s12601-016-0028-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12601-016-0028-6

Key words

Search

Navigation