6 Summary and Conclusions
The symbioses between invertebrates and chemosynthetic bacteria allow both host and symbiont to colonize and thrive in otherwise inhospitable deep-sea habitats. Given the global distribution of the bathymodioline symbioses, this association is an excellent model for evaluating co-speciation and evolution of symbioses. Thus far, the methanotroph and chemoautotroph endosymbionts of mussels are tightly clustered within two independent clades of gamma Proteobacteria, respectively. Further physiological and genomic studies will elucidate the ecological and evolutionary roles that these bacterial clades play in the symbiosis and chemosynthetic community. Due to the overall abundance of the methanotrophic symbioses at hydrothermal vents and hydrocarbon seeps, they likely play a significant, but as of yet unquantified, role in the biogeochemical cycling of methane. With this in mind, the search for methanotrophic symbioses should not be restricted to these known deep-sea habitats, but rather should be expanded to include methane-rich coastal marine and freshwater environments inhabited by methanotrophs and bivalves. Our current understanding of the bathymodioline symbioses provides a strong foundation for future explorations into the origin, ecology, and evolution of methanotroph symbioses, which are now becoming possible through a combination of classical and advanced molecular techniques.
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Anthony C (1982) The biochemistry of methylotrophs. Academic Press, New York
Apps JA, van de Kamp PC (1993) Energy gases of abiogenic origin in the Earth’s crust. In: Howell DG, Wiese K, Fanelli M, Zink L, Cole F (eds) The future of energy gases. US Geol Surv Prof Pap 1570:81–132
Barry JP, Buck KR, Kochevar RK, Nelson DC, Fujiwara Y, Goffredi SK, Hashimoto J (2002) Methane-based symbiosis in a mussel, Bathymodiolus platifrons, from cold seeps in Sagami Bay, Japan. Invert Biol 121:47–54
Belkin S, Nelson DC, Jannasch HW (1986) Symbiotic assimilation of CO2 in two hydrothermal vent animals, the mussel Bathymodiolus thermophilus and the tubeworm Riftia pachyptila. Biol Bull 170:110–121
Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jorgensen BB, Witte U, Pfannkuche O (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407:623–626
Bowman JP, Jimenez L, Rosario I, Hazen TC, Sayler GS (1993) Characterization of the methanotrophic bacterial community present in a trichloroethylene-contaminated groundwater site. Appl Environ Microbiol 59:2380–2387
Bratina BJ, Brusseau GA, Hanson RS (1992) Use of 16S rRNA analysis to investigate phylogeny of methylotrophic bacteria. Int J Syst Bacteriol 42:645–648
Brooks JM, Kennicutt MC II, Fisher CR, Macko SA, Cole K, Childress JJ, Bidigare RR, Vetter RD (1987) Deep-sea hydrocarbon seep communities: evidence for energy and nutritional carbon sources. Science 20:1138–1142
Brown KM (1990) The nature and hydrogeologic significance of mud diapirism and diatremes from accretionary systems. J Geophys Res 95:8969–8982
Campbell KA, Bottjer DJ (1993) Fossil cold seeps. Res Exp 9:326–343
Cary SC, Fisher CR, Felbeck H (1988) Mussel growth supported by methane as sole carbon and energy source. Science 240:78–80
Cavanaugh CM (1985) Symbioses of chemoautotrophic bacteria and marine invertebrates from hydrothermal vents and reducing sediments. Biol Soc Wash Bull 6:373–388
Cavanaugh CM (1992) Methanotroph-invertebrate symbioses in the marine environment: ultrastructural, biochemical, and molecular studies. In: Murrell JC, Kelly DP (eds) Microbial growth on C1 compounds. Intercept, Andover, UK, pp 315–328
Cavanaugh CM, Levering PR, Maki JS, Mitchell R, Lidstrom ME (1987) Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325:346–347
Cavanaugh CM, Wirsen C, Jannasch HJ (1992) Evidence for methylotrophic symbionts in a hydrothermal vent mussel (Bivalvia: Mytilidae) from the Mid-Atlantic Ridge. Appl Environ Microbiol 58:3799–3803
Cavanaugh CM, McKiness ZP, Newton ILG, Stewart FJ (2005) Marine chemosynthetic symbioses. In: Dworkin M, Falkow S, Rosenberg E, et al (eds) The Prokaryotes: a handbook on the biology of bacteria, 3rd edn. Springer, Berlin Heidelberg New York (in press)
Childress JJ, Fisher CR, Brooks JM, Kennicutt MC II, Bidigare R, Anderson AE (1986) A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science 233:1306–1308
Dando PR, Bussman I, Niven SJ, O’Hara SCM, Schmaljohann R, Taylor LJ (1994) A methane seep area in the Skagerrak, the habitat of the pogonophore Siboglinum poseidoni and the bivalve mollusc Thyasira sarsi. Mar Ecol Prog Ser 107:157–167
DeChaine EG, Bates A, Shank TM, Cavanaugh CM (2005) Off-axis symbiosis found: characterization and biogeography of bacterial symbionts of Bathymodolus mussels from Lost City hydrothermal vents, In review
Dedysh SN (2002) Methanotrophic bacteria of acidic sphagnum peat bogs. Microbiology 71:638–650
Distel D, Lee HK, Cavanaugh CM (1995) Intracellular coexistence of methano-and thioautotrophic bacteria in a hydrothermal vent mussel. Proc Natl Acad Sci USA 92:9598–9602
Distel D, Baco AR, Chuang E, Morrill W, Cavanaugh C, Smith CR (2000) Do mussels take wooden steps to deep-sea vents? Science 403:725–726
Dubilier N, Windoffer R, Giere O (1998) Ultrastructure and stable carbon isotope composition of the hydrothermal vent mussels Bathymodiolus brevior and B. sp. affinis brevior from the North Fiji Basin, western Pacific. Mar Ecol Prog Ser 165:187–193
Dubilier N, Amann R, Erseus C, Muyzer G, Park SY, Giere O, Cavanaugh CM (1999) Phylogenetic diversity of bacterial endosymbionts in the gutless marine oligochete Olavius loisae (Annelida). Mar Ecol Prog Ser 178:271–280
Duperron S, Nadalig T, Caprais J-C, Sibuet M, Fiala-Medioni A, Amann R, Dubilier N (2005a) Dual symbiosis in a Bathymodiolus mussel from a methane seep on the Gabon continental margin (South East Atlantic): 16S rRNA phylogeny and distribution of the symbionts in the gills (in press)
Duperron ST, Bergen C, Zielinski F, McKiness ZP, DeChaine EG, Sibuet M, Cavanaugh CM, Dubilier N (2005b) A dual symbiosis shared by two Mid-Atlantic Ridge bathymodioline mussels (Bivalvia: Mytilidae) Env. Microbiol. In press.
Eckelbarger KJ, Young CM (1999) Ultrastructure of gametogenesis in a chemosynthetic mytilid bivalve (Bathymodiolus childressi) from a bathyal, methane seep environment (northern Gulf of Mexico). Mar Biol 135:635–646
Fiala-Médioni A, McKiness Z, Dando P, Boulegue J, Mariotti A, Alayse-Danet A, Robinson J, Cavanaugh C (2002) Ultrastructural, biogeochemical, and immunological characterization of two populations of a new species of Mytilid mussel, Bathymodiolus azoricus, from the Mid-Atlantic Ridge: evidence for a dual symbiosis. Mar Biol 141:1035–1043
Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399–436
Fisher CR, Childress JJ (1992) Organic carbon transfer from methanotrophic symbionts to the host hydrocarbon-seep mussel. Symbiosis 12:221–235
Fisher CR, Childress JJ, Oremland RS, Bidigare RR (1987) The importance of methane and thiosulfate in the metabolism of the bacterial symbionts of two deep-sea mussels. Mar Biol 96:59–71
Fisher CR, Brooks JM, Vodenichar JS, Zande JM, Childress JJ, Burke RA Jr (1993) The co-occurrence of methanotrophic and chemoautotrophic sulfur-oxidizing bacterial symbionts in a deep-sea mussel. Mar Ecol 14:277–289
Fisher CR, Childress JJ, Macko SA, Brooks JM (1994) Nutritional interaction in Galapagos Rift hydrothermal vent communities: inferences from stable carbon and nitrogen isotope analyses. Mar Ecol Prog Ser 103:45–55
Fujiwara Y, Takai K, Uematsu K, Tsuchida S, Hunt JC, Hashimoto J (2000) Phylogenetic characterization of endosymbionts in three hydrothermal vent mussels: influence on host distributions. Mar Ecol Prog Ser 208:147–155
Grassle JF (1985) Hydrothermal vent animals — distribution and biology. Science 229:713–717
Gustafson R, Turner R, Lutz R, Vrijenhoek R (1998) A new genus and five new species of mussels (Bivalvia, Mytilidae) from deep-sea sulfide/hydrocarbon seeps in the Gulf of Mexico. Malacologia 40:63–112
Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471
Hanson RS, Netrusov AI, Tsuji K (1991) The obligate methanotrophic bacteria Methylococcus, Methylomonas, Methylosinus and related bacteria. In: Balows A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer, Berlin Heidelberg New York, pp 2350–2365
Hashimoto J (2001) A new species of Bathymodiolus (Bivalvia: Mytilidae) from hydrothermal vent communities in the Indian Ocean. Venus Jpn J Malacol 60:141–149
Hashimoto J, Okutani T (1994) Four new mytilid mussels associated with deep sea chemosynthetic communities around Japan. Venus Jpn J Malacol 53:61–83
Hedberg HD (1980) Methane generation and petroleum migration. In: Roberts WH III, Cordell RJ (eds) Problems of petroleum migration. American Association of Petroleum Geologists. Studies in geology no 10. Am Assoc Petrol Geol, Tulsa, pp 179–206
Hinrichs K-U, Hayes JM, Sylva SP, Brewer PG, DeLong EF (1999) Methane-consuming archaebacteria in marine sediments. Nature 398:802–805
Holmes A, Owens N, Murrell J (1995) Detection of novel marine methanotrophs using phylogenetic and functional gene probes after methane enrichment. Microbiology 141:1947–1955
Hornafius JS, Quigley D, Luyendyk BP (1999) The world’s most spectacular marine hydrocarbon seeps (Coal Oil Point, Santa Barbara Channel, California): quantification of emissions. J Geophys Res 104:20703–20711
Huber R, Kurr M, Jannasch HW, Stetter KO (1989) A novel group of abyssal methnogenic archaebaceria (Methanopyrus) growing at 110-degrees-C. Nature 342:833–834
Judd AG (2003) The global importance and context of methane escape from the seabed. Geo Mar Lett 23:147–154
Judd AG, Hovland M, Dimitrov LI. Garcia Gil S, Jukes V (2002) The geological methane budget at continental margins and its influence on climate change. Geofluids 2:109–126
Kelley DS, Karson JA, Blackman DK, Früh-Green GL, Butterfield DA, Lilley MD, Olson EJ, Schrenk MO, Roe KK, Lebon GT, Rivizzigno P, and the AT3-60 Shipboard Party (2001) An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30°N. Nature 412:145–149
Kenk VC, Wilson BR (1985) A new mussel (Bivalvia, Mytilidae) from hydrothermal vents in the Galapagos Rift zone. Malacologia 26:253–271
Kennicutt MC, Burke RA, MacDonald IR, Brooks JM, Denoux GJ, Macko SA (1992) Stable isotope partitioning in seep and vent organisms: chemical and ecological significance. Chem Geol 101:293–310
Kim S, Mullineaux LS (1998) Distribution and near-bottom transport of larvae and other plankton at hydrothermal vents. Deep Sea Res II 45:423–440
Kochevar RE, Childress JJ, Fisher CR, Minnich E (1992) The methane mussel: roles of symbiont and host in the metabolic utilization of methane. Mar Biol 112:389–401
Lee RW, Childress JJ (1994) Assimilation of inorganic nitrogen by chemoautotrophic and methanotrophic symbioses. Appl Environ Microbiol 60:1852–1858
Lee RW, Childress JJ (1996) Inorganic N assimilation and ammonium pools in a deep-sea mussel containing methanotrophic endosymbionts. Biol Bull 190:373–384
Lee RW, Thuesen EV, Childress JJ, Fisher CR (1992) Ammonium and free amino acid uptake by a deep-sea mussel containing methanotrophic bacterial symbionts. Mar Biol 113:99–106
Lee R, Robinson JJ, Cavanaugh CM (1999) Pathways of inorganic nitrogen assimilation in chemoautotrophic bacteria-marine invertebrate symbioses: expression of host and symbiont glutamine synthetase. J Exp Biol 202:289–300
Le Pennec M, Beninger PG (1997) Ultrastructural characteristics of spermatogenesis in three species of deep-sea hydrothermal vent mytilids. Can J Zool 75:308–316
Lilley MD, Butterfield DA, Lupton JE, Olson EJ (2003) Magmatic events can produce rapid changes in hydrothermal vent chemistry. Nature 472:878–881
Lonsdale P (1977) Clustering of suspension-feeding macrobenthos near abyssal hydrothermal vents at oceanic spreading centers. Deep Sea Res 24:857
Lupton JE, Lilley MD, Olson EJ, von Damm KL (1991) Gas chemistry of vent fluids from 9°–10°N on the East Pacific Rise. EOS 72:F481
MacAvoy SE, Fisher CR, Carney RS, Macko SA (2005) Nutritional associations among fauna at hydrocarbon seep communities in the Gulf of Mexico. Mar Ecol Prog Ser (in press)
McKiness ZP, Cavanaugh CM (2005) The ubiquitous mussel: Bathymodiolus aff. brevior symbiosis discovered at the Central Indian Ridge hydrothermal vents. Mar Ecol Prog Ser (in press)
McKiness ZP, McMullin ER, Fisher CR, Cavanaugh CM (2005) A new bathymodioline mussel symbiosis at the Juan de Fuca hydrothermal vents (submitted)
Milkov AV (2000) Worldwide distribution of submarine mud volcanoes and associated gas hydrates. Mar Geol 167:29–42
Miyazaki J-I, Shintaku M, Kyuno A, Fujiwara Y, Hashimoto J, Iwasaki H (2004) Phylogenetic relationships of deep-sea mussels of the genus Bathymodiolus (Bivalvia: Mytilidae). Mar Biol 144:527–535
Nelson DC, Hagan KD, Edwards DB (1995) The gill symbiont of the hydrothermal vent mussel Bathymodiolus thermophilus is a psychrophilic, chemoautotrophic, sulfur bacterium. Mar Biol 121:487–495
O’Mullan GD, Maas PAY, Lutz RA, Vrijenhoek RC (2001) A hybrid zone between hydrothermal vent mussels (Bivalvia: Mytilidae) from the Mid-Atlantic Ridge. Mol Ecol 10:2819–2831
Page HM, Fisher CR, Childress JJ (1990) Role of filter-feeding in the nutritional biology of a deep-sea mussel with methanotrophic symbionts. Mar Biol 104:251–257
Peek AS, Vrijenhoek RC, Gaut BS (1998) Accelerated evolutionary rate in sulfur-oxidizing endosymbiotic bacteria associated with the mode of symbiont transmission. Mol Biol Evol 15:1514–1523
Pernthaler A, Amann R (2004) Simultaneous fluorescence in situ hybridization of mRNA and rRNA in environmental bacteria. Appl Environ Microbiol 70:5426–5433
Pile AJ, Young CM (1999) Plankton availability and retention efficiencies of cold-seep symbiotic mussels. Limnol Oceanogr 44:1833–1839
Pimenov NV, Kalyuzhnaya MG, Khmelenina VN, Mityushina LL, Trotsenko YA (2002) Utilization of methane and carbon dioxide by symbiotrophic bacteria in gills of Mytilidae (Bathymodiolus) from the Rainbow and Logatchev hydrothermal fields on the Mid-Atlantic Ridge. Microbiology 71:587–594
Pranal V, Fiala-Médioni A, Guezennec J (1997) Fatty acid characteristics in two symbiont-bearing mussels from deep-sea hydrothermal vents of the south-western Pacific. J Mar Biol Assoc UK 77:473–492
Reeburgh WS (1980) Anaerobic methane oxidation: rate distributions in Skan Bay sediments. Earth Planet Sci Lett 47:345–352
Robinson JJ, Polz MF, Fiala-Médioni A, Cavanaugh CM (1998) Physiological and immunological evidence for two distinct C1-utilizing pathways in Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), a dual endosymbiotic mussel from the Mid-Atlantic Ridge. Mar Biol 132:625–633
Schmaljohan R (1991) Oxidation of various potential energy sources by the methanotrophic endosymbionts of Siboglinum poseidoni (Pogonophora). Mar Ecol Prog Ser 76:143–148
Schmaljohan R, Flügel HJ (1987) Methane-oxidizing bacteria in Pogonophora. Sarsia 72:91–98
Schmaljohan R, Faber E, Whiticar MJ, Dando PR (1990) Co-existence of methane-and sulphur-based endosymbioses between bacteria and invertebrates at a site in the Skagerrak. Mar Ecol Prog Ser 61:119–124
Shima S, Warkentin E, Thauer RK, Ermler U (2002) Structure and function of enzymes involved in the methanogenic pathway utilizing carbon dioxide and molecular hydrogen. J Biosci Bioeng 93:519–530
Sibuet M, Olu K (1998) Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep Sea Res II 45:517–567
Streams ME, Fisher CR, Fiala-Médioni A (1997) Methanotrophic symbiont location and fate of carbon incorporated from methane in a hydrocarbon seep mussel. Mar Biol 129:465–476
Taviani M (1994) The Calcari-A-Lucina macrofauna reconsidered — deep-sea faunal eases from Miocene age cold vents in the Romagna Appenine, Italy. Geo Mar Lett 14:185–191
Trask JL, van Dover CL (1999) Site-specific and ontogenetic variations in nutrition of mussels (Bathymodiolus sp.) from the Lucky Strike hydrothermal vent field, Mid-Atlantic Ridge. Limnol Oceanogr 44:334–343
Tunnicliffe V (1991) The biology of hydrothermal vents — ecology and evolution. Oceanogr Mar Biol 29:319–407
Tunnicliffe V, Fowler C (1996) Influence of sea-floor spreading on the global hydrothermal vent fauna. Nature 379:531–533
Tunnicliffe V, McArthur AG, Mchugh D (1998) A biogeographical perspective of the deep-sea hydrothermal vent fauna. Adv Mar Biol 34:353–442
Vacelet J, Fiala-Médioni A, Fisher CR, Boury-Esnault N (1996) Symbiosis between methane-oxidizing bacteria and a deep-sea carnivorous cladorhizid sponge. Mar Ecol Prog Ser 145:77–85
Van Dover CL (2000) The ecology of deep-sea hydrothermal vents. Princeton Univ Press, Princeton, NJ, 424 pp
Van Dover CL (2002) Trophic relationships among invertebrates at the Kairei hydrothermal vent field (Central Indian Ridge). Mar Biol 141:761–772
Van Dover CL, Humphris SE, Fornari D, Cavanaugh CM, Collier R, Goffredi SK, Hashimoto J, Lilley M, Reysenbach AL, Shank TM, von Damm KL, Banta A, Gallant RM, Götz D, Green D, Hall J, Harmer TL, Hurtado LA, Johnson P, McKiness ZP, Meredith C, Olson E, Pan IL, Turnipseed M, Won Y, Young CR III, Vrijenhoek RC (2001) Biogeography and ecological setting of Indian Ocean hydrothermal vents. Science 294:818–823
Van Dover CL, German C.R, Speer K.G, Parson L.M, and Vrijenhoek R.C (2002) Evolution and biogeography of deep-sea vent and seep invertebrates. Science 295:1253–1257
Von Cosel R, Olu K (1998) Gigantism in Mytilidae. A new Bathymodiolus from cold seep areas on the Barbados accretionary Prism. CR Acad Sci Paris Sci Vie 321:655–663
Von Cosel R, Métivier B, Hashimoto J (1994) Three new species of Bathymodiolus (Bivalvia: Mytilidae) from hydrothermal vents in the Lau Basin and the North Fiji Basin, Western Pacific, and the Snake Pit area, Mid-Atlantic Ridge. Veliger 37:374–392
Vrijenhoek RC (1997) Gene flow and genetic diversity in naturally fragmented metapopulations of deep-sea hydrothermal vent animals. J Heredity 88:285–293
Vrijenhoek RC, Shank T, Lutz R (1998) Gene flow and dispersal in deep-sea hydrothermal vent animals. Cah Biol Mar 39:363–366
Won Y, Hallam SJ, O’Mullan GD, Pan IL, Buck KR, Vrijenhoek RC (2003a) Environmental acquisition of thiotrophic endosymbionts by deep-sea mussels of the genus Bathymodiolus. Appl Environ Microbiol 69:6785–6792
Won Y, Young CR, Lutz RA, Vrijenhoek RC (2003b) Dispersal barriers and isolation among deep-sea mussel populations (Mytilidae: Bathymodiolus) from eastern Pacific hydrothermal vents. Mol Ecol 12:169–184
Yamanaka T, Mizota C, Maki Y, Fujikura K, Chiba H (2000) Sulfur isotope composition of soft tissues of deep-sea mussels, Bathymodiolus spp, in Japanese waters. Benthos Res 55:63–68
Yamanaka T, Mizota C, Fujiwara Y, Chiba H, Hashimoto J, Gamo T, Okudaira T (2003) Sulphur-isotopic composition of the deep-sea mussel Bathymodiolus marisindicus from currently active hydrothermal vents in the Indian Ocean. J Mar Biol Assoc UK 83:841–848
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2005 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
DeChaine, E.G., Cavanaugh, C.M. (2005). Symbioses of Methanotrophs and Deep-Sea Mussels (Mytilidae: Bathymodiolinae). In: Overmann, J. (eds) Molecular Basis of Symbiosis. Progress in Molecular and Subcellular Biology, vol 41. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-28221-1_11
Download citation
DOI: https://doi.org/10.1007/3-540-28221-1_11
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-28210-5
Online ISBN: 978-3-540-28221-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)
