Ultrastructural, biochemical, and immunological characterization of two populations of the mytilid mussel Bathymodiolus azoricus from the Mid-Atlantic Ridge: Evidence for a dual symbiosis

Marine Biology

Volumn 141, Issue 6, 2002, Pages 1035-1043

  Fiala Medioni A ^a   McKiness, Z P ^b   Dando, P ^c   Boulegue, J ^a   Mariotti, A ^a   Alayse Danet, A M ^d   Robinson, J J ^b   Cavanaugh, C M ^b  

^a SORBONNE UNIVERSITÉ   (France)

^b HARVARD UNIVERSITY   (United States)

^c BANGOR UNIVERSITY   (United Kingdom)

^d IFREMER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROTHERMAL VENT; MOLLUSC; PHYSIOLOGY; SYMBIOSIS;

ATLANTIC OCEAN;

BATHYMODIOLUS; BATHYMODIOLUS AZORICUS; BIVALVIA; COCCOIDEA; METHYLOCOCCACEAE; MOLLUSCA; MYTILIDAE;

EID: 0036962764     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-002-0903-9     Document Type: Article

References (45)

1. Anthony C (1982) The biochemistry of methylotrophs. Academic, London
2. Anthony C, Zatman LJ (1964) The microbial oxidation of methanol 2. The methanol-oxidizing enzyme of Pseudomonas sp. M27. Biochem J 92:614-621
3. Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JA, Struhl K (1990) Current protocols in molecular biology. Wiley, New York
4. Brooks JM, Kennicutt II MC, 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 238:1138-1142
5. Cavanaugh CM (1993) Methanotroph-invertebrate symbioses in the marine environment: ultrastructural, biochemical, and molecular studies. In: Murrell JC, Kelly DP (eds) Microbial growth on Cl compounds. Intercept, Andover, UK
6. Cavanaugh CM (1994) Microbial symbiosis: patterns of diversity in the marine environment. Am Zool 34:79-89
7. Cavanaugh CM, Levering PR, Maki JS, Mitchell R, Lidstrom ME (1987) Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature 325:346-348
8. 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
9. Charlou JL, Donval JP, Douville E, Jean-Baptiste P, Radford-Knoery J, Fouquet Y, Dapoigny A, Stievnard M (2000) Compared geochemical signatures and the evolution of Menez Gwen (37°17′N) and Lucky Strike (37°50′N) hydrothermal fluids, south of the Azores Triple Junction on the Mid-Atlantic Ridge. Chem Geol 171:49-75
10. Childress JJ, Fisher CR (1992) The biology of hydrothermal vent animals: physiology, biochemistry, and autotrophic symbioses. Oceanogr Mar Biol Annu Rev 30:337-441
11. Childress JJ, Fisher CR, Brooks JM, Kennicutt II MC, Bidigare R, Anderson AE (1986) A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science 233:1306-1308
12. Desbruyères D, Alayse-Danet AM, Antoine E, Barbier G, Barriga F, Biscoito M, Briand P, Brulport JP, Comtet T, Cornec L, Crassous P, Dando P, Fabri MC, Felbeck H, Lallier F, Fiala-Médioni A, Gonzalvez J, Menard F, Kerdoncuff J, Patching J, Saldhana L, Sarradin PM (1994) New information on the ecology of deep-sea vent communities in the Azores Triple Junction area: preliminary results of the DIVA 2 cruise (31 May-4 July, 1994). InterRidge News 3:18-19
13. Desbruyères D, Biscoito M, Caprais JC, Colaço A, Comtet T, Crassous P, Fouquet Y, Kripounoff A, Le Bris N, Olu K, Riso R, Sarradin PM, Segonzac M, Vangriesheim A (2001) Variations in the deep-sea hydrothermal communities on the Mid-Atlantic Ridge near the Azores Plateau. Deep-Sea Res 48:1325-1346
14. Distel DL, Lee K-W, Cavanaugh CM (1995) Intracellular coexistence of methano- and thioautotrophic bacteria in a hydrothermal vent mussel. Proc Natl Acad Sci USA 92:9598-9602
15. Fassel TA, Buchholz LA, Collins MLP, Remson CC (1992) Localization of methanol dehydrogenase in two strains of methylotrophic bacteria detected by immunogold labelling. Appl Environ Microbiol 58:2302-2307
16. Felbeck H (1981) Chemoautotrophic potential of the hydrothermal vent tube worm, Riftia pachyptila Jones (Vestimentifera). Science 213:336-338
17. Fiala-Médioni A, Le Pennec M (1987) Trophic structural adaptations in relation with the bacterial association of bivalve molluscs from hydrothermal vents and subduction zones. Symbiosis 4:63-74
18. Fiala-Médioni A, Alayse AM, Cahet G (1986) Evidence of in situ uptake and incorporation of bicarbonate and amino acids by a hydrothermal vent mussel. J Exp Mar Biol Ecol 96:191-198
19. Fiala-Médioni A, Michalski JC, Jollés J, Alonso C, Montreuil J (1994) Lysosomic and activities in the gill of bivalves from deep hydrothermal vents. C R Acad Sci Ser II Sci Vie 317:239-244
20. Fisher CR (1990) Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Rev Aquat Sci 2:399-436
21. Fisher CR (1995) Toward an appreciation of hydrothermal vent animals: their environment, physiological ecology, and tissue stable isotope values. In: Seafloor hydrothermal systems: physical, chemical, biological, and geological interactions. American Geophysical Union, Washington DC, pp 297-316
22. Fisher CR, Childress JJ, Oremland RS, Bidigare RR (1987) The importance of methane and thiosulfate in the metabolism of the bacterial symbionts of two seep-sea mussels. Mar Biol 96:59-71
23. Fisher CR, Childress JJ, Arp AJ, Brooks JM, Distel D, Favrizzi JA, Felbeck H, Hessler R, Johnson KS, Kennicut II MC, Macko SA, Newton A, Powell MA, Somero GN, Soto T (1988) Microhabitat variation in the hydrothermal vent mussel, Bathymodiolus thermophilus, at the Rose Garden vent on the Galapagos Rift. Deep-Sea Res 35:1769-1791
24. Fisher CR, Brooks JM, Vodenichar JS, Zande JM, Childress JJ, Burke Jr RA (1993) The co-occurrence of methanotrophic and chemoautotrophic sulfur-oxidizing bacterial symbionts in a deep-sea mussel. Mar Ecol 14:277-289
25. 13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13-47.
26. Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439-471
27. Harder W, Attwood MM, Quayle JR (1973) Methanol assimilation by Hyphomicrobium sp. J Gen Microbiol 78:155-163
28. Ivanoff MV, Yu Lein A, Galchenco VF (1993) The oceanic global methane cycle. In: Oremland RS (ed) Biogeochemistry of global change. Chapman and Hall, New York, pp 505-520
29. Jouanneau Y, Tabita FR (1986) Independent regulation of synthesis of form I and form II ribulose bisphosphate carboxylase-oxygenase in Rhodopseudomonas sphaeroides. J Bacteriol 165:620-624
30. Laemmli EK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
31. Langmuir CH, Humphris S, Fornari D, Van Dover C, Damm KV, Tivey MK, Colodner D, Charlou JL, Desonie D, Wilson C, Fouquet Y, Klinkhammer G, Bougault H (1997) Hydrothermal vents near a mantle hot spot: the Lucky-Strike vent field at 37°N on the Mid-Atlantic Ridge. Earth Planet Sci Lett 148:69-91
32. Lee RW, Thuesen EV, Childress JJ, Fisher CR (1992) Ammonium and free amino acid uptake by a deep-sea mussel (Bathymodiolus sp., undescribed) containing methanotrophic bacterial symbionts. Mar Biol 113:99-106
33. Margulis L, Fester R (1991) Symbiosis as a source of evolutionary innovation. MIT Press, Cambridge, Mass.
34. Nelson D, Fisher C (1995) Chemoautotrophic and methanotrophic endosymbiotic bacteria at deep-sea vents and seeps. In: Karl D (ed) Microbiology of deep-sea hydrothermal vents. CRC, Boca Raton, Fla.
35. Robinson JJ, Cavanaugh CM (1995) Expressions of form I and form II Rubisco in chemoautotrophic symbioses: implications for the interpretation of stable carbon isotope values. Limnol Oceanogr 40:1496-1502
36. Robinson JJ, Polz MF, Fiala-Médioni A, Cavanaugh CM (1998) Physiological and immunological evidence for two distinct Cl-utilizing pathways in Bathymodiolus puteoserpentis, a dual endosymbiotic mussel from the Mid-Atlantic Ridge. Mar Biol 132:625-633
37. Somero GN, Anderson AE, Childress JJ (1989) Transport, metabolism and detoxification of hydrogen sulfide in animals from sulfide-rich marine environments. Rev Aquat Sci 1:591-614
38. Stephens RL, Haygood MG, Lidstrom ME (1988) Identification of putative methanol dehydrogenase (moxF) structural genes in methylotrophs and cloning of moxF genes from Methylococcus capsulatus Bath and Methylomonas albus BG8. J Bacteriol 170:2063-2069
39. Tabita FR (1988) Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganisms. Microbiol Rev 52:155-189
40. 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
41. Van Dover CL, Fry B (1989) Stable isotopic compositions of hydrothermal vent organisms. Mar Biol 102:257-263
42. Van Dover CL, Desbruyères D, Segonzac M, Comtet T, Saldanha L, Fiala-Médioni A, Langmuir C (1996) Biology of the Lucky-Strike hydrothermal field. Deep-Sea Res 43:1509-1529
43. Von Cosel R, Comtet T, Krylova E (1999) Bathymodiolus (Bivalvia: Mytilidae) from the hydrothermal vents on the Azores Triple Junction and the Logatchev hydrothermal field, Mid-Atlantic Ridge. Veliger 42:218-248
44. Whittenbury R, Davies SL, Davey JF (1970) Exospores and cysts formed by methane-utilizing bacteria. J Gen Microbiol 61:219-226
45. Wishnick M, Lane MD (1971) Ribulose diphosphate carboxylase from spinach leaves. Meth Enzymol 23:570-577