Influence of CH4 and H2S availability on symbiont distribution, carbon assimilation and transfer in the dual symbiotic vent mussel Bathymodiolus azoricus

Biogeosciences

Volumn 5, Issue 6, 2008, Pages 1681-1691

  Riou, V ^a,b   Halary, S ^c,d   Duperron, S ^c,d   Bouillon, S ^b,e,f   Elskens, M ^b   Bettencourt, R ^a   Santos, R S ^a   Dehairs, F ^b   Colaco A ^a  

^a UNIVERSITY OF THE AZORES   (Portugal)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c SORBONNE UNIVERSITÉ   (France)

^d CNRS   (France)

^e NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^f UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); BATHYMODIOLUS; BATHYMODIOLUS AZORICUS;

EID: 77952353564     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-5-1681-2008     Document Type: Article

References (49)

1. Abramoff, M. D., Magelhaes, P. J., and Ram, S. J.: Image processing with Image J, Biophotonics Int., 11, 36-42, 2004.
2. Arndt, C., Gaill, F., and Felbeck, H.: Anaerobic sulfur metabolism in thiotrophic symbioses, J. Exp. Biol., 204, 741-750. 2001. (Pubitemid 34861174)
3. Baxter, J., Hirt, R., Bodrossy, L., Kovacs, K., Embley, T., Prosser, J., and Murrell, J.: The ribulose-1,5-bisphosphate carboxylase/oxygenase gene cluster of Methylococcus capsulatus (Bath), Arch. Microbiol., 177, 279-289, 2002. (Pubitemid 34230664)
4. 2 in two hydrothermal vent animals, the mussel Bathymodiolus thermophilus and the tube worm Riftia pachyptila, Biol. Bull., 170, 110-121, 1986.
5. Bettencourt, R., Roch, P., Stefanni, S., Rosa, D., Colaço, A., and Santos, R. S.: Deep sea immunity: unveiling immune constituents from the hydrothermal vent mussel Bathymodiolus azoricus, Mar. Environ. Res., 64(2), 108-127, 2007. (Pubitemid 46990516)
6. Bettencourt, R., Dando, P., Rosa, D., Riou, V., Colaço, A., Sarrazin, J., Sarradin, P. M., and Santos, R. S.: Changes of gill and hemocyte- related bio-indicators during long term maintenance of the vent mussel Bathymodiolus azoricus held in aquaria at atmospheric pressure, Comp. Biochem. Physiol., Part A, 150(1), 1-7, 2008.
7. Cavanaugh, C. M., Levering, P. R., Maki, J. S., Mitchell, R., and Lidstrom, M. E.: Symbiosis of methylotrophic bacteria and deepsea mussels, Nature, 325, 346-347, 1987.
8. Cavanaugh, C. M., Wirsen, C. O., and Jannasch, H. W.: Evidence for methanotrophic symbionts in a hydrothermal vent mussel (Bivalvia: Mytilidae) from the Mid-Atlantic Ridge, Appl. Environ. Microb., 58, 3799-3803, 1992.
9. Childress, J. J., Fisher, C. R., Brooks, J. M., Kennicutt, M. C., Bidigare, R., and Andreson, A. E.: A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas, Science, 233(4770), 1306-1308, 1986.
10. 13C signature of hydrothermal mussels is related with the end-member fluid concentration of H2S and CH4 at the Mid-Atlantic Ridge hydrothermal vent fields, Cah. Biol. Mar., 43, 259-262, 2002a. (Pubitemid 36022073)
11. Colaço, A. and Santos, R. S.: LABHORTA, A Land-based laboratory for vent studies, in Towards Planning of Sea-floor Observatory Programs for the MAR region (Proceedings of the II Mo-MAR Workshop), Arquipélago, Life and Marine Sciences, Supplement 3, XII, edited by: Santos, R. S., Escartin, J., Colaço, A., and Adamczewska, A., 36, 2002b.
12. Company, R., Serafim, A., Cosson, R. P., Fiala-Médioni, A., Camus, L., Colaço, A., Santos, R. S., and Bebianno, M. J.: Antioxidant biochemical responses to long-term copper exposure in Bathymodiolus azoricus from Menez-Gwen hydrothermal vent, Sci. Total Environ., 389(2-3), 407-417, 2008. (Pubitemid 350101752)
13. Desbruyères, D., Almeida, A., Biscoito, M., Comtet, T., Khripounoff, A., Le Bris, N., Sarradin, P. M., and Segonzac, M.: A review of the distribution of hydrothermal vent communities along the northern Mid-Atlantic Ridge: dispersal vs. environmental controls, Hydrobiologia, 440, 201-216, 2000. (Pubitemid 32228534)
14. de Zwaan, A., de Bont, A. M. T., and Hemelraad, J.: The role of phosphoenolpyruvate carboxykinase in the anaerobic metabolism of the sea mussel Mytilus edulis, J. Comp. Physiol., 153B, 267-274, 1983.
15. Dixon, D. R., Pruski A. M., and Dixon, L. R. J.: The effects of hydrostatic pressure change on DNA integrity in the hydrothermalvent mussel Bathymodiolus azoricus: implications for future deep-sea mutagenicity studies, Mutat. Res., 552, 235-246, 2004. (Pubitemid 39036830)
16. Duperron, S., Nadalig, T., Caprais, J. C., Sibuet, M., Fiala-Médioni, A., Amann, R., and Dubilier, N.: Dual symbiosis in a Bathymodiolus sp. mussel from a methane seep on the Gabon continental margin (Southeast Atlantic): 16S rRNA phylogeny and distribution of the symbionts in gills, Appl. Environ. Microb., 71(4), 1694-1700, 2005. (Pubitemid 40546083)
17. Duperron, S., Bergin, C., Zielinski, F., Blazejak, A., Pernthaler, A., McKiness, Z. P., DeChaine, E., Cavanaugh, C. M., and Dubilier, N.: 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, 2006. (Pubitemid 44025336)
18. Duperron, S., Sibuet, M., MacGregor, B. J., Kuypers, M. M. M., Fisher, C. R., and Dubilier, N.: Diversity, relative abundance and metabolic potential of bacterial endosymbionts in three Bathymodiolus mussel species from cold seeps in the Gulf of Mexico, Environ. Microbiol., 9, 1423-1438, 2007. (Pubitemid 46763522)
19. Duperron, S., Laurent, M. C. Z., Gaill, F., and Gros, O.: Sulphuroxidizing extracellular bacteria in the gills of Mytilidae associated with wood falls, FEMS Microbiol. Ecol., 63(3), 338-349, 2008. (Pubitemid 351208041)
20. Elsaied, H. E., Kaneko, R., and Naganuma, T.: Molecular characterization of a deep-sea methanotrophic mussel symbiont that carries a RuBisCO Gene, Mar. Biotechnol., 8, 511-520, 2006. (Pubitemid 44663648)
21. Fiala-Médioni, A., Alayse, A. M., and Cahet, G.: 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, 1986.
22. Fiala-Médioni, A., McKiness, Z. P., Dando, P., Boulegue, J., Mariotti, A., Alayse-Danet, A. M., Robinson, J. J., and Cavanaugh, C. M.: Ultrastructural, biochemical, and immunological characterization of two populations of the mytilid mussel Bathymodiolus azoricus from the Mid-Atlantic Ridge: evidence for a dual symbiosis, Mar. Biol., 141, 1035-1043, 2002. (Pubitemid 36128303)
23. Fisher, C. R.: Chemoautotropic and methanotrophic symbioses in marine invertebrates, Crit. Rev. Aquat. Sci., 2, 399-436, 1990.
24. Fisher, C. R. and Childress, J. J.: Organic carbon transfer from methanotrophic symbionts to the host hydrocarbon-seep mussel, Symbiosis, 12, 221-235, 1992.
25. Fisher, C. R., Brooks, J. M., Vodenichar, J. S., Zande, J. M., Childress, J. J., and Burke Jr., R. A.: The co-occurrence of methanotrophic and chemoautotrophic sulfur oxidizing bacterial symbionts in a deep-sea mussel, Mar. Ecol., 14, 277-289, 1993. (Pubitemid 2030760)
26. 2 assimilation in marine nitrifying bacteria: an enzymatic approach, Mar. Biol., 74, 295-300, 1983.
27. Grieshaber, M. K., Hardewig I., Kreutzer, U., and Pörtner, H. O.: Physiological and metabolical responses to hypoxia in invertebrates, Rev. Physiol. Bioch. P., 125, 43-147, 1994.
28. Halary, S., Riou, V., Gaill, F., Boudier, T., and Duperron, S.: 3D FISH for the quantification of methane- and sulphur-oxidizing endosymbionts in bacteriocytes of the hydrothermal vent mussel Bathymodiolus azoricus, ISME J., 2(3), 284-292, 2008. (Pubitemid 351334277)
29. Kadar, E., Bettencourt, R., Costa, V., Santos, R. S., Lobo-da-Cunha, A., and Dando, P.: Experimentally induced endosymbiont loss and re-acquirement in the hydrothermal vent bivalve Bathymodiolus azoricus, J. Exp. Mar. Biol. Ecol., 318, 99-110, 2005.
30. Kates, M.: Bacterial lipids, Adv. Lipid Res., 2, 17-90, 1964.
31. 13C-labelled fatty acids, Environ. Microbiol., 5(11), 1155-1167, 2003a. (Pubitemid 37417787)
32. Knief, C., Lipski, A., and Dunfield, P. F.: Diversity and activity of methanotrophic bacteria in different upland soils, Appl. Environ. Microb., 69(11), 6703-6714, 2003b. (Pubitemid 37420208)
33. Kochevar, R. E., Childress, J. J., Fisher, C. R., and Minnich, E.: The methane mussel: Roles of symbiont and host in the metabolic utilization of methane, Mar. Biol., 112, 389-401, 1992.
34. Lee, R. W. and Childress, J. J.: Assimilation of inorganic nitrogen by seep mytilid Ia, an undescribed deep-sea mussel containing methanotrophic endosymbionts: Fate of assimilated nitrogen and the relation between methane and nitrogen assimilation, Mar. Ecol. Prog. Ser., 123, 137-148, 1995. (Pubitemid 26463206)
35. Müller-Kraft, G., Uhlenhut, J., and Babel, W.: Heterotrophic carbon dioxide fixation by a methylotrophic Ancylobacter species, J. Basic Microb., 31 (4), 317-319, 1991.
36. Nelson, D. C., Hagen, K. D., and Edwards, D. B.: The gill symbiont of the hydrothermal vent mussel Bathymodiolus thermophilus is a psychrophilic, chemoautotrophic, sulfur bacterium, Mar. Biol., 121, 487-495, 1995.
37. Pearson, A., Brocks, J. J., and Budin, M.: Phylogenetic and biochemical evidence for sterol biosynthesis in the bacterium Gemmata obscuriglobus, P. Natl. Acad. Sci. USA, 100(26), 15352-15357, 2003. (Pubitemid 38020993)
38. Pruski, A. M., Rousse, N., Fiala-Médioni, A., and Boulègue, J.: Sulphur signature in the hydrothermal vent mussel Bathymodiolus azoricus from the mid-Atlantic Ridge, J. Mar. Biol. Assoc. UK, 82(3), 463-468, 2002.
39. Robinson, J. J., Polz, M. F., Fiala-Médioni, A., and Cavanaugh, C. M.: Physiological and immunological evidence for two distinct pathways in Bathymodiolus puteoserpentis (Bivalvia: Mytilidae), a dual endosymbiotic mussel from the Mid-Atlantic Ridge, Mar. Biol., 132, 625-633, 1998. (Pubitemid 29006793)
40. Salerno, J., Macko, S. A., Hallam, S. J., Bright, M., Won, Y.-J., McKiness, Z., and Van Dover, C. L.: Characterization of Symbiont Populations in Life-History Stages of Mussels From Chemosynthetic Environments, Biol. Bull., 208, 145-155, 2005. (Pubitemid 40589415)
41. Sarradin, P. M., Caprais, J. C., Riso, R., Comtet, T., and Aminot, A.: Brief account of the chemical environment at hydrothermal vent mussel beds on the MAR, Cah. Biol. Mar., 39, 253-254, 1998. (Pubitemid 29311899)
42. Sibuet, M. and Olu, K.: Biogeography, biodiversity and fluid dependence of deep sea cold seep communities at active and passive margins, Deep-Sea Res. Part II, 45, 517-567, 1998. (Pubitemid 28338374)
43. Schobert, P. and Bowien, B.: Unusual C3 and C4 metabolism in the chemoautotroph Alcaligenes eutrophus, J. Bacteriol., 159(1), 167-172, 1984. (Pubitemid 14084956)
44. Smith, K. L. J.: Deep-sea hydrothermal vent mussels: nutritional state and distribution at the Galapagos rift, Ecology, 66, 1067-1080, 1985.
45. Streams, M. E., Fisher, C. R., and Fiala-Médioni, A.: Methanotrophic symbiont location and fate of carbon incorporated from methane in a hydrocarbon seep mussel, Mar. Biol., 129(3), 465-476, 1997. (Pubitemid 27441782)
46. Trask, J. L. and Van Dover, C. L.: 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, 1999. (Pubitemid 29150782)
47. Van Dover, C. L.: The ecology of deep-sea hydrothermal vents, Princeton University Press, Princeton, N. J., 192-194, 2000.
48. White, D. C., Davis, W. M., Nickels, J. S., King, J. D., and Bobbie, R. J.: Determination of the sedimentary microbial biomass by extractable lipid phosphate, Oecologia, 40, 51-62, 1979.
49. Won, Y. J., Hallam, S. J., O'Mullan, G. D., Pan, I. L., Buck, K. R., and Vrijenhoek, R. C.: Environmental Acquisition of Thiotrophic Endosymbionts by Deep-Sea Mussels of the Genus Bathymodiolus, Appl. Environ. Microb., 69(11), 6785-6792, 2003. (Pubitemid 37420218)