Abstract
Specimens of alvinellid polychaetes (Alvinella pompejana Desbruyères and Laubier, 1980 andA. caudata Desbruyères and Laubier, 1986) and their tubes were sampled from deep-sea hydrothermal vents at 13°N from the manned submersible “Nautile” during the “Hydronaut” cruise (October to November 1987) on the East Pacific Rise. Samples were subjected to bacterial analysis aboard the mother ship “Nadir” to detect bacteria involved in the nitrogen and sulphur cycles, in non-specific heterotrophic processes, and displaying resistance to selected heavy metals. Cultures were incubated at different temperatures under atmospheric and “in situ” (250 atm) pressures. Bacterial growth was observed in enrichment cultures for most metabolic types screened. Heavy-metal-resistant bacteria were also detected in many samples. No filamentous bacterial form was observed in the cultures. The results demonstrate a high metabolic diversity in episymbiotic flora, indicating that the worm (A. pompejana orA. caudata), its tube and its epiflora represent a complex micro-ecosystem.
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Literature cited
Abd El Malek, Y., Rizk, S. G. (1958). Counting of sulphate reducing bacteria in mixed bacterial populations. Nature, Lond. 182: p. 538
Adair, F. W., Gundersen, K. (1969). Chemoautotrophic sulfur bacteria in the marine environment: isolation, cultivation and distribution. Can. J. Microbiol. 15: 345–353
Alayse-Danet, A. M. (1988). Rapport préliminaire des recherches effectuées pendant la campagne “Hydronaut”. Ifremer/DERO/EP (Département Etudes et Recherche Océaniques/Environnement Profond), Brest, France
Alayse-Danet, A. M., Gaill, F., Desbruyères, D. (1986).In situ bicarbonate uptake by bacteria-Alvinella associations. Mar. Ecol. 7: 233–240
Belliveau, B. H., Starodub, M. E., Cotter, C., Trevors, J. T. (1987). Metal resistance and accumulation in bacteria. Biotech. Adv. 5: 101–127
Baross, J. A., Deming, J. W. (1985). The role of bacteria in the ecology of black smoker environments. Bull. biol. Soc. Wash. 6: 355–371
Baross, J. A., Lilley, M. D., Gordon, L. I. (1982). Is the CH4, H2 and CO venting from submarine hydrothermal systems produced by thermophilic bacteria? Nature, Lond. 298: 366–368
Cavanaugh, C. M:, Gardiner, S. L., Jones, M. L., Jannasch, H. W., Waterbury, J. B. (1981). Prokaryotic cells in the hydrothermal vent tube wormRiftia pachyptila Jones: possible chemoautotrophic symbionts. Science, N.Y. 213: 340–342
Chamroux, S. (1972). Etude des bactéries marines réduisant le nitrate. 1: Isolement. Annls Inst. Pasteur, Paris 122: 475–481
Cosson-Mannevy, M. A., Cosson, R., Gaill, F. (1986). Mise en évidence de protéines de type métallothionéine chez deux invertébrés des sources hydrothermales, le pogonophore vestimentifèreRiftia pachyptila et l'annélide polychèteAlvinella pompejana. C. r. hebd. Séanc. Acad. Sci., Paris 302: 347–352
Desbruyères, D., Crassous, P., Crassle, J., Khripounoff, A., Reyss, D., Rio, M., Van Praet, M. (1982). Données écologiques sur un nouveau site d'hydrothermalisme actif de la ride du Pacifique oriental. C. r. hebd. Séanc. Acad. Sci., Paris 295: 489–494
Desbruyères, D., Gaill, F., Laubier, L., Fouquet, Y. (1985). Polychaetous annelids from hydrothermal vent ecosystem: an ecological review. Bull. biol. Soc. Wash. 6: 103–116
Desbruyères, D., Gaill, F., Laubier, L., Prieur, D., Rau, G. H. (1983). Unusual nutrition of the “Pompeii worm”Alvinella pompejana (polychaetous annelid) from a hydrothermal vent environment: SEM, TEM,13C and15N evidence. Mar. Biol. 76: 201–205
Desbruyères, D., Laubier, L. (1980).Alvinella pompejana gen. sp. nov., Ampharetidae aberrant des sources hydrothermales de la ride Est-Pacifique. Oceanol. Acta 3: 267–274
Desbruyères, D., Laubier, L. (1982).Paralvinella grasslei, new genus, new species of Alvinellidae (Polychaeta: Ampharaetidae) from the Galapagos rift geothermal vents. Proc. biol. Soc. Wash. 95: 484–494
Desbruyères, D., Laubier, L. (1986). Les Alvinellidae, une famille nouvelle d'annélides polychètes inféodées aux sources hydrothermales sous marines: systématique, biologie et écologie. Can. J. Zool. 64: 2227–2245
Felbeck, H., Somero, G. N. (1982). Primary production in deep-sea hydrothermal vent organisms: role of sulfide-oxidizing bacteria. Trends biochem. Sciences 7: 201–204
Fiala-Médioni, A. (1984). Mise en évidence par microscopie électronique à transmission de l'abondance de bactéries symbiotiques dans la branchie de mollusques bivalves de sources hydrothermales profondes. C. r. hebd. Séanc. Acad. Sci., Paris 298: 487–492
Gaill, F., Desbruyères, D., Prieur, D. (1987). Bacterial communities associated with “Pompeii worms” from the East Pacific Rise hydrothermal vents: SEM, TEM observations, Microb. Ecol. 13: 129–139
Gaill, F., Desbruyères, D., Prieur, D., Gourret, J. P. (1984a). Mise en évidence de communautés bactériennes épibiontes du “ver de Pompéi” (Alvinella pompejana). C. r. hebd. Séanc. Acad. Sci., Paris 298: 553–558
Gaill, F., Halpern, S., Quintana, C., Desbruyères, D. (1984b). Présence intracellulaire d'arsenic et de zinc associés au soufre chez un Polychète des sources hydrothermales. C. r. hebd. Séanc. Acad. Sci., Paris 298: 331–335
Hajj, H., Makemson, J. (1976). Determination of growth ofSphaerotilus discophorus in the presence of manganese. Appl. envirl Microbiol. 32: 699–702
Jacq, E., Prieur, D., Nichols, P., White, D. C., Porter, T., Geesey, G. G. (1989). Microscopic examination and fatty acid characterization of filamentous bacteria colonizing substrata around subtidal hydrothermal vents. Archs Microbiol. 152: 64–71
Jannasch, H. W., Wirsen, C. O. (1979). Chemosynthetic primary production at East Pacific sea floor spreading centers. BioSci. 29: 592–598
Jannasch, H. W., Wirsen, C. O. (1981). Morphological survey of microbial mats near deep-sea thermal vents. Appl. envirl Microbiol. 41: 428–538
Jeanthon, C., Prieur, D. (1990). Resistance to heavy metals of heterotrophic bacteria isolated from the deep-sea hydrothermal vent polychaeteAlvinella pompejana. Prog. Oceanogr. (in press)
Johnson, I., Flower, N., Loutit, M. W. (1981). Contribution of periphytic bacteria to the concentration of chromium in the crabHelice crassa. Microb. Ecol. 7: 245–252
Kobayashi, T., Enomoto, R., Sakazaki, R., Kuwuhara, S. (1963). A new selective isolation medium for pathogenicVibrios: TCBS agar. Jap. J. Bact. 18: 387–391
Laubier, L., Desbruyères, D., Chassard-Bouchaud, C. (1983). Microanalytical evidence of sulfur accumulation in a polychaete from deep-sea hydrothermal vents. Mar. Biol. Lett 4: 113–116
Le Pennec, M., Prieur, D. (1984). Observations sur la nutrition d'un Mytilidae d'un site d'hydrothermalisme actif de la dorsale du Pacifique oriental. C. r. hebd. Séanc. Acad. Sci., Paris 298: 493–498
Lewis, R. F., Pramer, D. (1958): Isolation ofNitrosomonas in pure culture. J. Bact. 76: 524–528
Lilley, M. D., Baross, J. A., Gordon, L. I. (1983). Reduced gases and bacteria in hydrothermal fluids: the Galapagos spreading center and 21°N East Pacific Rise. In: Rona, P. A., Böstrom, K., Laubier, L., Smith, K. L., Jr. (eds.) Hydrothermal processes at sea floor spreading centers. Plenum Press, New York, p. 411–419
Mevel, G. (1986). Contribution à l'étude de la nitrification dans l'eau et le sédiment d'écosystèmes littoraux et estuariens. Etudein situ et expérimentale. Thèse doctorat d'Etat. Université de Brest
Nealson, K. H. (1978). The isolation and characterization of marine bacteria which catalyse manganese oxidation. In: Krumbein, W. E. (ed.) Environmental biogeochemistry and geomicrobiology. Vol. 3. Ann Arbor Science Publishers Inc., Ann Arbor, Michigan, p. 847–858
Nelson, D. C., Jannasch, H. W. (1983). Chemoautotrophic growth of a marineBeggiatoa in sulfide-gradient cultures. Archs Microbiol. 136: 262–269
Oeschger, R., Schmaljohann, R. (1988). Association of various type of epibacteria withHalicryptus spinulosus (Priapulidae). Mar. Ecol. Prog. Ser. 48: 285–293
Oppenheimer, C. H., Zobell, C. E. (1952). The growth and viability of sixty-three species of marine bacteria as influenced by hydrostatic pressure. J. mar. Res. 11: 10–18
Postgate, J. R. (1966). Media for sulphur bacteria. Lab. Pract. 15: 1239–1244
Postgate, J. R. (1972). The acetylene reduction test for nitrogen fixation. In: Norriss, J. R., Ribbons, P. W. (eds.) Methods in microbiology. Vol. 6B. Academic Press, London, p. 343–356
Prieur, D., Jeanthon, C. (1987). Preliminary study of heterotrophic bacteria isolated from two deep-sea hydrothermal vent invertebrates:Alvinella pompejana (polychaete) andBathymodiolus thermophilus (bivalve). Symbiosis 4: 87–98
Ruby, E. G., Wirsen, C. O., Jannasch, H. W. (1981). Chemolithotrophic sulfur-oxidizing bacteria from the Galapagos rift hydrothermal vents. Appl. envirl Microbiol. 42: 317–324
Sieburth, J. McN. (1975). Microbial seascapes. University Park Press, Baltimore, Md
Sieburth, J. McN. (1987). Contrary habitats for redox-specific processes: methanogenesis in oxic waters and oxidation in anoxic waters. In: Sleigh, M. A. (ed.) Microbes in the sea. Ellis Horwood Ltd., Chichester, p. 11–31
Tuttle, J. H. (1985). The role of sulfur-oxidizing bacteria at deep-sea hydrothermal vents. Bull. biol. Soc. Wash. 6: 335–343
Tuttle, J. H., Jannasch, H. W. (1972). Occurrence and type ofThiobacillus-like bacteria in the sea. Limnol. Oceanogr. 17: 532–543
Tuttle, J. H., Wirsen, C. O., Jannasch, H. W. (1983). Microbial activities in the emitted hydrothermal waters of the Galápagos Rift vents. Mar. Biol. 73: 293–299
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Communicated by J. M. Pérès, Marseille
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Prieur, D., Chamroux, S., Durand, P. et al. Metabolic diversity in epibiotic microflora associated with the Pompeii wormsAlvinella pompejana andA. caudata (Polychaetae: Annelida) from deep-sea hydrothermal vents. Mar. Biol. 106, 361–367 (1990). https://doi.org/10.1007/BF01344313
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DOI: https://doi.org/10.1007/BF01344313