Skip to main content
SpringerLink
Log in

How does the annelid Alvinella pompejana deal with an extreme hydrothermal environment?

  • Review
  • Published:
Reviews in Environmental Science and Bio/Technology Aims and scope Submit manuscript

Abstract

Alvinella pompejana, the so-called Pompeii worm (Desbruyères and Laubier, 1980), is found exclusively in association to high temperature venting, at the surface of hydrothermal chimneys of the East Pacific Rise. The main characteristics of this emblematic species is its tolerance to high temperature but its ability to colonize extremely hot substrates has been the subject of much controversy. In the last decade, new tools allowing in situ and in vivo investigation have been determinant in the understanding of the strategies and adaptations required to colonize such an extremely hot environment. New data relative to the characterization of the animal habitat conditions, on one hand, to the molecular adaptations of this organism and the colonization processes by this species, on the other hand, are now available. Advanced methods and tools, that have fostered the physico-chemical characterization of vent habitats in recent years, are first reviewed. Factors controlling the physico-chemical variability of vent habitats and the threats A. pompejana might effectively face are discussed. The exceptional thermotolerance of this species and the maximum temperature it could sustain are then considered in the light of molecular data relative to its collagen stability. Life history traits as well as biological controls on tube micro-habitat conditions are discussed on the basis of new in situ and in vivo experiments and characterization. Finally, the current knowledge and opened questions related to the molecular adaptations to chemical stresses are briefly stated. The ability of Alvinella pompejana to colonize these substrates is far from being fully understood, but the exceptional properties of its extracellular biopolymers and the behavior of the worm can be now considered as major clues in the colonization process. Alvinella pompejana could thus stand at the limits authorized for its biological machinery in a highly dynamic environment where temperature can readily reach lethal values, but where temperature regulation by the animal itself would prevent exposure to deleterious thermal spikes. The dynamic system associating this pioneer species and its associated microflora might be viewed as a key to the subsequent colonization of these environments by less tolerant species, highlighting A. pompejana as a new type of ecosystem bioengineer.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alain K, Zbinden M, Le Bris N, Lesongeur F, Querellou J, Gaill F, Cambon-Bonavita M-A (2004) Early steps in microbial colonisation processes at deep-sea hydrothermal vents. Environ Microbiol 6(3):227–241

    Google Scholar 

  • Aller RC (1982) The effects of macrobenthos on chemical properties of marine sediment and overlying water. In: McCall PL, Tevesz MJS (eds) Animal-sediment relations. Plenum Press, New York, pp 53–102

    Google Scholar 

  • Arvidson RS, Morse JW, Joye SB (2004) The sulfur biogeochemistry of chemosynthetic cold seep communities, Gulf of Mexico, USA. Marine Chemistry 87, 97–119

    Google Scholar 

  • Auerbach G, Gaill F, Jaenike R, Schulthess T, Timpl R, Engel J (1995) Pressure dependence of collagen melting. Matrix Biol 14:589–592

    CAS  Google Scholar 

  • Bach W, Edwards KJ (2003) Iron and sulfide oxidation within the basaltic ocean crust: implications for chemolithoautotrophic microbial biomass production. Geochim Cosmochim Acta 67:3871–3887

    CAS  Google Scholar 

  • Bates AE, Tunnicliffe V, Lee RW (2005) Role of thermal conditions in habitat selection by hydrothermal vent gastropods. Mar Ecol Prog Series 305:1–15

    Google Scholar 

  • Burjanadze TV (2000) New analysis of the phylogenetic change of collagen thermostability. Biopolymer 53:523–528

    CAS  Google Scholar 

  • Campbell BJ, Jeanthon C, Kosta 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 Microbiol 67:4566–4572

    CAS  Google Scholar 

  • Campbell BJ, Stein JL, Cary SC (2003) Evidence of chemolithoautotrophy in the baterial community associated with Alvinella pompejana, a hydrothermal vent polychaete. Appl Environ Microbiol 69:5070–5078

    CAS  Google Scholar 

  • Cary SC, Cottrell MT, Stein JL, Camacho F, Desbruyères D (1997) Molecular identification and localization of filamentous symbiotic bacteria associated with the hydrothermal vent annelid Alvinella pompejana. Appl Environ Microbiol 63:1124–1130

    CAS  Google Scholar 

  • Cary SC, Shank T, Stein J (1998) Worms bask in extreme temperatures. Nature 391:545–546

    CAS  Google Scholar 

  • Charlou JL, Donval JP, Fouquet Y, Jean-Batiste P, Holm N (2002) Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14′, MAR). Chem Geol 191:345–359

    CAS  Google Scholar 

  • Chevaldonné P, Desbruyères D, Le Haître M (1991) Time-series of temperature from three deep-sea hydrothermal vent sites. Deep-Sea Res 38:1417–1430

    Google Scholar 

  • Chevaldonné P, Desbruyères D, Childress JJ (1992) And some even hotter. Nature 359:593

    Google Scholar 

  • Chevaldonné P, Jollivet D (1993) Videoscopic study of deep-sea hydrothermal vent alvinellid polychaete populations: biomass estimation and behaviour. Mar Ecol Prog Series 95:251–262

    Article  Google Scholar 

  • Chevaldonné P, Fisher CR, Childress JJ, Desbruyères D, Jollivet D, Zal F, Toulmond A (2000) Thermotolerance and the “Pompeii worms. Mar Ecol Progr Series 208:293–295

    Google Scholar 

  • Childress JJ, Fisher CR (1992) The biology of hydrothermal vent animals: physiology, biochemistry and autotrophic symbioses. In: Barnes M, Ansell AD, Gibson RN (eds) Ocean. Mar. Biol. Ann. Review. UCL press, pp 337–441

  • Childress JJ, Lee RW, Saunders NK, Felbeck H, Oros DR, Toulmond A, Desbruyères D, Kennicutt MC, Brooks J (1993) Inorganic carbon uptake in hydrothermal vent tubeworms facilitated by high environmental pCO2. Nature 362:147–149

    CAS  Google Scholar 

  • Desbruyères D, Gaill F, Laubier L, Fouquet Y (1985) Polychaetous annelids from hydrothermal vent ecosystems: an ecological overview. Biol Soc Washington Bull 6:103–116

    Google Scholar 

  • Desbruyères D, Chevaldonne P, Alayse-Danet AM, Caprais JC, Cosson R, Gaill F, Guezennec J, Hourdez S, Jollivet D, Jouin-Toulmond C, Lallier FH, Laubier L, Riso R, Sarradin PM, Toulmond A, Zal F (1998) Burning subjects: biology and ecology of the “Pompei worm” (Alvinella pompejana Desbruyères et Laubier), a normal dweller of an extreme deep-sea environment. Deep-Sea Res II 45:383–422

    Google Scholar 

  • Desbruyères D, Almeida A, Biscoito M, Comtet T, Khripounoff A, Le Bris N, Sarradin PM, Segonzac M (2000) A review of the distribution of hydrothermal vent communities along the Northern Mid Atlantic Ridge: dispersal vs environmental controls. Hydrobiology 440:201–216

    Google Scholar 

  • Di Meo CA, Wakefield JR, Cary SC (1999) A new device for sampling small volumes of water from marine microenvironments. Deep-Sea Res I 46:1279–1287

    CAS  Google Scholar 

  • Di Meo-Savoie CA, Luther GW III, Cary SC (2004) Physico-chemical characterization of the microhabitat of the epibionts associated with Alvinella pompejana, a hydrothermal vent annelid. Geochim Cosmochim Acta 68:2055–2066

    CAS  Google Scholar 

  • Douville E, Charlou JL, Oelkers EH, Bienvenu P, Colon CFJ, Donval JP, Fouquet Y, Prieur D, Appriou P (2002) The rainbow vent fluids (36°14′N, MAR): the influence of ultramafic rocks and phase separation on trace metal content in mid-Atlantic Ridge hydrothermal fluids. Chem Geol 184:37–48

    CAS  Google Scholar 

  • Edmond JM, Measures C, Magnum B, Grant B, Sclater FR, Collier R, Hudson A, Gordon LI, Corliss JB (1979) On the formation of metal-rich deposits at ridge crests. Earth Planet Sci Lett 46:19–30

    CAS  Google Scholar 

  • Fisher CR, Childress JJ, Arp AJ, Brooks JM, Distel D, Favuzzi JA, Felbeck H, Hessler R, Johnson KS, Kennicutt MC II, 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

    Google Scholar 

  • Gaill F, Desbruyeres D, Prieur D, Gourret JP (1984) Mise en évidence de communautés bactériennes épibiontes du “Ver de Pompéï” (Alvinella pompejana). CR Acad Sci Paris 298(19):553–558

    Google Scholar 

  • Gaill F, Hunt S (1986) Tubes of deep-sea hydrothermal vent worms Riftia pachyptila (vestimentifera) and Alvinella pompejana (annelida). Mar Ecol Prog Series 34:267–274

    Google Scholar 

  • Gaill F, Bouliguand Y (1987) Alternating positive and negative twist of polymers in an invertebrate integument. Mol Liq Cryst 153:31–41

    Google Scholar 

  • Gaill F, Desbruyeres D, Laubier L (1988a) Relationships between the “Pompeii worms” and their epibiotic bacteria. Oceanol Act 8:147–155

    Google Scholar 

  • Gaill F, Herbage D, Lepescheux L (1988b) Cuticle structure and composition of two hydrothermal vents invertebrates. Oceanol Act 8:155–159

    Google Scholar 

  • Gaill F, Hunt S (1991) The biology of annelid worms from high temperature hydrothermal vent regions. Rev Aquat Sci 4:107–137

    Google Scholar 

  • Gaill F, Wiedeman A, Kuhn K, Timpl R, Engel J (1991) Molecular characterization of cuticle and interstitial collagen from worms collected at deep-sea level. J Mol Biol 221:209–223

    CAS  Google Scholar 

  • Gaill F (1993) Aspects of life development at deep-sea hydrothermal vents. FASEB J 7:558–565

    CAS  Google Scholar 

  • Gaill F, Mann K, Wiedemann H, Engel J, Timpl R (1995). Structural comparison of cuticle and interstitial collagens from annelids living in shallow sea water and at deep-sea hydrothermal vents. J Mol Biol 246:284–294

    CAS  Google Scholar 

  • Gaill F, Zbinden M, Pradillon F (2003) Adaptations of hydrothermal vent organisms to their environment. In: Legakis A, Sfenthourakis S, Polymeni R, Thessalou-Legaki M (eds) 13th International Congress of Zoology. Pensoft, Sofia-Moskow, Athens, pp 513–517

  • Geret F, Riso R, Sarradin PM, Caprais JC, Cosson R (2002) Metal bioaccumulation and storage forms in the shrimp, Rimicaris exoculata, from the Rainbow hydrothermal field (Mid Atlantic Ridge); preliminary approach to the fluid–organism relationship. Cah Biol Mar 43:43–52

    Google Scholar 

  • Girguis PR, Lee RW (2006) Thermal preference and tolerance of alvinellids. Science 312:231

    Google Scholar 

  • Haddad A, Camacho F, Durand P, Cary SC (1995) Phylogenetic characterization of the epibiotic bacteria associated with the hydrothermal vent polychaete Alvinella pompejana. Appl Environ Microbiol 61:1679–1687

    CAS  Google Scholar 

  • Hamaraoui L, Zaoui D, Gaill F. (1998) Biochemical characteristics of collagens from marine invertebrates with special emphasis on Polychaeta and Vestimentifera from deep-sea hydrotermal vents. Cah Biol Mar 39:109–120

    Google Scholar 

  • Hessler RR, Kaharl VA (1995) The deep-sea hydrothermal vent community: an overview. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE (eds) Seafloor hydrothermal systems: physical, chemical, biological and geological interactions. AGU, Washington DC, pp 72–84

    Google Scholar 

  • Hourdez S, Lallier FH, De Cian M-C, Green BN, Weber RE (2000) The gas transfer system in Alvinella pompejana (Annelida Polychaeta, Terebellida). Functional properties of intracellular and extracellular hemoglobins. Physiol Bioch Zool 73:365–373

    CAS  Google Scholar 

  • Hourdez S, Weber RE (2005) Molecular and functional adaptations in deep-sea hemoglobins. J Inorg Biochem 99:130–141

    CAS  Google Scholar 

  • Hurtado LA, Lutz RA, Vrijenhoek RC (2004) Distinct patterns of genetic differentiation among annelids of eastern Pacific hydrothermal vents. Mol Ecol 13:2603–2615

    CAS  Google Scholar 

  • Johnson KS, Beelher CL, Sakamoto-Arnold CM (1986a) A submersible flow analysis system. Anal Chim Acta 179:245–257

    CAS  Google Scholar 

  • Johnson KS, Beelher CL, Sakamoto-Arnold CM, Childress JJ (1986b) In situ measurements of chemical distributions in a deep-sea hydrothermal vent field. Science 231:1139–1141

    CAS  Google Scholar 

  • Johnson KS, Childress JJ, Beelher CL (1988a) Short time temperature variability in the Rose Garden hydrothermal vent field: an unstable deep sea environment. Deep-Sea Res I 35:1711–1721

    Google Scholar 

  • Johnson KS, Childress JJ, Hessler RR, Sakamoto-Arnold CM, Beelher CL (1988b) Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center. Deep-Sea Res I 35:1723–1744

    Google Scholar 

  • Johnson KS, Childress JJ, Beelher CL, Sakamoto CM (1994) Biogeochemistry of hydrothermal vent mussel communities: the deep sea analogue to the intertidal zone. Deep-Sea Res I 41:993–1011

    CAS  Google Scholar 

  • Jouan L, Marco S, Taveau J-C (2003) Revisiting the structure of Alvinella pompejana hemoglobin at 20 Angstrom resolution by cryoelectron microscopy. J Struct Biol 143:33–44

    CAS  Google Scholar 

  • Juniper KS, Jonasson IR, Tunicliffe V, Southward AJ (1992) Influence of tube building polychaete on hydrothermal chimney mineralization. Geology 20:895–898

    Google Scholar 

  • Kadar E, Costa V, Santos RS (2006) Distribution of micro-essential (Fe, Cu, Zn) and toxic (Hg) metals in tissues of two nutritionally distinct hydrothermal shrimps. Sci Tot Environ 358:143–150

    CAS  Google Scholar 

  • Kaule G, Timpl R, Gaill F, Gunzler V (1998) Prolyl activity in tissue homogenates of annelids from deep sea hydrothermal vents. Matrix Biol 17:205–212

    CAS  Google Scholar 

  • Koschinsky A, Seifert R, Halbach P, Bau M, Brasse S, De Carvalho LM, Fonseca N (2002) Geochemistry of diffuse low-temperature hydrothermal fluids in the North Fidji Basin. Geochim Cosmochim Acta 66:1409–1427

    CAS  Google Scholar 

  • Le Bris N, Sarradin PM, Birot D, Alayse-Danet A (2000) A new chemical analyzer for in situ measurement of nitrate and total sulfide over hydrothermal vent biological communities. Marine Chem 72:1–15

    CAS  Google Scholar 

  • Le Bris N, Sarradin PM, Pennec S (2001) A new deep-sea probe for in situ pH measurement in the environment of hydrothermal vent biological communities. Deep Sea Res I 48:1941–1951

    CAS  Google Scholar 

  • Le Bris N, Sarradin PM, Caprais JC (2003) Contrasted sulphide chemistries in the environment of 13°N EPR vent fauna. Deep-Sea Res I 50:737–747

    CAS  Google Scholar 

  • Le Bris N, Zbinden M, Gaill F (2005) Processes controlling the physico-chemical micro-environments associated with Pompeii worms. Deep-Sea Res Part I:10–1083

    Google Scholar 

  • Le Bris N, Govenar B, Le Gall C, Fisher CR (2006a) Variability of physico-chemical conditions in 9°N EPR diffuse flow vent habitat. Mar Chem 98:167–182

    CAS  Google Scholar 

  • Le Bris N, Rodier P, Sarradin P-M, Le Gall C (2006b) Is temperature a good proxy for sulfide in hydrothermal vent habitats? Cah Biol Mar (in press)

  • Lee RW (2003) Thermal tolerance of deep-Sea hydrothermal vent animals for the Northeast Pacific. Biol Bull 205:98–101

    Google Scholar 

  • Luther GW, Reimers CE, Nuzzio DB, Lovalvo D (1999) In situ deployment of voltammetric, potentiometric and amperometric microelectrodes from a ROV to determine dissolved O2, Mn, Fe, S(−2), and pH in porewaters. Environ Sci Tech 33:4352–4356

    CAS  Google Scholar 

  • Luther GW, Glazer BT, Hohmann L, Popp JI, Taillefert M, Rozan TF, Brendel PJ, Theberge SM, Nuzzio DB (2001a) Sulfur speciation monitored in situ with solid state gold amalgam voltammetric microelectrodes: polysulfides as a special case in sediments, microbial mats and hydrothermal vent waters. J Environ Monit 3:61–66

    CAS  Google Scholar 

  • Luther GW, Rozan TF, Taillefert M, Nuzzio DB, Meo CD, Shank TM, Lutz RA, Cary SC (2001b) Chemical speciation drives hydrothermal vent ecology. Nature 410:813–816

    CAS  Google Scholar 

  • Mann K, Mechling DE, Bachinger HP, Eckerson C, Gaill F, Timpl R (1996) Glycosylated threonine but not 4-hydroyproline dominates the triple helix stabilizing positions in the sequence of a hydrothermal vent worm cuticle collagen. J Mol Biol 261:255–266

    CAS  Google Scholar 

  • Marie B, Genard B, Rees J-F, Zal F (2006) Effect of ambient oxygen concentration on activities of enzymatic antioxidant defences and aerobic metabolism in the hydrothermal vent worm, Paralvinella grasslei. Mar Biol (in press)

  • Marsh AG, Mullineaux LS, Young CM, Manahan DT (2001) Larval dispersal potential of the tubeworm. Riftia pachyptila at deep-sea hydrothermal vents. Nature 411:77–80

    CAS  Google Scholar 

  • Martineu P, Juniper SK, Fisher CR, Massoth GJ (1997) Sulfide binding in the body fluids of hydrothermal vent alvinellid polychaetes. Physiol Zool 70:578–588

    Article  CAS  Google Scholar 

  • Mill PJ (1978) Physiology of Annelids, Academic Press, New York, pp 369–339

  • Millero FJ, Hubinger S, Fernandez M, Garnett S (1987a) Oxidation of H2S in seawater as a function of temperature, pH and ionic strength. Environ Sci Tech 21:439–443

    CAS  Google Scholar 

  • Millero FJ, Sotolongo S, Izaguirre M (1987b) The oxidation kinetics of Fe(II) in seawater. Geochimica Cosmochimica Acta 51:793–801

    CAS  Google Scholar 

  • McCollom TM, Shock EL (1997) Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems. Geochim Cosmochim Acta 61:4375–4391

    CAS  Google Scholar 

  • McCollom TM (2000) Geochemical constraints on primary productivity in submarine hydrothermal vent plumes. Deep-Sea Res I 47:85–101

    CAS  Google Scholar 

  • Mullineaux LS, Peterson CH, Micheli F, Mills SW (2003) Successional mechanisms varies along a thermal gradient in hydrothermal fluid flux at deep-sea vents. Ecol Monogr 73:523–542

    Google Scholar 

  • Nakagawa S, Takai K, Inagaki F, Hirayama H, Nunoura T, Horikoshi K, Yoshihiko S (2005) Distribution, phylogenetic diversity and physiological characteristics of epsilon-proteobacteria in deep-sea hydrothermal field. Environ Microbiol 7(10):1619–1632

    CAS  Google Scholar 

  • Piccino P, Viard F, Sarradin P-M, Le Bris N, Le Guen D, Jollivet D (2004) Thermal selection of PGM allozymes in newly founded populations of the thermolerant vent polychaete Alvinella pompejana. Proceedings of the Royal Society of London 271:2351–2359

    Google Scholar 

  • Powell MA, Vetter RD, Somero GN (1987) Sulfide detoxification and energy exploitation by marine animals. In: Dejours P, Taylor CR, Weibel ER (eds) Comparative physiology: life in water and on land. Fidia Research series IX-Liviana press, Padova, pp 241–250

    Google Scholar 

  • Pradillon F, Shillito B, Young CM, Gaill F (2001) Developmental arrest in vent worms embryos. Nature 413:698–699

    CAS  Google Scholar 

  • Pradillon F, Gaill F (2003) Oogenesis characteristics in the hydrothermal vent polychaete Alvinella pompejana. Invert Reprod Develop 43:223–235

    Google Scholar 

  • Pradillon F, Shillito B, Chervin J-C, Hamel G, Gaill F (2004) Pressurized vessels for the study of deep-sea fauna. High Press Res 24:169–172

    Google Scholar 

  • Pradillon F, Zbinden M, Mullineaux LS, Gaill F (2005a) Colonisation of newly-opened habitat by a pioneer species, Alvinella pompejana (Polychaeta: Alvinellidae), at East Pacific Rise vent sites. Mar Ecol Progr Series 302:147–157

    Google Scholar 

  • Pradillon F, Le Bris N, Shillito B, Young CR, Gaill F (2005b) Influence of environmental conditions on early development of the hydrothermal vent polychaete Alvinella pompejana. J Exp Biol 208:1551–1561

    Google Scholar 

  • Pradillon F, Schmidt A, Peplies J, Dubilier N (in press) Identification of early life history stages of marine species with whole-larvae in situ hybridisation assay. Mar Ecol Prog. Series

  • Ravaux J, Gaill F, Le Bris N, Sarradin P-M, Jollivet D, Shillito B (2003) Heat shock response and temperature resistance in the deep-sea vent shrimp Rimicaris Exoculata. J Exp Biol 206:2345–2354

    Google Scholar 

  • Sarradin PM, Caprais JC, Briand P, Gaill F, Shillito B, Desbruyères D (1998) Chemical and thermal description of the Genesis hydrothermal vent community environment (13°N, EPR). Cah Biol Mar 39:159–167

    Google Scholar 

  • Sarradin PM, Caprais JC, Riso R, Kerouel R, Aminot A (1999) Chemical environment of the hydrothermal mussels communities in the Lucky Strike and Menez Gwen vent fields, MAR. Cah Biol Mar 40:93–104

    Google Scholar 

  • Sarrazin J, Juniper SK, Massoth G, Legendre P (1999) Physical and chemical factors influencing species distributions on hydrothermal sulfide edifices of the Juan de Fuca Ridge, Northeast Pacific. Mar Ecol Progr Ser 190:89–112

    CAS  Google Scholar 

  • Shank TM, Fornari DJ, Von Damm KL, Lilley MD, Haymon RM, Lutz RA (1998) Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vents (9°50′N, East Pacific Rise). Deep-Sea Res II 45:465–515

    Google Scholar 

  • Shillito B, Jollivet D, Sarradin PM, Rodier P, Lallier F, Desbruyères D, Gaill F (2001) Temperature resistance of Hesiolyra bergi, a polychaetous annelid living on deep-sea vent smoker. Mar Ecol Progr Ser 216:141–149

    Google Scholar 

  • Shillito B, Le Bris N, Gaill F, Rees JF, Zal F (2004) First access to live Alvinellas. High Press Res 24(1):169–172

    Google Scholar 

  • Shillito B, Le Bris N, Hourdez S, Ravaux J, Cottin D, Caprais J-C, Jollivet D, Gaill F (2006) Temperature resistance studies on the deep-sea vent shrimp Mirocaris fortunate. J Exp Biol 209:945–955

    Google Scholar 

  • Sicot FX, Exposito J-Y, Masselot M, Garrone R, Deutxch J, Gaill F (1997) Cloning of an annelid fibrillar collagen gene and phylogenetic analysis of vertebrate and invertebrate collagens, in: nucleic acids, protein synthesis and molecular genetics. Eur J Biochem 590:1–9

    Google Scholar 

  • Sicot FX, Mesnage M, Masselot M, Exposito J-Y, Garrone R, Deutxch J, Gaill F (2000) Molecular adaptation to an extreme environment: origin of the thermal stability of the Pompeii worm collagen. J Mol Biol 302:811–820

    CAS  Google Scholar 

  • Sung W, Morgan JJ (1980) Kinetics and products of ferrous iron oxygenation in aqueous systems. Environ Sci Tech 14:561–569

    CAS  Google Scholar 

  • Takai K, Campbell BJ, Cary SC, Suzuki M, Oida H, Nunoura T, Hirayama H, Nakagawa S, Suzuki Y, Inagaki F, Horikoshi K (2005) Enzymatic and genetic characterization of carbon and energy metabolisms by deep-sea hydrothermal chemolithoautotrophic isolates of epsilonproteobacteria. Appl Environ Microbiol 71:7310–7320

    CAS  Google Scholar 

  • Tapley DW, Buettner GR, Shick JM (1999) Free radicals and chemiluminescence as products of the spontaneous oxidation of sulfide in seawater, and their biological implications. Biol Bull 196:52–56

    CAS  Google Scholar 

  • Taylor CD, Wirsen CO (1997) Microbiology and ecology of filamentous sulfur formation. Science 277:1483–1485

    CAS  Google Scholar 

  • Taylor CD, Wirsen CO, Gaill F (1999) Rapid microbial production at filamentous sulfur mats at hydrothermal vents. Appl Environ Microbiol 35:2253–2255

    Google Scholar 

  • Tivey MK, McDuff RE (1990) Mineral precipitation in the walls of black smoker chimneys: a quantitative model of transport and chemical reaction. J Geophys Res 95:617–637

    Google Scholar 

  • Tivey MK (1995) Modeling chimney growth and associated fluid flow at seafloor hydrothermal vent sites. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE (eds) Seafloor Hydrothermal Systems: Physical, Chemical, Biological and Geological Interactions. AGU, Washington DC, pp 158–177

    Google Scholar 

  • Tivey MK, Bradley AM, Joyce TM, Kadko D (2002) Insights into tide-related variability at seafloor hydrothermal vents from time-series temperature measurements. Earth Planet Sci Lett 202:693–707

    CAS  Google Scholar 

  • Tivey MK (2004) Environmental conditions within active seafloor vent structures: sensitivity to vent fluid composition and fluid flow. In: Wilcock W, Cary C, DeLong E, Kelley D, Baross J (eds) Subseafloor biosphere at mid-ocean ridges, geophysical monograph series, no. 144. AGU, Washington, DC, pp 137–152

    Google Scholar 

  • Toulmond A, El Idrissi Slitine F, De Frescheville J, Jouin C (1990) Extracellular haemoglobins of hydrothermal vent annelids: structural and functional characteristics in three alvinellid species. Biol Bull 179:366–373

    CAS  Google Scholar 

  • Tunnicliffe V (1991) The biology of hydrothermal vents: ecology and evolution. In: Barnes M (ed) Oceanogr. Mar. Biol. Annu. Rev. Aberdeen University Press, pp 319–407

  • Tunnicliffe V, Juniper SK (1990) Dynamic character of the hydrothermal vent habitat and the nature of the sulphide chimney fauna. Progr Oceanogr 24:1–13

    Google Scholar 

  • Van Dover C, Lutz RA (2004) Experimental ecology at deep-sea hydrothermal vents: a perspective. J Exp Mar Biol Ecol 300:273–307

    Google Scholar 

  • Visman B (1991) Sulfide tolerance: physiological mechanisms and ecological implications. Ophelia 34:1–27

    Google Scholar 

  • Von Damm KL (1995) Controls on the chemistry and temporal variability of seafloor hydrothermal fluids. In: Humphris SE, Zierenberg RA, Mullineaux LS, Thomson RE (eds) Seafloor hydrothermal systems: physical, chemical, biological and geological interactions. AGU, Washington DC, pp 222, 247

    Google Scholar 

  • Von Damm KL, Lilley MD (2004) Diffuse flow hydrothermal fluids from 9°50′N East Pacific Rise: origin, evolution and biogeochemical controls. In: Wilcock W, Cary C, Delong E (eds) Subseafloor biosphere at mid-oceanic ridges. AGU, Washington DC

    Google Scholar 

  • Wirsen CO, Sievert SM, Cavanaugh CM, Molyneaux SJ, Ahmad AR, Taylor LT, DeLong EF, Taylor CD (2002) Characterization of an autotrophic sulfide-oxidizing Marine Arcobacter sp. that produces filamentous sulfur. Appl Environ Microbiol 68:316–325

    CAS  Google Scholar 

  • Zbinden M, Le Bris N, Compère P, Martinez I, Guyot F, Gaill F (2003) Mineralogical gradients associated with Alvinellids at deep-sea hydrothermal vents. Deep-Sea Res I 50:269–280

    CAS  Google Scholar 

  • Zhang JZ, Millero FJ (1994) Kinetics of oxidation of hydrogen sulfide in natural waters. In: Alpers CN, Blowes DW (eds) Environmental geochemistry of hydrogen sulfide in natural waters. ACS, Washington DC, pp 393–411

    Google Scholar 

  • Zal F, Green BN, Martineu P, Lallier FH, Toulmond A, Vinogradov SN, Childress JJ (2000) Polypeptide chain composition diversity of hexagonal-bilayer haemoglobins within a single family of annelids, the Alvinellidae. Eur J Biochem 267:5227–5236

    CAS  Google Scholar 

  • Zal F, Poch O, Bigot Y, Cormier P, Dietrich J, Duchiron F, Gaill F, Higuet D, Hourdez S, Jollivet D, Knoops B, Lallier F, Laullier M, Lecompte O, Leize-Wagner E, Moras D, Rees J-F, Shillito B (in press) Alvinella Consortium: a large scale sequencing project at the French Genoscope. Cah Biol Mar

Download references

Acknowledgements

This work was financially supported by Ifremer, CNRS, INSU (Dorsales and GEOMEX programs), and the European Community (Ventox project EVK3-1999-00056P). We would like to particularly acknowledge the captains and crews of Research Vessels, the Nautile, Alvin and Victor 6000 operation groups, and instrumentation engineers and technicians for their essential support at sea.

Author information

Authors and Affiliations

  1. Département Etude des Ecosystèmes Profonds, Ifremer, Centre de Brest, BP70, Plouzané, 29280, France

    N. Le Bris

  2. Systématique Adaptation et Evolution, UMR 7138 CNRS-IRD-MNHN-UPMC-ENS, 7 quai Saint Bernard, Paris, 75252, France

    F. Gaill

Authors
  1. N. Le Bris
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Gaill
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. Le Bris.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Le Bris, N., Gaill, F. How does the annelid Alvinella pompejana deal with an extreme hydrothermal environment?. Rev Environ Sci Biotechnol 6, 197–221 (2007). https://doi.org/10.1007/s11157-006-9112-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11157-006-9112-1

Keywords

Search

Navigation