Skip to main content

Adaptations to hypoxia in hydrothermal-vent and cold-seep invertebrates

  • Review Paper
  • Chapter
  • First Online:
Life in Extreme Environments

Abstract

The deep sea harbors very unusual environments, such as hydrothermal vents and cold seeps, that illustrate an apparent paradox: the environmental conditions are very challenging and yet they display a high biomass when compared to the surrounding environment at similar depth. Hypoxia is one of the challenges that these species face to live there. Here, we review specific adaptations of their respiratory system that the species have developed to cope with hypoxia, at the morphological, physiological, and biochemical levels. Most studies to date deal with annelids and crustaceans, and trends can be drawn: development of ventilation and branchial surfaces to help with oxygen extraction, and an increase in finely tuned oxygen binding proteins to help with oxygen storage and transport. Beside these respiratory adaptations most animals have developed enhanced anaerobic capacities and specific ways to deal with sulfide.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Andersen AC, Jolivet S, Claudinot S, Lallier FH (2002) Biometry of the branchial plume in the hydrothermal vent tubeworm Riftia pachyptila (Vestimentifera; Annelida). Can J Zool 80:320–332

    Article  Google Scholar 

  • Arndt C, Schiedek D, Felbeck H (1998) Metabolic response of the hydrothermal vent tubeworm Riftia pachyptila to severe hypoxia. Mar Ecol Prog Ser 174:151–158

    CAS  Google Scholar 

  • Arp AJ, Childress JJ (1981) Blood function in the hydrothermal vent Vestimentiferan tube worm. Science 213:342–344

    Article  CAS  PubMed  Google Scholar 

  • Arp AJ, Childress JJ (1983) Sulfide binding by the blood of the hydrothermal vent tube worm Riftia pachyptila. Science 219:295–297

    Article  CAS  PubMed  Google Scholar 

  • Arp AJ, Childress JJ, Fisher CR Jr (1984) Metabolic and blood gas transport characteristics of the hydrothermal vent bivalve, Calyptogena magnifica. Physiol Zool 57:648–662

    CAS  Google Scholar 

  • Arp AJ, Doyle ML, Di Cera E, Gill SJ (1990) Oxygenation properties of the two co-occurring hemoglobins of the tube worm Riftia pachyptila. Resp Physiol 80:323–334

    Article  CAS  Google Scholar 

  • Ballard RD, Grassle JF (1979) Return to oases of the deep (strange world without a sun). Natl Geogr 156(5):680–703

    Google Scholar 

  • Belman BW, Childress JJ (1976) Circulatory adaptations to the oxygen minimum layer in the Bathypelagic Mysid Gnathophausia ingens. Biol Bull 150(1):15–37

    Article  PubMed  CAS  Google Scholar 

  • Bridges CR, Hupperts V, Eshky AA, Taylor AC (1997) Haemocyanin oxygen transport in Ocypode spp.: modulation of oxygen affinity? J Mar Biol Ass U K 77:145–158

    CAS  Google Scholar 

  • Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube-worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–342

    Article  CAS  PubMed  Google Scholar 

  • Chausson F, Bridges CR, Sarradin PM, Green BN, Riso R, Caprais JC, Lallier FH (2001) Structural and functional properties of hemocyanin from Cyanagraea praedator, a deep-sea hydrothermal vent crab. Proteins 45:351–359

    Article  PubMed  CAS  Google Scholar 

  • Chausson F, Sanglier S, Leize E, Hagège A, Bridges CR, Sarradin, P-M, Shillito B, Lallier FH, Zal F (2004) Respiratory adaptations to the deep-sea hydrothermal vent environment: the case of Segonzacia mesatlantica, a crab from the Mid-Atlantic Ridge. Micron 35:31–41

    Article  PubMed  CAS  Google Scholar 

  • Chevaldonné P (1986) Ecologie des cheminées actives. Ph.D. thesis. Université de Méditerranée, Marseille. 257 pp

    Google Scholar 

  • Chevaldonné P, Desbruyères D, Le Haitre M (1991) Time-series of temperature from three deep-sea hydrothermal vent sites. Deep-Sea Res I 38(11):1417–1430

    Article  Google Scholar 

  • Chevaldonné P, Desbruyères D, Childress JJ (1992) Some like it hot ... and some even hotter. Nature 359:593–594

    Article  Google Scholar 

  • Childress JJ (1975) The respiratory rates of midwater crustaceans as a function of depth of occurrence and relation to the minimum layer off Southern California. Comp Biochem Physiol 50A:787–799

    Article  Google Scholar 

  • Childress JJ, Arp AJ, Fisher CR (1984) Metabolic and respiratory characteristics of the hydrothermal vent tube worm Riftia pachyptila. Mar Biol 83:109–124

    Article  CAS  Google Scholar 

  • Childress JJ, Mickel TJ (1985) Metabolic rates of animals from hydrothermal vents and other deep-sea habitats. Biol Soc Wash Bull 6:249–260

    Google Scholar 

  • Childress JJ, Fischer CR (1992) The biology of hydrothermal vent animals: physiology, biochemistry and autotrophic symbioses. Oceanogr Mar Biol Annu Rev 30:337–441

    Google Scholar 

  • Childress JJ, Seibel BA (1998) Life at stable oxygen levels: adaptations of animals to oceanic oxygen minimum layers. J Exp Biol 201:1223–1232

    PubMed  CAS  Google Scholar 

  • Cordes EE, Hourdez S, Predmore BL, Redding ML, Fisher CR (2005) Succession of hydrocarbon seep communities associated with the long-lived foundation species Lamellibrachia luymesi. Mar Ecol Prog Ser 305:17–29

    CAS  Google Scholar 

  • Corliss JB, Ballard RD (1977) Oases of life in the cold Abyss. Natl Geogr 152(4):441–454

    Google Scholar 

  • Corliss JB, Dymond J, Gordon LI, Edmond JM, Herzen RPV, Ballard RD, Green K, Williams D, Bainbridge A, Crane K, van Andel TH (1979) Submarine thermal springs on the Galápagos Rift. Science 203:1073–1083

    Article  CAS  PubMed  Google Scholar 

  • Desbruyères D, Chevaldonné P, Alayse A-M, Jollivet D, Lallier FH, Jouin-Toulmond C, Zal F, Sarradin P-M, Cosson R, Caprais J-C, Arndt C, O’Brien J, Guezennec J, Hourdez S, Riso R, Gaill F, Laubier L, Toulmond A (1998) Biology and ecology of the pompei worm (Alvinella Pompejana Desbruyères and Laubier), a normal dweller on an extreme deep-sea environment: a synthesis of current knowledge and recent developments. Deep-Sea Res Part II 45:383–422

    Article  Google Scholar 

  • Doeller JE, Grieshaber MK, Kraus DW (2001) Chemolithoheterotrophy in a metazoan tissue: thiosulfate production matches ATP demand in ciliated mussel gills. J Exp Biol 204:3755–3764

    PubMed  CAS  Google Scholar 

  • Felbeck H (1981) Chemoautotrophic potential of the hydrothermal vent tubeworm, Riftia Pachyptila Jones (Vestimentifera). Science 213:336–338

    Article  CAS  PubMed  Google Scholar 

  • Felbeck H, Somero GN, Childress JJ (1981) Calvin-Benson cycle and sulfide oxidation enzymes in animals from sulfide-rich habitats. Nature 293:291–293

    Article  CAS  Google Scholar 

  • Fisher CR, Childress JJ, Arp AJ, Brooks JM, Distel D, Favuzzi JA, Felbeck H, Hessler R, Johnson KS, Kennicutt MC, Macko SA, Newton A, Powell MA, Somero GN, Soto T (1988) Microhabitat variation in the hydrothermal vent mussel Bathymodiolus thermophilus, at Rose Garden vent on the Galapagos Rift. Deep-Sea Res 35(10/11):1769–1792

    Article  Google Scholar 

  • Fisher CR (1995) Toward an appreciation of hydrothermal-vent animals: their environment, physiological ecology, and tissue stable isotope values. In: Humphris SE et al. (eds) Seafloor hydrothermal systems: physical, chemical, biological, and geological interactions. American Geophysical Union, Washington DC, pp 297–316

    Google Scholar 

  • Fisher CR (1996) Ecophysiology of primary production at deep-sea vents and seeps. In: Deep-sea and extreme shallow-water habitats: affinities and adaptations. Austrian Academy of Sciences Press, Vienna, pp 313–336

    Google Scholar 

  • Fisher CR, MacDonald IR, Sassen R, Young CM, Macko SA, Hourdez S, Carney RS, Joye S, McMullin E (2000) Methane ice worms: Hesiocaeca methanicola colonizing fossil fuel reserves. Naturwissenschaften 87:184–187

    Article  PubMed  CAS  Google Scholar 

  • Flores JF, Fisher CR, Carney SL, Green BN, Freytag JK, Schaeffer SW, Royer WE (2005) Sulfide binding is mediated by zinc ions discovered in the crystal structure of a hydrothermal vent tubeworm hemoglobin. Proc Natl Acad Sci USA 102(8):2713–2718

    Article  PubMed  CAS  Google Scholar 

  • Flores JF, Hourdez S The zinc-mediated sulfide-binding mechanism of hydrothermal vent tubeworm 400-Kda hemoglobin. Cah Biol Mar 47(4), (in press)

    Google Scholar 

  • Fox HM, Gilchrist BM, Phear EA (1951) Functions of haemoglobin in Daphnia. Proc R Soc B 138:514–528

    CAS  Google Scholar 

  • Fox HM (1957) Haemoglobin in the crustacea. Nature 179:148

    Article  PubMed  CAS  Google Scholar 

  • Greaves J, Rainer JS, Mangum CP (1992) Size-exclusion high performance liquid chromatography of the Dodecameric and Hexameric forms of hemocyanin from Callinectes sapidus. Mar Biol 113:33–36

    Article  CAS  Google Scholar 

  • Grieshaber MK, Hardewig I, Kreutzer U, Pörtner H-O (1994) Physiological and metabolic responses to hypoxia in invertebrates. Rev Physiol Biochem Pharmacol 125:43–147

    Article  PubMed  CAS  Google Scholar 

  • Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Ann Rev Physiol 60:33–53

    Article  CAS  Google Scholar 

  • Hand SC, Somero GN (1983) Energy metabolism pathways of hydrothermal vent animals: adaptations to a food-rich and sulfide-rich deep-sea environment. Biol Bull 165:167–181

    Article  CAS  Google Scholar 

  • Hessler RR, Jumars PA (1974) Abyssal community analysis from replicate box cores in the Central North Pacific. Deep-sea Res 21:185–209

    Google Scholar 

  • Hourdez S, JouinToulmond C (1998) Functional anatomy of the respiratory system of Branchipolynoe species (Polychaeta, Polynoidae), commensal with Bathymodiolus species (Bivalvia, Mytilidae) from deep sea hydrothermal vents. Zoomorphology 118(4):225–233

    Article  Google Scholar 

  • Hourdez S, Lallier FH, Green BN, Toulmond A (1999a) Hemoglobins from deep-sea hydrothermal vent scaleworms of the genus Branchipolynoe: a new type of quaternary structure. Proteins 34:427–434

    Article  CAS  Google Scholar 

  • Hourdez S, Lallier FH, Martin-Jezequel V, Weber RE, Toulmond A (1999b) Characterization and functional properties of the extracellular coelomic hemoglobins from the deep-sea, hydrothermal vent scaleworm Branchipolynoe symmytilida. Proteins 34(4):435–442

    Article  CAS  Google Scholar 

  • Hourdez S, Lallier FH, De Cian M-C, Green BN, Weber RE, Toulmond A (2000a) Gas transfer system in Alvinella pompejana (Annelida Polychaeta, Terebellida): functional properties of intracellular and extracellular hemoglobins. Phys Biochem Zool 73(3):365–373

    Article  CAS  Google Scholar 

  • Hourdez S, Lamontagne J, Peterson P, Weber RE, Fisher CR (2000b) Hemoglobin from a deep-sea hydrothermal-vent copepod. Biol Bull 199(2):95–99

    Article  CAS  Google Scholar 

  • Hourdez S, Frederick L-A, Schernecke A, Fisher CR (2001) Functional respiratory anatomy of a deep-sea Orbiniid Polychaete from the Brine Pool Nr-1 in the Gulf of Mexico. Inv Biol 120(1):29–40

    Article  Google Scholar 

  • Hourdez S, Weber RE, Green BN, Kenney JM, Fisher CR (2002) Respiratory adaptations in a deep-sea Orbiniid Polychaete from Gulf of Mexico Brine Pool NR-1: metabolic rates and hemoglobin structure/function relationships. J Exp Biol 205:1669–1681

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Johnson KS, Childress JJ, Beehler CL (1988) Short-term temperature variability in the Rose Garden hydrothermal vent field: an unstable deep-sea environment. Deep-Sea Res 35(10/11):1711–1721

    Article  Google Scholar 

  • Johnson L, Rees CJC (1988) Oxygen consumption and gill surface area in relation to habitat and lifestyle of four crab species. Comp Biochem Physiol 89A:243–246

    Article  Google Scholar 

  • Jokumsen A, Weber RE (1982) Hemocyanin–oxygen affinity in hermit crab blood is temperature independent. J Exp Zool 221:389–394

    Article  Google Scholar 

  • Jones ML (1981) Riftia pachyptila Jones: observations on the Vestimentiferan worm from the Galápagos Rift. Science 213:333–336

    Article  PubMed  CAS  Google Scholar 

  • Jones ML (1988) The Vestimentifera, their biology, systematic and evolutionary patterns. Oceanol Acta Spec 8:69–82

    Google Scholar 

  • Jouin C, Toulmond A (1989) The ultrastructure of the gill of the lugworm Arenicola marina (L) (Annelida, Polychaeta). Acta Zool Stockh 70(2):121–129

    Article  Google Scholar 

  • Jouin C, Gaill F (1990) Gills of hydrothermal vent annelids : structure, ultrastructure and functionnal implications in two Alvinellid species. Prog Oceanogr 24:59–69

    Article  Google Scholar 

  • Jouin-Toulmond C, Augustin D, Desbruyeres D, Toulmond A (1996) The gas transfer system in Alvinellids (Annelida Polychaeta, Terebellida). Anatomy and ultrastructure of the anterior circulatory system and characterization of a coelomic, intracellular, haemoglobin. Cah Biol Mar 37(2):135–151

    Google Scholar 

  • Jouin-Toulmond C, Hourdez S (2006) Morphology, ultrastructure and functional anatomy of the branchial organ of Terebellides stroemii (Polychaeta: Trichobranchidae), with remarks on the systematic position of the genus Terebellides. Cah Biol Mar 47(3):287–299

    Google Scholar 

  • Kennicutt MC II, Brooks JM, Bidigare RR, Fay RR, Wade TL, McDonald TJ (1985) Vent-type taxa in a hydrocarbon seep region on the Louisiana slope. Nature 317:351–353

    Article  CAS  Google Scholar 

  • Kennish MJ, Lutz RA (1992) The hydrothermal vent clam, Calyptogena magnifica (Boss and Turner 1980): a review of existing literature. Rev Aquat Sci 6(1):29–66

    Google Scholar 

  • Kimura HM, Sato Y, Sasayama Y, Naganuma T (2003) Molecular characterization and in situ localization of endosymbiotic 16s ribosomal RNA and Rubisco genes in the pogonophoran tissue. Mar Biotech 5:261–269

    Article  CAS  Google Scholar 

  • Kobayashi M, Hoshi T (1982) Relationship between haemoglobin concentration of Daphnia magna and the ambient oxygen concentration. Comp Biochem Physiol 72:247–249

    Article  Google Scholar 

  • Kobayashi M, Hoshi T (1984) Analysis of the respiratory role of haemoglobin in Daphnia magna. Zool Sci 1:523–532

    CAS  Google Scholar 

  • Kraus DW, Doeller JE (2004) Sulfide consumption by mussel gill mitochondria is not strictly tied to oxygen reduction: measurements using a novel polarographic sulfide sensor. J Exp Biol 207:3667–3679

    Article  PubMed  CAS  Google Scholar 

  • Lallier FH, Truchot JP (1997) Hemocyanin oxygen-binding properties of a deep-sea hydrothermal vent shrimp: evidence for a novel cofactor. J Exp Zool 277:357–364

    Article  CAS  Google Scholar 

  • Lallier FH, Camus L, Chausson F, Truchot JP (1998) Structure and function of hydrothermal vent crustacean haemocyanin: an update. Cah Biol Mar 39(3–4):313–316

    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

    Article  CAS  Google Scholar 

  • Levin LA (2003) Oxygen minimum zone benthos: adaptation and community response to hypoxia. Oceanogr Mar Biol Annu Rev 41:1–45

    Google Scholar 

  • Magenheim AJ, Gieskes JM (1992) Hydrothermal discharge and alteration in near-surface sediments from the Guaymas Basin, Gulf of California. Geochim Cosmochim Acta 56:2329–2338

    Article  CAS  Google Scholar 

  • McMahon BR (2001) Respiratory and circulatory compensation to hypoxia in crustaceans. Respir Physiol 128:349–364

    Article  PubMed  CAS  Google Scholar 

  • Mickel TJ, Childress JJ (1982a) Effects of pressure and temperature on the EKG and heart rate of the hydrothermal vent crab Bythograea thermydron (Brachyura). Biol Bull 162:70–82

    Article  Google Scholar 

  • Mickel TJ, Childress JJ (1982b) Effects of temperature, pressure, and oxygen concentration on the oxygen consumption rate of the hydrothermal vent crab Bythograea thermydron (Brachyura). Phys Zool 55(2):199–207

    Google Scholar 

  • Morris S, Bridges CR (1985) An investigation of haemocyanin oxygen affinity in the semi-terrestrial crab Ocypode saratan Forsk. J Exp Biol 117:119–132

    CAS  Google Scholar 

  • Morris S, Bridges CR, Grieshaber MK (1985) Respiratory properties of the haemolymph of the intertidal prawn Palaemon elegans (Rathke). J Exp Biol 233:175–186

    CAS  Google Scholar 

  • Morris S, Greenaway P, McMahon BR (1988) Adaptations to terrestrial existence by the robber crab, Birgus latro. I. An in vitro investigation of blood gas transport. J Exp Biol 140:477–491

    Google Scholar 

  • Numoto N, Nakagawa T, Kita A, Sasayama Y, Fukumori Y, Miki K (2005) Structure of an extracellular giant hemoglobin of the gutless beard worm Oligobrachia mashikoi. Proc Natl Acad Sci USA 102(41):14521–14526

    Article  PubMed  CAS  Google Scholar 

  • O’Brien J, Vetter RD (1990) Production of thiosulphate during sulphide oxidation by mitochondria of the symbiont-containing bivalve Solemya reidi. J Exp Biol 149:133–148

    PubMed  CAS  Google Scholar 

  • Parrino V, Kraus DW, Doeller JE (2000) ATP production from the oxidation of sulfide in gill mitochondria of the ribbed mussel Geukensia demissa. J Exp Biol 203:2209–2218

    PubMed  CAS  Google Scholar 

  • Paull CK, Hecker B, Commeau R, Freeman-Lynde RP, Neumann C, Corso WP, Golubic S, Hook JE, Sikes E, Curray J (1984) Biological communities at the Florida escarpment resemble hydrothermal vent taxa. Science 226:965–967

    Article  CAS  PubMed  Google Scholar 

  • Powell MA, Somero GN (1986) Adaptations to sulfide by hydrothermal vent animals: sites and mechanisms of detoxification and metabolism. Biol Bull 171:274–290

    Article  CAS  Google Scholar 

  • Sanders NK (1989) Functional properties of hemocyanins from deep-sea crustaceans. PhD thesis. University of California, Santa Barbara USA. 209 pp

    Google Scholar 

  • Sanders NK, Arp AJ, Childress JJ (1988) Oxygen binding characteristics of the hemocyanins of two deep-sea hydrothermal vent crustaceans. Respir Physiol 71:57–68

    Article  PubMed  CAS  Google Scholar 

  • Segonzac M, Desaintlaurent M, Casanova B (1993) Enigma of the trophic adaptation of the shrimp Alvinocarididae in hydrothermal areas along the Mid-Atlantic Ridge. Cah Biol Mar 34(4):535–571

    Google Scholar 

  • Sell AF (2000) Life in the extreme environment at a hydrothermal vent: haemoglobin in a deep-sea copepod. Proc R Soc Lond B 267:2323–2326

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Smith EB, Scott KM, Nix ER, Korte C, Fisher CR (2000) Growth and condition of seep mussels (Bathymodiolus childressi) at a Gulf of Mexico Brine Pool. Ecology 81(9):2392–2403

    Google Scholar 

  • Terwilliger NB, Terwilliger RC (1984) Hemoglobin from the "Pompeii Worm", Alvinella pompejana, an annelid from a deep sea hot hydrothermal vent environment. Mar Biol Lett 5:191–201

    CAS  Google Scholar 

  • Terwilliger RC, Terwilliger NB, Arp AJ (1983) Thermal vent clam (Calyptogena magnifica) hemoglobin. Science 219:981–983

    Article  CAS  PubMed  Google Scholar 

  • Terwilliger RC, Terwilliger NB, Hughes GM, Southward AJ, Southward EC (1987) Studies on the haemoglobins of the small pogonophorans. J Mar Biol Ass U K 67:219–239

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Truchot J-P (1992) Respiratory function of arthropod hemocyanins. In: Mangum CP (ed) Blood and tissues oxygen carriers. Spinger Verlag, Berlin Heidelberg, pp 377–410

    Google Scholar 

  • Tunnicliffe V (1991) The biology of hydrothermal vents: ecology and evolution. Oceanogr Mar Biol Annu Rev 29:319–407

    Google Scholar 

  • Tyler PA, German CR, Ramirez-Llodra E, Van Dover CL (2003) Understanding the biogeography of chemosynthetic ecosystems. Oceanol Acta 25(5):227–241

    Article  Google Scholar 

  • Vetter RD, Wells ME, Kurtsman AL, Somero GN (1987) Sulfide detoxification by the hydrothermal vent crab Bythograea thermydron and other decapod crustaceans. Physiol Zool 60:121–137

    CAS  Google Scholar 

  • Völkel S, Grieshaber MK (1997) Sulphide oxidation and oxidative phosphorylation in the mitochondria of the lugworm Arenicola marina. J Exp Biol 200:83–92

    Google Scholar 

  • Von Damm KL (1990) Seafloor hydrothermal activity: black smoker chemistry and chimneys. Ann Rev Earth Planet Sci 18:173–204

    Article  Google Scholar 

  • Weber RE (1978) Respiratory pigments. In: Mills PJ (ed) Physiology of annelids. Academic Press, New York, pp 393–437

    Google Scholar 

  • Williams AB (1980) A new crab family from the vicinity of submarine thermal vents on the Galapagos Rift (Crustacea: Decapoda: Brachyura). Proc Biol Soc Wash 93(2):443–472

    Google Scholar 

  • Wittenberg JB (1985) Oxygen supply to intracellular bacterial symbionts. Bull Biol Soc Wash 6:301–310

    Google Scholar 

  • Wittenberg JB, Stein JL (1995) Hemoglobin in the symbiont-harboring gill of the marine gastropod Alviniconcha hessleri. Biol Bull 188:5–7

    Article  PubMed  CAS  Google Scholar 

  • Zal F, Lallier FH, Green BN, Vinogradov SN, Toulmond A (1996a) The multi-hemoglobin system of the hydrothermal vent tube worm Riftia pachyptila. 2. Complete polypeptide chain composition investigated by maximum entropy analysis of mass spectra. J Biol Chem 271(15):8875–8881

    Article  CAS  Google Scholar 

  • Zal F, Lallier FH, Wall JS, Vinogradov SN, Toulmond A (1996b) The multi-hemoglobin system of the hydrothermal vent tube worm Riftia pachyptila. 1. Reexamination of the number and masses of its constituents. J Biol Chem 271(15):8869–8874

    Article  PubMed  CAS  Google Scholar 

  • Zal F, Green BN, Lallier FH, Toulmond A (1997) Investigation by electrospray ionization mass spectrometry of the extracellular hemoglobin from the polychaete annelid Alvinella pompejana: An unusual hexagonal bilayer hemoglobin. Biochemistry 36(39):11777–11786

    Article  PubMed  CAS  Google Scholar 

  • Zal F (1998) Sulphide-binding processes of Riftia pachyptila haemoglobins. Cah Biol Mar 39(3–4):327–328

    Google Scholar 

  • Zal F, Leize E, Lallier FH, Toulmond A, VanDorsselaer A, Childress JJ (1998) S-Sulfohemoglobin and disulfide exchange: the mechanisms of sulfide binding by Riftia pachyptila hemoglobins. Proc Natl Acad Sci USA 95(15):8997–9002

    Article  PubMed  CAS  Google Scholar 

  • Zal F, Green BN, Martineu P, Lallier FH, Toulmond A, Vinogradov SN, Childress JJ (2000a) Polypeptide chain composition difersity of hexagonal-bilayer haemoglobins within a single family of annelids, the Alvinellidae. Eur J Biochem 267:1–11

    Article  Google Scholar 

  • Zal F, Leize E, Oros DR, Hourdez S, Van Dorsselaer A, Childress JJ (2000b) Haemoglobin structure and biochemical characteristics of the sulphide-binding component from the deep-sea clam Calyptogena magnifica. Cah Biol Mar 41(4):413–423

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stéphane Hourdez .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Hourdez, S., Lallier, F.H. (2006). Adaptations to hypoxia in hydrothermal-vent and cold-seep invertebrates. In: Amils, R., Ellis-Evans, C., Hinghofer-Szalkay, H. (eds) Life in Extreme Environments. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6285-8_19

Download citation

Publish with us

Policies and ethics