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Physiological adaptations to extreme pressures: the implications for palaeoecology

Published online by Cambridge University Press:  03 November 2011

A. G. Macdonald
Affiliation:
Department of Physiology, Marischal College,University of Aberdeen, Aberdeen AB9 IAS, Scotland, U.K.

Abstract

Present-day organisms have colonised two distinct high pressure environments: the deep sea and oil well and other crustal fluids. In the former, pressures attain 100 MPa and temperatures are generally less than 4°C. In the latter, the temperatures are high, up to 150°C, and occur in combination with pressures of up to 50 MPa. The high temperature is close to the limit of thermal stability of the macromolecules essential for life. The adaptation of present-day marine organisms to high pressure is known to involve modifications to their cell membrane lipids and subtle changes in both structural proteins and enzymes. There is no reason to suppose that they are close to the maximum pressure to which they could adapt and higher pressures could have been colonised in the geological past. The existence of “marker” compounds, characteristic of high pressure organisms, is discussed, and the possibility that isotope ratios are distorted by metabolic processes at high pressure is raised.

Type
Physiological adaptations in some recent and fossil organisms
Copyright
Copyright © Royal Society of Edinburgh 1989

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References

Avrova, N. F. 1984. The effect of natural adaptations of fishes to environmental temperature on brain ganglioside fatty acid and long chain base composition. COMP BIOCHEM PHYSIOL 78B, 903–9.Google Scholar
Bernhardt, G., Jaenicke, R., Ludemann, H.-D., Konig, H. & Stetter, K. O. 1988. High pressure enhances the growth rate of thermophilic archaebacterium Methanococcus thermolithicus without excluding its temperature range. ENVIRON MICROBIOL 54, 1258–61.CrossRefGoogle Scholar
Brandts, J. F. 1967. Heat effects on proteins and enzymes. In Rose, A. (ed) Thermobiology, 2572. New York: Academic Press.Google Scholar
Brandts, J. F., Oliveira, R. J. & Westort, C. 1970. Thermodynamics of protein denaturation. Effect of pressure on the denaturation of ribonuclease A. BIOCHEMISTRY 9, 1038–47.CrossRefGoogle ScholarPubMed
Brassell, S. C., Eglington, G., Marlowe, I. T., Pflaumann, U. & Sarnthein, M. 1986. Molecular stratigraphy: a new tool for climatic assessment. NATURE 320, 129133.CrossRefGoogle Scholar
Brenner, R. R. 1984. Effect of unsaturated acids on membrane structure and enzyme kinetics. PROG LIPID RES 23, 6996.CrossRefGoogle ScholarPubMed
Brock, T. D. 1985. Life at high temperatures. SCI 230, 132–38.CrossRefGoogle ScholarPubMed
Bubela, B. 1982. Combined effects of temperature and other environmental stresses in microbiologically enhanced oil recovery. In Donaldson, E. C. & Bennett, Clark J. (eds) Proceedings of the International Conference in Microbial Enhancement of Oil Recovery, 118–23. Bartlesville, Oklahoma: United States Department of Energy.Google Scholar
Bubela, B. 1985. Effect of biological activity on the movement of fluids through porous rocks and sediments and its application to enhanced oil recovery. GEOMICROBIOL J 4, 313–27.CrossRefGoogle Scholar
Chong, P. L.-G. & Cossins, A. R. 1984. Interacting effects of temperature pressure and cholesterol content upon the molecular order of dioleoylphosphatidylcholine vesicles. BIOCHIM BIOPHYS ACTA 772, 197201.CrossRefGoogle ScholarPubMed
Clayton, R. N., Goldsmith, J. R., Karel, K. J., Mayeda, T. K. & Newton, R. C. 1975. Limits on the effect of pressure on isotopic fractionation. GEOCHIM COSMOCHIM ACTA 39, 11971201.CrossRefGoogle Scholar
Comita, P. B. & Gagosian, R. B. 1983. Membrane lipid from deep-sea hydrothermal vent methanogen: a new macrocyclic glycerol diether. SCIENCE 222, 1329–31.CrossRefGoogle ScholarPubMed
Coolbear, K. P., Berde, C. B. & Keough, K. M. W. 1983. Gel to liquid-crystalline phase transitions of aqueous dispersions of polyunsaturated mixed-acid phosphatidylcholines. BIOCHEMISTRY 22, 1466–73.CrossRefGoogle ScholarPubMed
Cossins, A. R. 1983. The adaptation of membrane structure and function to changes in temperature. In Cossins, A. R. & Sheterline, P. (eds) Cellular Acclimatisation to Environmental Change, 332. Cambridge: Cambridge University Press.Google Scholar
Curtis, C. D. 1977. Sedimentary geochemistry: environments and processes dominated by involvement of an aqueous phase. PHILOS TRANS R SOC LONDON A286, 272353.Google Scholar
Davis, J.-S. 1981. The influence of pressure on the self-assembly of thick filaments from the myosin vertebrate skeletal muscle. BIOCHEM J 197, 301–8.CrossRefGoogle ScholarPubMed
Deckmann, M., Haimovitz, R. & Shinitzky, M. 1985. Selective release of integral proteins from human erythrocyte membranes by hydrostatic pressure. BIOCHIM BIOPHYS ACTA 821, 334–40.CrossRefGoogle ScholarPubMed
De Long, E. F. & Yayanos, A. A. 1986. Biochemical function and ecological significance of novel bacterial lipids in deep-sea prokanyotes. APPL ENVIRON MICROBIOL 51, 730–37.CrossRefGoogle Scholar
De Long, E. F. & Yayanos, A. A. 1987. Properties of the glucose transport system in some deep-sea bacteria. APPL ENVIRON MICROBIOL 53, 527–32.CrossRefGoogle Scholar
Deming, J. W., Hada, H., Colwell, R. R.Luehrsen, K. R. & Fox, G. E. 1984. The ribonucleotide sequence of 5S RNA from two strains of deep-sea barophilic bacteria. J GEN MICROBIOL 130, 1191–920.Google ScholarPubMed
Deming, J. W. & Baross, J. A. 1986. Solid medium for culturing black smoker bacteria at temperatures to 120°C. APPL ENVIRON MICROBIOL 51, 238–43.CrossRefGoogle Scholar
De Rosa, M., Gambacorta, A. & Gliozzi, A. 1986. Structure, biosynthesis and physicochemical properties of Archaebacteria lipids. MICROBIOL REV 50, 7080.CrossRefGoogle ScholarPubMed
Dostalek, M. & Kvet, R. 1964. Utilization of the osmotolerance of sulphate-reducing bacteria in study of the genesis of subterranean waters. FOLIA MICROBIOL 9, 103–14.CrossRefGoogle Scholar
Douglas, R. G. & Savin, S. M., quoted in Douglas, R. & Woodruff, F. 1981. In Emiliani, C. (ed) The Sea, Vol. 7, 12331327. New York: Wiley Interscience.Google Scholar
Emiliani, C. 1961. The temperature decrease of surface seawater in high latitudes and of abyssal-hadal water in oceanic basins during the past 75 million years. DEEP SEA RES 8, 144–47.Google Scholar
Engelborghs, Y.Heremans, K. A. H. & De Maeyer, L. C. M. 1976. Effects of temperature and pressure on polymerisation equilibrium of neuronal microtubules. NATURE 259, 686–89.CrossRefGoogle ScholarPubMed
Fayers, F. J., Hawes, R. I. & Mathews, J. D. 1980. Some aspects of the potential application of EOR processes in north sea reservoirs. In Proceedings of the European Offshore Petroleum Conference, 473–86. London: European Offshore Petroleum Conference.Google Scholar
Gavish, B., Gratton, E. & Hardy, C. J. 1983. Adiabatic compressibility of globular proteins PROC NATL ACAD SCI USA 80, 750–54.CrossRefGoogle ScholarPubMed
Gekko, K. & Koga, S. 1983. The effect of pressure on thermal stability and in vitro fibril formation of collagen. AGRIC BIOL CHEM 47, 1027–33.Google Scholar
Gliozzi, A., Paoli, G., De Rosa, M. & Gambacerta, A. 1983. Effect of isoprenoid cydization on the transition of lipids in thermophilic archaebacteria. BIOCHIM BIOPHYS ACTA 735, 234–42.CrossRefGoogle Scholar
Grassle, J. F. 1985. Hydrothermal vent animals: distribution and biology. SCIENCE 229, 713–17.CrossRefGoogle ScholarPubMed
Harper, A. A., Macdonald, A. G., Wardle, C. S. & Pennec, J.-P. 1987. The pressure tolerance of deep sea fish axons: Results of Challenger Cruise 6B/85. COMP BIOCHEM PHYSIOL 88A, 647–53.CrossRefGoogle Scholar
Herbert, B. N. & Stott, F. D. J. 1983. The effects of pressure and temperature on bacteria in oilfield water injection systems. In Tiller, A. K. (ed.) Microbiol Corrosion, 717. London: Metals Society.Google Scholar
Heremans, K. 1982. High pressure effects on proteins and other biomolecules. ANN REV BIOPHYS BIOENG 11, 121.CrossRefGoogle Scholar
Iqbal, M. & Verrall, R. E. 1988. Implications of protein folding. J BIOL CHEM 263, 4159–65.CrossRefGoogle ScholarPubMed
Jaenicke, R. 1983. Biochemical processes under high pressure. NATURWISSENSCHAFTEN 70, 332–41.CrossRefGoogle Scholar
Jaenicke, R., Ludemann, H.-D. & Schade, B. C. 1981. High pressure effects on the endothermic association of tobacco mosaic virus. BIOPHYS STRUCT MECH 7, 1952033.CrossRefGoogle Scholar
Jannasch, H. W. 1985. The chemosynthetic support of life and the microbiol diversity at deep-sea hydrothermal vents. PROC R SOC LONDON B225, 277–97.Google Scholar
Jannasch, H. W. & Taylor, C. D. 1984. Deep sea microbiology. ANN REV MICROBIOL 38, 487514.CrossRefGoogle ScholarPubMed
Jannasch, H. W. & Wirsen, C. O. 1984. Variability of pressure adaptation in deep sea bacteria. ARCH MICROBIOL 139, 281–88.CrossRefGoogle Scholar
Josephs, R. & Harrington, W. F. 1967. An unusual pressure dependence for a reversibly associating protein system: sedimentation studies on myosin. PROC NATL ACAD SCI USA 58, 1587–94.CrossRefGoogle ScholarPubMed
King, L. & Weber, G. 1986. Conformational drift in dissociated lactate dehydrogenases. BIOCHEMISTRY 25, 3632–37.CrossRefGoogle ScholarPubMed
Kitching, J. A. 1957. Effects of high hydrostatic pressures on Actinophrys sol (Heliozoa). J EXP BIOL 34, 511–17.CrossRefGoogle Scholar
Kornblatt, J., Kornblatt, J. & Hui, Bon Hoa G. 1982. The pressure-induced, reversible inactivation of mouse grain enolases. EUR J BIOCHEM 128, 577–81.CrossRefGoogle Scholar
Kundrot, C. E. & Richards, F. M. 1987. Changes in the high resolution structure of crystalline hen egg-white lysozyme produced by a hydrostatic pressure of 100 atmospheres. In Jannasch, H. W., Marquis, R. E. & Zimmerman, A. M. (eds) Current perspectives in High Pressure Biology, 245–55. London: Academic Press.Google Scholar
Laidler, K. J. & Bunting, P. S. 1973. The chemical kinetics of enzyme action. Oxford: Clarendon Press.Google Scholar
Langworthy, T. A. 1985. In Woese, C. R. & Wolfe, R. S. (eds) The Bacteria VIII Archaebacteria Lipids of Archaebacteria, 459–97. New York: Academic Press.Google Scholar
Lazar, I. 1982. Microbiol enhancement of oil recovery in Romania. In Donaldson, E. C. & Bennett, Clark J. (eds) Proceedings of the International Conference on Microbiol Enhancement of Oil Recovery, 140–48. Bartlesville, Oklahoma: United States Department of Energy.Google Scholar
Li, T. M., Hook, J. W., Drickamer, H. G. & Weber, G. 1976. Plurality of pressure-denatured forms in chymotrypsinogen and lysozyme. BIOCHEMISTRY 15, 5571–80.CrossRefGoogle ScholarPubMed
Macdonald, A. G. 1987. The role of membrane fluidity in complex processes under high pressure. In Jannasch, H. W., Marquis, R. E. & Zimmerman, A. M. (eds) Current perspectives in high pressure biology, 207–24. New York: Academic Press.Google Scholar
Macdonald, A. G. 1975. Physiological aspects of deep sea biology. Cambridge: Cambridge University Press.Google Scholar
Macdonald, A. G., Gilchrist, I. & Wardle, C. S. 1987. Effects of hydrostatic pressure on the motor activity of fish from shallow water and 900 m depths; some results of Challenger cruise 6B/85. COMP BIOCHEM PHYSIOL 88A, 543–47.CrossRefGoogle Scholar
Macdonald, A. G., Wahle, K. W. J., Cossins, A. R. & Behan, M. K. 1988. Temperature, pressure and cholesterol effects on bilayer fluidity; a comparison of pyrene excimer/monomer ratios with the steady-state fluorescence polarization of diphenylhexatriene in liposomes and microsomes. BIOCHIM BIOPHYS ACTA 938, 231–42.CrossRefGoogle ScholarPubMed
Macdonald, A. G. & Cossins, A. R. 1985. The theory of homeoviscous adaptation of membranes applied to deep sea animals SYMP SOC EXPTL BIOL 39, 301–22. Cambridge: Cambridge University Press.Google Scholar
Macdonald, A. G. & Gilchrist, I. 1982. The pressure tolerance of deep sea amphipods collected at their ambient high pressure. COMP BIOCHEM PHYSIOL 71A, 349–52.CrossRefGoogle Scholar
Marquis, R. E. 1983. Barotolerance and Microbial enhancement of oil recovery. In Zajic, J. E. et al. . (eds) Microbial enhanced oil recovery, 813. Oklahoma: Penn Well Books.Google Scholar
Marquis, R. E. 1984. Reversible actions of hydrostatic pressure and compressed gases on microorganisms. In Hurst, A. & Nasim, A. (eds) Repairable lesions in microorganisms, 273301. London: Academic Press.Google Scholar
Marsland, D. A. 1970. Pressure-temperature studies on the mechanism of cell division. In Zimmerman, A. M. (ed.) High pressure effects on cellular processes, 259312. New York: Academic Press.Google Scholar
Melchior, D. L. 1982. In Razin, S. & Roltem, S. (eds) Current topics: membranes and transport, lipid phase transitions and regulation of membrane fluidity in prokaryotes, 263316. New York: Academic Press.Google Scholar
Miller, S. L. & Bada, J. L. 1988. Submarine hot springs and the origins of life. NATURE 334, 609–11.CrossRefGoogle Scholar
Morild, E. 181. The theory of pressure effects of enzymes. ADV PROT CHEM 34, 93166.Google Scholar
Muller, K., Seifert, T. & Jaenicke, R. 1984. High pressure dissociation of lactate dehydrogenase from Bacillus stearothermophilus and reconstitution of the enzyme after denaturation in 6 M guanidine hydrochloride. EUR BIOPHYS J 11, 8794.CrossRefGoogle ScholarPubMed
O'Connor, T. M., Houston, L. L. & Sampson, F. 1974. Stability of neuronal microtubules to high pressure in vivo and in vitro. PROC NATL ACAD SCI, USA 71, 4198–202.CrossRefGoogle ScholarPubMed
Paladini, A. A. & Weber, G. 1981. Pressure-induced reversible dissociation of enolase. BIOCHEMISTRY 20, 2587–93.CrossRefGoogle ScholarPubMed
Pande, C. & Wishnia, A. 1986. Pressure dependence of equilibria and kinetics of Escherischia coli ribosomal sub-unit association. J BIOCHEM 261, 6272–78.Google Scholar
Pennec, J.-P., Wardle, C. S., Harper, A. A. & Macdonald, A. G. 1988. Effects of high hydrostatic pressure on the isolated hearts of shallow water and deep sea fish; results of Challenger cruise 6B/85. COMP BIOCHEM PHYSIOL 89A, 215–18.CrossRefGoogle Scholar
Rozanova, E. P. & Nazina, T. N. 1979. Occurrence of thermophilic sulfate-reducing bacteria in oil-bearing strata of Apsheron and Western Siberia. MIKROBIOLOGIYA 48, 907–11.Google Scholar
Schade, B. C., Ludemann, H.-D., Rudolph, R. & Jaenicke, R. 1980. Kinetics of reconstitution of porcine muscle lactic dehydrogenase after reversible high pressure dissociation. BIOPHYS CHEM 11, 257263.CrossRefGoogle ScholarPubMed
Schulz, E., Lundemann, H.-D. & Jaenicke, R. 1976. High pressure equilibrium studies on the dissociation-association of E. coli ribosomes. FEBS LETT 64, 4043.CrossRefGoogle ScholarPubMed
Siebenaller, J. F. 1984. Structural comparison of lactate dehydrogenase homologs differing in sensitivity to hydrostatic pressure. BIOCHIM BIOPHYS ACTA 786, 161–69.CrossRefGoogle ScholarPubMed
Siebenaller, J. F. 1987. Pressure adaptation in deep sea animals. In Hannasch, H. W., Marquis, R. E. & Zimmerman, A. M. (eds) Current perspectives in high pressure biology, 245–55. London: Academic Press.Google Scholar
Siebenaller, J. F. & Somero, G. N. 1979. Pressure-adaptive differences in the binding and catalytic properties of muscle-type (M4) lactate dehydrogenases of shallow and deep-living marine fishes. J COMP PHYSIOL B129, 295300.CrossRefGoogle Scholar
Small, D. M. 1986. The physical chemistry of lipids from alkanes to phospholipids. New York: Plenum.CrossRefGoogle Scholar
Somero, G. N. 1983. Environmental adaptation of proteins: strategies for conservation of critical functional and structural traits. COMP BIOCHEM PHYSIOL 76A, 621–33.CrossRefGoogle Scholar
Somero, G. N., Siebenaller, J. F. & Hockachka, P. W. 1983. Biochemical and physiological adaptations of deep sea animals. In Rowe, G. T. (ed.) The Sea, Vol 8. Deep Sea Biology, 261330. New York: Wiley-Interscience.Google Scholar
Somero, G. N. & Low, P. S. 1977. Enzyme hydration may explain catalytic efficiency differences among lactate dehydrogenase homologues. NATURE 266, 276–78.CrossRefGoogle ScholarPubMed
Springham, D. G., McKay, A., Moses, V., Robinson, J. P., Brown, M. J., Foster, M., Hume, J., May, C. W., McRoberts, T. S. & Weston, A. 1982. Some constraints on the use of bacteria in enhanced oil recovery. In Donaldson, E. C. & Bennett, Clark J. (eds) Proceedings of the International Conference on Microbiol Enhancement of Oil Recovery, 158–61. Bartlesville, Oklahoma: United States Department of Energy.Google Scholar
Suzuki, K. & Taniguchi, Y. 1972. Effect of pressure on biopolymer and model systems. In Sleigh, M. A. & Macdonald, A. G. (eds) Effects of pressure on organisms 103–24. SYMP SOC EXP BIOL 26, Cambridge: Cambridge University Press.Google Scholar
Swezey, R. R. & Somero, G. N. 1982. Polymerization thermodynamics and structural stabilities of skeletal muscle actins from vertebrates adapted to different temperatures and hydrostatic pressures. BIOCHEMISTRY 21, 4496–503.CrossRefGoogle Scholar
Thompson, R. B. & Lakowicz, J. R. 1984. Effect of pressure on the self-association of melittin. BIOCHEMISTRY 23, 3411–17.CrossRefGoogle ScholarPubMed
Trent, J. D., Chastain, R. A., Yayanos, A. A. 1984. Possible artefactual basis for apparent bacterial growth at 250°C. NATURE 307, 737740.CrossRefGoogle Scholar
Wardle, C. S., Tetteh-Lartey, N., Macdonald, A. G., Harper, A. A. & Pennec, J.-P. 1987. The effect of pressure on the lateral swimming muscle of the European eel Anguilla anguilla and the deep sea eel Histobranchus bathybius; results of Challenger cruise 6B/85. COMP BIOCHEM PHYSIOL 88A, 595–98.CrossRefGoogle Scholar
Weber, G. & Drickamer, H. G. 1983. The effect of high pressure upon proteins and other biomolecules. Q REV BIOPHYS 16, 89112.CrossRefGoogle ScholarPubMed
Wirsen, C. O., Jannasch, H. W., Wakeham, S. G. & Canuel, E. A. 1987. Membrane lipids of a psychrophilic and barophilic deep-sea bacterium. CURRENT MICROBIOL 14, 319–22.CrossRefGoogle Scholar
Woese, C. R. 1982. Archaebacteria and cellular origins: an overview. ZBL BAKT HYG 1 ABT ORIG C3, 117.Google Scholar
Yayanos, A. A. 1986. Evolutional and ecological implications of the properties of deep-sea barophilic bacteria. PROC NATL ACAD SCI USA 83, 9542–46.CrossRefGoogle Scholar
Yayanos, A. A. & De Long, E. F. 1987. Deep sea bacterial fitness to environmental temperatures and pressures. In Jannasch, H. W., Marquis, R. E. & Zimmerman, A. M. (eds) Current perspectives in high pressure biology, 1732. London: Academic Press.Google Scholar
Yayanos, A. A. & Dietz, A. S. 1983. Death of a hadal deep-sea bacterium after decompression. SCIENCE 220, 497–98.CrossRefGoogle Scholar
Zhaochen, Z. & Tongiuo, Q. 1982. A survey of research on the application of microbial techniques to the petroleum production in China. In Donaldson, E. C. & Bennett, Clark J. (eds) Proceedings of the International Conference on Microbiol Enhancement of Oil Recovery, 135–39. Bartlesville, Oklahoma: United States Department of Energy.Google Scholar
Zipp, A. & Kauzmnn, W. 1973. Pressure denaturation of metmyoglobin. BIOCHEMISTRY 12, 4217–28.CrossRefGoogle Scholar
Zobell, C. E. 1958. Ecology of sulfate reducing bacteria. PRODUCERS MONTHLY MAY, 1229.Google Scholar