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Annual Review of Marine Science

Volume 14, 2022

The Goldilocks Principle: A Unifying Perspective on Biochemical Adaptation to Abiotic Stressors in the Sea

Abstract

The ability of marine organisms to thrive over wide ranges of environmental stressors that perturb structures of proteins, nucleic acids, and lipids illustrates the effectiveness of adaptation at the biochemical level. A critical role of these adaptations is to achieve a proper balance between structural rigidity, which is necessary for maintaining three-dimensional conformation, and flexibility, which is required to allow changes in conformation during function. The Goldilocks principle refers to this balancing act, wherein structural stability and functional properties are poised at values that are just right for the environment the organism faces. Achieving this balance involves changes in macromolecular sequence and adaptive change in the composition of the aqueous or lipid milieu in which macromolecules function. This article traces the development of the field of biochemical adaptation throughout my career and shows how comparative studies of marine animals from diverse habitats have shed light on fundamental properties of life common to all organisms.

Keyword(s): adaptation, autobiography, corresponding states, Goldilocks principle, marginal stability, molecular evolution, protein stability
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/content/journals/10.1146/annurev-marine-022521-102228
2022-01-03
2024-05-12
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Literature Cited

  1. Beers JM, Jayasundara N. 2015. Antarctic notothenioid fish: What are the future consequences of ‘losses’ and ‘gains’ acquired during long-term evolution at cold and stable temperatures?. J. Exp. Biol. 218:1834–45
     [Google Scholar]
  2. Bowlus RD, Somero GN. 1979. Solute compatibility with enzyme function and structure: rationales for the selection of osmotic agents and end-products of anaerobic metabolism in marine invertebrates. J. Exp. Zool. 208:137–52
     [Google Scholar]
  3. Braby CE, Somero GN. 2006. Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). J. Exp. Biol 209:2554–66
     [Google Scholar]
  4. Buckley BA, Gracey AY, Somero GN. 2006. The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis. J. Exp. Biol. 209:2660–77
     [Google Scholar]
  5. Buckley BA, Somero GN. 2009. cDNA microarray analysis reveals the capacity of the cold-adapted Antarctic fish Trematomus bernacchii to alter gene expression in response to heat stress. Polar Biol 32:403–15
     [Google Scholar]
  6. Čapek M. 1961. The Philosophical Impact of Contemporary Physics Princeton, NJ: Van Nostrand
  7. Castellini MA, Somero GN. 1981. Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. J. Comp. Physiol. 143:191–98
     [Google Scholar]
  8. Childress JJ, Felbeck H, Somero GN. 1987. Symbiosis in the deep sea. Scientific American May 114–20
     [Google Scholar]
  9. Childress JJ, Somero GN. 1979. Depth-related enzymic activities in muscle, heart and brain of deep-living pelagic marine teleosts. Mar. Biol. 52:273–82
     [Google Scholar]
  10. Connor KM, Gracey AY 2011. Circadian cycles are the dominant transcriptional rhythm in the intertidal mussel Mytilus californianus. PNAS 108:16110–15
     [Google Scholar]
  11. Cossins AR, Friedlander MJ, Prosser CL. 1977. Correlations between behavioural temperature adaptations by goldfish and the viscosity and fatty acid composition of their synaptic membranes. J. Comp. Physiol. 120:109–21
     [Google Scholar]
  12. Dahlhoff EP, Schneidemann S, Somero GN. 1990. Pressure-temperature interactions on M4-lactate dehydrogenases from hydrothermal vent fishes: evidence for adaptation to elevated temperatures by the zoarcid Thermarces andersoni, but not the bythitid, Bythites hollisi. Biol. Bull. 179:134–39
     [Google Scholar]
  13. Dahlhoff EP, Somero GN. 1993. Temperature effects on mitochondria from abalones (genus Haliotis): adaptive plasticity and its limits. J. Exp. Biol. 185:151–68
     [Google Scholar]
  14. Dayton PK, Sala E. 2001. Natural history: the sense of wonder, creativity and progress in ecology. Sci. Mar. 65:199–206
     [Google Scholar]
  15. Dickson KA, Somero GN. 1987. Partial characterization of the buffering components of the red and white myotomal muscle of marine teleosts, with special emphasis on scombrid fishes. Physiol. Zool. 60:699–706
     [Google Scholar]
  16. Dietz TJ, Somero GN 1992. Heat shock protein 90 (HSP90) threshold induction temperature is subject to acclimatization in eurythermal goby fishes (genus Gillichthys). PNAS 89:3389–93
     [Google Scholar]
  17. Dong Y, Li X, Choi FMP, Williams GA, Somero GN, Helmuth B. 2017. Untangling the roles of microclimate, behaviour and physiological polymorphism in governing vulnerability of intertidal snails to heat stress. Proc. R. Soc. B 284:20162367
     [Google Scholar]
  18. Dong Y, Liao M, Meng X, Somero GN 2018. Structural flexibility and protein adaptation to temperature: molecular dynamics analysis of malate dehydrogenases of marine molluscs. PNAS 115:1274–79
     [Google Scholar]
  19. Dong Y, Miller LP, Sanders JG, Somero GN. 2008. Heat-shock protein 70 (Hsp70) expression in four limpets of the genus Lottia: interspecific variation in constitutive and inducible synthesis correlations with in situ exposure to heat stress. Biol. Bull. 215:173–81
     [Google Scholar]
  20. Dong Y, Somero GN. 2009. Temperature adaptation of cytosolic malate dehydrogenases of limpets (genus Lottia): differences in stability and function due to minor changes in sequence correlate with biogeographic and vertical distributions. J. Exp. Biol. 212:169–77
     [Google Scholar]
  21. Evans T, Somero GN. 2008. A microarray-based transcriptomic time-course of hyper- and hypoosmotic signaling events in the euryhaline fish Gillichthys mirabilis: osmosensors to effectors. J. Exp. Biol. 211:3636–49
     [Google Scholar]
  22. Fields PA, Dong Y, Meng X, Somero GN. 2015. Adaptations of protein structure and function to temperature: There is more than one way to “skin the cat. J. Exp. Biol. 218:1801–11
     [Google Scholar]
  23. Fields PA, Rudomen E, Somero GN. 2006. Temperature sensitivities of cytosolic malate dehydrogenases from native and invasive species of marine mussels (genus Mytilus): sequence-function linkages and correlations with biogeographic distribution. J. Exp. Biol. 209:656–77
     [Google Scholar]
  24. Fields PA, Somero GN 1998. Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes. PNAS 95:11476–81
     [Google Scholar]
  25. Gibbs A, Somero GN. 1989. Pressure adaptation of Na+/K+-ATPase in gills of marine teleosts. J. Exp. Biol. 143:475–92
     [Google Scholar]
  26. Gibbs A, Somero GN. 1990. Pressure adaptation of teleost gill Na+/K+-adenosine triphosphatase: role of lipid and protein moieties. J. Comp. Physiol. B 160:431–39
     [Google Scholar]
  27. Gracey AY, Chaney M, Boomhower J, Tyburczy W, Connor K, Somero GN 2008. Rhythms of gene expression in a fluctuating intertidal environment. Curr. Biol. 18:1501–7
     [Google Scholar]
  28. Gracey AY, Troll J, Somero GN. 2001. Hypoxia-induced gene expression profiling in the euryoxic fish G. mirabilis. PNAS 98:1993–98
     [Google Scholar]
  29. Graves JE, Somero GN. 1982. Electrophoretic and functional enzymic evolution in four species of eastern Pacific barracudas from different thermal environments. Evolution 36:97–106
     [Google Scholar]
  30. Griffin DR 1998.. Donald R. Griffin The History of Neuroscience in Autobiography, Vol. 2 LR Squire 68–93 San Diego, CA: Academic
  31. Hand SC, Somero GN. 1982. Urea and methylamine effects on rabbit muscle phosphofructokinase: catalytic stability and aggregation state as a function of pH and temperature. J. Biol. Chem. 257:734–41
     [Google Scholar]
  32. Hand SC, Somero GN. 1983. Phosphofructokinase of the hibernator Citellus beecheyi: temperature and pH regulation of activity via influences on the tetramer-dimer equilibrium. Physiol. Zool. 56:380–88
     [Google Scholar]
  33. Hazel JR. 1995. Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation?. Annu. Rev. Physiol. 57:19–42
     [Google Scholar]
  34. Hochachka PW, Somero GN. 1973. Strategies of Biochemical Adaptation Philadelphia: Saunders:
  35. Hochachka PW, Somero GN. 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution Oxford, UK: Oxford Univ. Press
  36. Hofmann GE, Buckley BA, Airaksinen S, Keen JE, Somero GN. 2000. Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii (family Nototheniidae). J. Exp. Biol. 203:2331–39
     [Google Scholar]
  37. Hofmann GE, Somero GN. 1996. Interspecific variation in thermal denaturation of proteins in the congeneric mussels Mytilustrossulus and M. galloprovincialis: evidence from the heat shock response and protein and protein ubiquitination. Mar. Biol. 126:65–75
     [Google Scholar]
  38. Holland LZ, McFall-Ngai M, Somero GN. 1997. Evolution of lactate dehydrogenase-A homologs of barracuda fishes (genus Sphyraena) from different thermal environments: Differences in kinetic properties and thermal stability are due to amino acid substitutions outside the active site. Biochemistry 36:3207–15
     [Google Scholar]
  39. Jayasundara J, Healy TM, Somero GN. 2013. Effects of temperature acclimation on cardiorespiratory performance of the Antarctic notothenioid Trematomus bernacchii. Polar Biol 36:1047–57
     [Google Scholar]
  40. Kültz D. 2005. Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67:225–57
     [Google Scholar]
  41. Kültz D. 2020. Evolution of cellular stress response mechanisms. J. Exp. Zool. A 333:359–78
     [Google Scholar]
  42. Liao M, Dong Y, Somero GN 2021. Thermal adaptation of mRNA secondary structure: stability versus lability. PNAS In press
    [Google Scholar]
  43. Liao M, Somero GN, Dong Y 2019. Comparing mutagenesis and simulations as tools for identifying functionally important sequence changes for protein thermal adaptation. PNAS 116:679–88
     [Google Scholar]
  44. Liao M, Zhang S, Zhang G, Chu Y, Somero GN, Dong Y. 2017. Heat-resistant cytosolic malate dehydrogenases of thermophilic intertidal snails (genus Echinolittorina): protein underpinnings of tolerance of body temperatures reaching 55°C. J. Exp. Biol. 220:2066–75
     [Google Scholar]
  45. Lockwood BL, Connor KM, Gracey AY. 2015. The environmentally tuned transcriptomes of Mytilus mussels. J. Exp. Biol. 218:1822–33
     [Google Scholar]
  46. Lockwood BL, Somero GN. 2012. Functional determinants of temperature adaptation in enzymes of cold- versus warm-adapted mussels (genus Mytilus). Mol. Biol. Evol. 29:3061–70
     [Google Scholar]
  47. Logan CA, Somero GN. 2010. Transcriptional responses to thermal acclimation in the eurythermal fish Gillichthys mirabilis (Cooper 1864). Am. J. Physiol. Integr. Comp. Physiol. 299:R843–52
     [Google Scholar]
  48. Logan CA, Somero GN. 2011. Effects of thermal acclimation on transcriptional responses to acute heat stress in the eurythermal fish Gillichthys mirabilis (Cooper). Am. J. Physiol. Regul. Integr. Comp. Physiol. 300:R1373–83
     [Google Scholar]
  49. Logue JA, DeVries AL, Fodor E, Cossins AR. 2000. Lipid compositional correlates of temperature-adaptive interspecific differences in membrane physical structure. J. Exp. Biol. 203:2105–15
     [Google Scholar]
  50. Low PS, Bada JL, Somero GN 1973. Temperature adaptation of enzymes: roles of the free energy, the enthalpy, and the entropy of activation. PNAS 70:430–32
     [Google Scholar]
  51. Low PS, Somero GN. 1974. Temperature adaptation of enzymes: a proposed molecular basis for the different catalytic efficiencies of enzymes from ectotherms and endotherms. Comp. Biochem. Physiol. B 49:307–12
     [Google Scholar]
  52. Low PS, Somero GN 1975a. Activation volumes in enzymic catalysis: their sources and modification by low-molecular-weight solutes. PNAS 72:3014–18
     [Google Scholar]
  53. Low PS, Somero GN 1975b. Protein hydration changes during catalysis: a new mechanism of enzymic rate enhancement and ion activation/inhibition of catalysis. PNAS 72:3305–9
     [Google Scholar]
  54. Macdonald JA, Montgomery JC, Wells RMG. 1988. The physiology of McMurdo Sound fishes: current New Zealand research. Comp. Biochem. Physiol. B 90:567–78
     [Google Scholar]
  55. Moyen NE, Somero GN, Denny MW. 2019. Impact of heating rate on cardiac thermal tolerance in the California mussel, Mytilus californianus. J. Exp. Biol. 222:jeb203166
     [Google Scholar]
  56. Moyen NE, Somero GN, Denny MW. 2020. Mussels’ acclimatization to high, variable temperatures is lost slowly upon transfer to benign conditions. J. Exp. Biol. 223:jeb222893
     [Google Scholar]
  57. Peck LS, Webb KE, Bailey DM. 2004. Extreme sensitivity of biological function to temperature in Antarctic marine species. Funct. Ecol. 18:625–30
     [Google Scholar]
  58. Podrabsky JE, Somero GN. 2004. Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. J. Exp. Biol. 207:2237–54
     [Google Scholar]
  59. Podrabsky JE, Somero GN 2006. Inducible heat tolerance in Antarctic notothenioid fishes. Polar Biol 30:39–43
     [Google Scholar]
  60. Ream RR, Theriot J, Somero GN. 2003. Influences of thermal acclimation and acute temperature change on the motility of epithelial wound healing cells (keratocytes) of tropical, temperate, and Antarctic fish. J. Exp. Biol. 206:4539–51
     [Google Scholar]
  61. Reeves RB. 1977. The interaction of body temperature and acid-base balance in ectothermic vertebrates. Annu. Rev. Physiol. 39:559–86
     [Google Scholar]
  62. Roberts D, Hofmann GE, Somero GN. 1997. Heat shock protein expression in Mytilus californianus: acclimatization (seasonal and tidal-height comparisons) and acclimation effects. Biol. Bull. 192:309–20
     [Google Scholar]
  63. Roberts SJ, Lowery MS, Somero GN. 1988. Regulation of binding of phosphofructokinase to myofibrils in the red and white muscle of the barred sand bass, Paralabrax nebulifer (Serranidae). J. Exp. Biol. 137:13–27
     [Google Scholar]
  64. Siebenaller JF, Somero GN. 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. 129:295–300
     [Google Scholar]
  65. Siebenaller JF, Somero GN. 1989. Biochemical adaptation to the deep sea. Crit. Rev. Aquat. Sci. 1:1–25
     [Google Scholar]
  66. Somero GN. 2000. Unity in diversity: a perspective on the methods, contributions, and future of comparative physiology. Annu. Rev. Physiol. 62:927–37
     [Google Scholar]
  67. Somero GN. 2020. The cellular stress response and temperature: function, regulation, and evolution. J. Exp. Zool. A 333:379–97
     [Google Scholar]
  68. Somero GN, Childress JJ. 1980. A violation of the metabolism-size scaling paradigm: activities of glycolytic enzymes in muscle increase in larger-size fish. Physiol. Zool. 53:322–37
     [Google Scholar]
  69. Somero GN, DeVries AL. 1967. Temperature tolerance of some Antarctic fishes. Science 156:257–58
     [Google Scholar]
  70. Somero GN, Giese AC, Wohlschlag DE. 1968. Cold adaptation of the Antarctic fish Trematomus bernacchii. Comp. Biochem. Physiol. 26:223–33
     [Google Scholar]
  71. Somero GN, Hochachka PW. 1968. The effect of temperature on catalytic and regulatory functions of pyruvate kinases of the rainbow trout and the Antarctic fish Trematomus bernacchii. Biochem. J. 110:395–400
     [Google Scholar]
  72. Somero GN, Lockwood BL, Tomanek L. 2017. Biochemical Adaptation: Response to Environmental Challenges from Life's Origins to the Anthropocene Sunderland, MA: Sinauer
  73. Stillman JH, Somero GN. 1996. Adaptation to temperature stress and aerial exposure in congeneric species of intertidal porcelain crabs (genus Petrolisthes): correlation of physiology, biochemistry and morphology with vertical distribution. J. Exp. Biol. 199:1845–55
     [Google Scholar]
  74. Stillman JH, Somero GN. 2000. A comparative analysis of thermal tolerance limits in porcelain crabs, genus Petrolisthes. Physiol. Biochem. Zool 73:200–8
     [Google Scholar]
  75. Sullivan KM, Somero GN. 1980. Enzyme activities of fish skeletal muscle and brain as influenced by depth of occurrence and habits of feeding and locomotion. Mar. Biol. 60:91–99
     [Google Scholar]
  76. Sullivan KM, Somero GN. 1983. Size- and diet-related variations in enzymic activity and tissue composition in the sablefish, Anoplopoma fimbria. Biol. Bull. 164:315–26
     [Google Scholar]
  77. Swezey RR, Somero GN. 1982. Polymerization thermodynamics and structural stabilities of skeletal muscle actins from vertebrates adapted to different temperatures and hydrostatic pressures. Biochemistry 21:4496–502
     [Google Scholar]
  78. Swezey RR, Somero GN. 1985. Pressure effects on actin self-assembly: interspecific differences in the equilibrium and kinetics of the G to F transformation. Biochemistry 24:852–60
     [Google Scholar]
  79. Tepolt C, Somero GN 2014. Master of all trades: thermal acclimation and adaptation of cardiac function in a broadly-distributed marine invasive species, the European green crab, Carcinus maenas. J. Exp. Biol. 217:1129–38
     [Google Scholar]
  80. Tomanek L, Somero GN. 1999. Evolutionary and acclimation-induced variation in the heat shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography. J. Exp. Biol. 202:2925–36
     [Google Scholar]
  81. Tomanek L, Somero GN. 2000. Time course of synthesis of heat-shock proteins in congeneric marine snails (genus Tegula) from different thermal habitats: relationships to severity of thermal stress and tidal period. Physiol. Biochem. Zool. 73:249–56
     [Google Scholar]
  82. Torres JJ, Somero GN. 1988. Vertical distribution and metabolism in Antarctic mesopelagic fishes. Comp. Biochem. Physiol. B 90:521–28
     [Google Scholar]
  83. Torson AS, Dong Y, Sinclair BJ. 2020. Help, there are ‘omics’ in my comparative physiology!. J. Exp. Biol. 223:jeb191262
     [Google Scholar]
  84. Weinstein RB, Somero GN. 1998. Effects of temperature on mitochondrial function in the Antarctic fish Trematomus bernacchii. J. Comp. Physiol. B 168:190–96
     [Google Scholar]
  85. Williams EE, Somero GN. 1996. Seasonal-, tidal cycle-, and microhabitat-related variation in membrane order of phospholipid vesicles from gills of the intertidal mussel Mytilus californianus. J. Exp. Biol. 199:1587–96
     [Google Scholar]
  86. Wohlschlag DE. 1964. Respiratory metabolism and ecological characteristics of some fishes in McMurdo Sound, Antarctica. Biology of the Antarctic Seas, Vol. 1 MO Lee 33–62 Washington DC: Am. Geophys. Union
     [Google Scholar]
  87. Yancey PH. 2005. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208:2819–30
     [Google Scholar]
  88. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN. 1982. Living with water stress: the evolution of osmolyte systems. Science 217:1214–22
     [Google Scholar]
  89. Yancey PH, Gerringer ME, Drazen JC, Rowden AA, Jamieson A 2014. Marine fish may be biochemically constrained from inhabiting deepest ocean depths. PNAS 111:4461–65
     [Google Scholar]
  90. Yancey PH, Rhea MD, Kemp KM, Bailey DM. 2004. Trimethylamine oxide, betaine and other osmolytes in deep-sea animals: depth trends and effects on enzymes under hydrostatic pressure. Cell. Mol. Biol. 50:371–76
     [Google Scholar]
  91. Yancey PH, Siebenaller JF. 2015. Co-evolution of proteins and solutions: protein adaptation versus cytoprotective micromolecules and their roles in marine organisms. J. Exp. Biol. 218:1880–96
     [Google Scholar]
  92. Yancey PH, Somero GN. 1978. Temperature dependence of intracellular pH: its role in the conservation of pyruvate apparent Km values of vertebrate lactate dehydrogenases. J. Comp. Physiol. 125:129–34
     [Google Scholar]
  93. Yancey PH, Somero GN. 1979. Counteraction of urea destabilization of protein structure by methylamine osmoregulatory solutes of elasmobranchs. Biochem. J. 183:317–23
     [Google Scholar]
  94. Yang T, Lai NC, Graham JB, Somero GN. 1992. Respiratory, blood, and heart enzymatic adaptations of Sebastolobus alascanus (Scorpaenidae; Teleostei) to the oxygen minimum zone: a comparative study. Biol. Bull. 183:490–99
     [Google Scholar]
  95. Yao C, Somero GN. 2012. The impact of acute temperature stress on hemocytes of invasive and native mussels (Mytilus galloprovincialis and M. californianus): DNA damage, membrane integrity and signaling pathways. J. Exp. Biol. 215:4267–77
     [Google Scholar]
/content/journals/10.1146/annurev-marine-022521-102228
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The Goldilocks Principle: A Unifying Perspective on Biochemical Adaptation to Abiotic Stressors in the Sea
Annual Review of Marine Science 14, 1 (2022); https://doi.org/10.1146/annurev-marine-022521-102228
/content/journals/10.1146/annurev-marine-022521-102228
/content/journals/10.1146/annurev-marine-022521-102228
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