Long-term cold acclimation extends survival time at 0°C and modifies the metabolomic profiles of the larvae of the fruit fly drosophila melanogaster

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Koštál, Vladimír ^a   Korbelová, Jaroslava ^a   Rozsypal, Jan ^b   Zahradníčková, Helena ^a   Cimlová, Jana ^a   Tomčala, Aleš ^a   Šimek, Petr ^a  

^a INSTITUTE OF ENTOMOLOGY   (Czech Republic)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCEROPHOSPHOETHANOLAMINE; GLYCEROPHOSPHOLIPID; GLYCEROPHOSPHORYLCHOLINE; PROLINE; TREHALOSE; AMINO ACID; FATTY ACID; POLYMER; POLYOL;

ANIMAL TISSUE; ARTHROPOD LARVA; ARTICLE; COLD ACCLIMATIZATION; COLD INJURY; COLD SHOCK RESPONSE; COLD TOLERANCE; DROSOPHILA MELANOGASTER; EMBRYO; LIPID COMPOSITION; MEMBRANE STRUCTURE; METABOLOMICS; NONHUMAN; PLASTICITY; SURVIVAL TIME; ACCLIMATIZATION; ANIMAL; CARBOHYDRATE METABOLISM; COLD; FEMALE; FREEZING; LARVA; METABOLISM; METABOLOME; PHYSIOLOGY; SURVIVAL; TIME;

DROSOPHILA MELANOGASTER; HEXAPODA;

ACCLIMATIZATION; AMINO ACIDS; ANIMALS; CARBOHYDRATE METABOLISM; COLD TEMPERATURE; DROSOPHILA MELANOGASTER; FATTY ACIDS; FEMALE; FREEZING; LARVA; METABOLOME; POLYMERS; SURVIVAL ANALYSIS; TIME FACTORS;

EID: 84856447886     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025025     Document Type: Article

References (94)

1. Throckmorton LH, (1975) The phylogeny, ecology, and geography of Drosophila. In: King RC, editors. Handbook of Genetics: Invertebrates of Genetic Interest New York Plenum pp. 421-469.
2. Strachan LA, Tarnowski-Garner HE, Marshall KE, Sinclair BJ, (2011) The evolution of cold tolerance in Drosophila larvae. Physiol Biochem Zool 84: 43-53.
3. Bale JS, (1993) Classes of insect cold hardiness. Funct Ecol 7: 751-753.
4. Loeb J, Northrop JH, (1917) On the influence of food and temperature upon the duration of life. J Biol Chem 32: 103-121.
5. Bliss CI, (1927) Temperature characteristics for prepupal development in Drosophila melanogaster. J Gen Physiol 9: 467-495.
6. Czajka MC, Lee RE Jr, (1990) A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. J Exp Biol 148: 245-254.
7. Hoffmann AA, Watson M, (1993) Geographical variation in the acclimation responses of Drosophila to temperature extremes. Amer Natur 142: S93-S113.
8. Kellermann V, van Heerwaarden B, Sgro CM, Hoffmann AA, (2009) Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 325: 1244-1246.
9. Moon I, Fujikawa S, Shimada K, (1996) Cryopreservation of Chymomyza larvae (Diptera: Drosophilidae) at -196°C with extracellular freezing. CryoLett 17: 105-110.
10. Koštál V, Zahradníčková H, Šimek P, (2011) Hyperprolinemic larvae of the drosophilid fly, Chymomyza costata, survive cryopreservation in liquid nitrogen. Proc Nat Acad Sci USA 108: 13041-13046.
11. Sinclair BJ, Roberts SR, (2005) Acclimation, shock and hardening in the cold. J Thermal Biol 30: 557-562.
12. Rako L, Hoffmann AA, (2006) Complexity of the cold acclimation response in Drosophila melanogaster. J Insect Physiol 52: 94-104.
13. Jensen D, Overgaard J, Sørensen JG, (2007) The influence of developmental stage on cold shock resistance and ability to cold-harden in Drosophila melanogaster. J Insect Physiol 53: 179-186.
14. Chen C-P, Walker VK, (1994) Cold-shock and chilling tolerance in Drosophila. J Insect Physiol 40: 661-669.
15. Rajamohan A, Sinclair BJ, (2008) Short-term hardening effects on survival of acute and chronic cold exposure by Drosophila melanogaster larvae. J Insect Physiol 54: 708-718.
16. Rajamohan A, Sinclair BJ, (2009) Hardening trumps acclimation in improving cold tolerance of Drosophila melanogaster larvae. Physiol Entomol 34: 217-223.
17. Overgaard J, Tomčala A, Sørensen JG, Holmstrup M, Krogh PH, et al. (2008) Effects of acclimation temperature on thermal tolerance and membrane phospholipid composition in the fruit fly Drosophila melanogaster. J Insect Physiol 54: 619-629.
18. Leopold RA, Rinehart JP, (2010) A template for insect cryopreservation. In: Denlinger DL, Lee RE, editors. Low Temperature Biology of Insects Cambridge Cambridge University Press pp. 325-341.
19. Morris GJ, Watson PF, (1984) Cold shock injury - a comprehensive bibliography. CryoLett 5: 352-372.
20. Novitski E, Rush G, (1949) Viability and fertility od Drosophila exposed to sub-zero temperatures. Biol Bull Mar Biol Lab, Woods Hole 97: 150-157.
21. Chiang HC, Benoit D, Maki J, (1962) Tolerance of adult Drosophila melanogaster to sub-freezing temperatures. Can Entomol 94: 722-727.
22. Tucic N, (1979) Genetic capacity for adaptation to cold resistance at different developmental stages of Drosophila melanogaster. Evolution 33: 350-358.
23. Kelty JD, Lee RE Jr, (1999) Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster. J Insect Physiol 45: 719-726.
24. Kelty JD, Lee RE Jr, (2001) Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophilidae) during ecologically based thermoperiodic cycles. J Exp Biol 204: 1659-1666.
25. MacMillan HA, Guglielmo CG, Sinclair BJ, (2009) Membrane remodeling and glucose in Drosophila melanogaster: A test of rapid cold-hardening and chilling tolerance hypotheses. J Insect Physiol 55: 243-249.
26. Lee RE Jr, Chen CP, Denlinger DL, (1987) A rapid cold-hardening process in insects. Science 238: 1415-1417.
27. Lee RE Jr, (2010) A primer on insect cold-tolerance. In: Denlinger DL, Lee RE, editors. Low Temperature Biology of Insects Cambridge Cambridge University Press pp. 3-34.
28. Muldrew K, Acker JP, Elliott JAV, McGann LE, (2004) The water to ice transition: Implications for living cells. In: Fuller B, Lane N, Benson EE, editors. Life in the Frozen State Boca Raton CRC Press pp. 67-108.
29. Privalov P, (1990) Cold denaturation of proteins. Crit Rev Biochem Mol Biol 25: 281-305.
30. Tsai CJ, Maizel JV, Nussinov R, (2002) The hydrophobic effect: A new insight from cold denaturation and two-state water structure. Crit Rev Biochem Mol Biol 37: 55-69.
31. Knight JD, Bale JS, Franks F, Mathias SF, Baust JG, (1986) Insect cold hardiness - supercooling points and prefreeze mortality. CryoLett 7: 194-203.
32. Drobnis EZ, Crowe LM, Berger T, Anchordoguy TJ, Overstreet JW, et al. (1993) Cold shock damage is due to lipid phase transition in cell membranes: a demonstration using sperm as a model. J Exp Zool 265: 432-437.
33. Hochachka PW, (1986) Defense strategies against hypoxia and hypothermia. Science 231: 234-241.
34. Rojas RR, Leopold RA, (1996) Chilling injury in the housefly: evidence for the role of oxidative stress between pupariation and emergence. Cryobiol 33: 447-458.
35. Koštál V, Vambera J, Bastl J, (2004) On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. J Exp Biol 207: 1509-1521.
36. Koštál V, Yanagimoto M, Bastl J, (2006) Chill-injury and disturbance of ion homeostasis in the coxal muscle of the tropical cockroach (Nauphoeta cinerea). Comp Biochem Physiol B 143: 171-179.
37. Kostal V, Renault D, Mehrabianova A, Bastl J, (2007) Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comp Biochem Physiol A 147: 231-238.
38. Sömme L, (1982) Supercooling and winter survival in terrestrial arthropods. Comp Biochem Physiol A 73: 519-543.
39. Storey KB, Storey JM, (1991) Biochemistry of cryoprotectants. In: Lee RE, Denlinger DL, editors. Insects at Low Temperature New York and London Chapman and Hall pp. 64-93.
40. Kostal V, (2010) Cell structural modifications in insects at low temperatures. In: Denlinger DL, Lee RE, editors. Low Temperature Biology of Insects Cambridge Cambridge University Press pp. 116-140.
41. Koštál V, Berková P, Šimek P, (2003) Remodelling of membrane phospholipids during transition to diapause and cold-acclimation in the larvae of Chymomyza costata (Drosophilidae). Comp Biochem Physiol B 135: 407-419.
42. Shimada K, Riihima A, (1990) Cold-induced freezing tolerance in diapausing and non-diapausing larvae of Chymomyza costata (Diptera: Drosophilidae) with accumulation of trehalose and proline. CryoLett 11: 243-250.
43. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, et al. (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85.
44. Gessner MO, Neumann PTM, (2005) Total lipids In: Graça MAS, Bärlocher F, Gessner MO, editors. Methods to study litter decomposition: A practical guide Berlin Springer pp. 103-107.
45. DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F, (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28: 350-356.
46. Bueding E, Orrell SA, (1964) A mild procedure for the isolation of polydisperse glycogen from animal tissue. J Biol Chem 239: 4018-4020.
47. Koštál V, Zahradníčková H, Šimek P, Zelený J, (2007) Multiple component system of sugars and polyols in the overwintering spruce bark beetle, Ips typographus. J Insect Physiol 53: 580-586.
48. Hušek P, (1997) Urine organic acid profiling by capillary gas chromatography after a simple sample pretreatment. Clin Chem 43: 1999-2001.
49. Hušek P, Šimek P, (2001) Advances in amino acid analysis. LC-GC North Am 19: 986-999.
50. Folch J, Lees M, Sloane Stanley GH, (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497-509.
51. Koštál V, Šimek P, (1998) Changes in fatty acid composition of phospholipids and triacylglycerols after cold-acclimation of an aestivating insect prepupa. J Comp Physiol B 168: 453-460.
52. Tomčala A, Tollarová M, Overgaard J, Šimek P, Koštál V, (2006) Seasonal acquisition of chill-tolerance and restructuring of membrane glycerophospholipids in an overwintering insect: triggering by low temperature, desiccation and diapause progression. J Exp Biol 209: 4102-4114.
53. Hoffmann AA, Anderson A, Hallas R, (2002) Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecol Lett 5: 614-618.
54. Gilchrist GW, Huey RB, Partridge L, (1997) Thermal sensitivity of Drosophila melanogaster: Evolutionary responses of adults and eggs to laboratory natural selection at different temperatures. Physiol Zool 70: 403-414.
55. Powell SJ, Bale JS, (2005) Low temperature acclimated populations of the grain aphid Sitobion avenae retain abiltiy to rapidly cold harden with enhanced fitness. J Exp Biol 208: 2615-2620.
56. Shintani Y, Ishikawa Y, (2007) Relationship between rapid cold-hardening and cold acclimation in the eggs of the yellow-spotted longicorn beetle, Psacothea hilaris. J Insect Physiol 53: 1055-1062.
57. Koštál V, (2006) Eco-physiological phases of insect diapause. J Insect Physiol 52: 113-127.
58. Duman JG, (1979) Thermal hysteresis factors in overwintering insects. J Insect Physiol 25: 805-810.
59. Duman JG, (2001) Antifreeze and ice nuclator proteins in terrestrial arthropods. Annu Rev Physiol 63: 327-357.
60. Zachariassen KE, Kristiansen E, (2000) Ice nucleation and antinucleation in nature. Cryobiol 41: 257-279.
61. Rinehart JP, Li A, Yocum GD, Robich RM, Hayward SAL, et al. (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc Natl Acad Sci U S A 104: 11130-11137.
62. Koštál V, Tollarová-Borovanská M, (2009) The 70 kDa heat shock protein assists during the reparation of chilling injury in the insect, Pyrrhocoris apterus. PLoS One 4: e4546.
63. Nedvěd O, (1998) Modelling the relationship between cold injury and accumulated degree days in terrestrial arthropods. CryoLett 19: 267-274.
64. Nedvěd O, Lavy D, Verhoef HA, (1998) Modelling the time-temperature relationship in cold injury and effect of high-temperature interruptions on survival in a chill-sensitive collembolan. Funct Ecol 12: 816-824.
65. Hoekstra FA, Golovina EA, Buitink J, (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6: 431-438.
66. Kandror O, DeLeon A, Goldberg AL, (2002) Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Nat Acad Sci USA 99: 9727-9732.
67. Hincha DK, Hagemann M, (2004) Stabilization of model membranes during drying by compatible solutes involved in the stress tolerance of plants and microorganisms. Biochem J 383: 277-283.
68. Hengherr S, Heyer AG, Köhler H-R, Schill RO, (2007) Trehalose and anhydrobiosis in tardigrades - evidence for divergence of responses to dehydrarion. FEBS J 275: 281-288.
69. Schill RO, Mali B, Dandekar T, Schnölzer M, Reuter D, et al. (2009) Molecular mechanisms of tolerance in tardigrades: New perspectives for preservation and stabilization of biological material. Biotechnol Adv 27: 348-352.
70. Storey KB, Baust JG, Storey JM, (1981) Intermediary metabolism during low temperature acclimation in the overwintering gall fly larva, Eurosta solidaginis. J Comp Physiol 144: 183-190.
71. Morgan TD, Chippendale GM, (1983) Free amino acids of the haemolymph of the Southwestern corn borer and the European corn borer in relation to their diapause. J Insect Physiol 29: 735-740.
72. Fields PG, Fleurat-Lessard F, Lavenseau L, Febvay G, Peypelut L, et al. (1998) The effect of cold acclimation and deacclimation on cold tolerance, trehalose and free amino acid levels in Sitophilus granarius and Cryptolestes ferrugineus (Coleoptera). J Insect Physiol 44: 955-965.
73. Renault D, Bouchereau A, Delettre YR, Hervant F, Vernon P, (2006) Changes in free amino acids in Alphitobius diaperinus (Coleoptera: Tenebrionidae) during thermal and food stress. Comp Biochem Physiol A 143: 279-285.
74. Zachariassen KE, (1985) Physiology of cold tolerance in insects. Physiol Rev 65: 799-832.
75. Sakurai M, Furuki T, Akao K, Tanaka D, Nakahara Y, et al. (2008) Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplancki. Proc Natl Acad Sci USA 105: 5093-5098.
76. Hengherr S, Worland MR, Reuner A, Brümmer F, Schill RO, (2009) High temperature tolerance in anhydrobiotic tardigrades is limited by glass transition. Physiol Biochem Zool 82: 749-755.
77. Sformo T, Walters K, Jeannet K, Wowk B, Fahy GM, et al. (2010) Deep supercooling, vitrification and limited survival to -100 degrees C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae. J Exp Biol 213: 502-509.
78. Arakawa T, Timasheff SN, (1983) Preferential interactions of proteins with solvent components in aquaeous amino acid solutions. Arch. Biochem Biophys 224: 169-177.
79. Arakawa T, Timasheff SN, (1985) The stabilization of proteins by osmolytes. Biophys J 47: 411-414.
80. Lee DH, Goldberg AL, (1998) Proteasome inhibitors cause induction of heat shock proteins and trehalose, which together confer thermotolerance in Sacharomyces cerevisiae. Mol Cell Biol 18: 30-38.
81. Viner RI, Clegg JS, (2001) Influence of trehalose on the molecular chaperone activity of p26, a small heat shock/α-crystallin protein. Cell Stress Chaperones 6: 126-135.
82. Benaroudj N, Lee DH, Goldberg AL, (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 29: 24261-24267.
83. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN, (1982) Living with water stress: Evolution of osmolyte systems. Science 217: 1214-1222.
84. Crowe JH, Crowe LM, Carpenter JF, Wistrom AC, (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242: 1-10.
85. Crowe JH, (2002) Lessons from nature: The role of sugars in anhydrobiosis. Comp Biochem Physiol A 131: 505-513.
86. Overgaard J, Malmendal A, Sørensen JG, Bundy JG, Loeschke V, et al. (2007) Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J Insect Physiol 53: 1218-1232.
87. Misener SR, Chen C-P, Walker VK, (2001) Cold tolerance and proline metabolic gene expression in Drosophila melanogaster. J Insect Physiol 47: 393-400.
88. Sinensky M, (1974) Homeoviscous adaptation - a homeostatic process that regulates viscosity of membrane lipids in Escherichia coli. Proc Nat Acad Sci USA 71: 522-525.
89. Cossins AR, Prosser CL, (1978) Evolutionary adaptation of membranes to temperature. Proc Nat Acad Sci USA 75: 2040-2043.
90. Hazel JR, (1995) Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation? Annu Rev Physiol 57: 19-42.
91. Hazel JR, (1989) Cold adaptation in ectotherms: Regulation of membrane function and cellular metabolism. Adv Comp Environ Physiol 4: 1-50.
92. Hodková M, Berková P, Zahradníčková H, (2002) Photoperiodic regulation of the phospholipid molecular species composition in thoracic muscles and fat body of Pyrrhocoris apterus (Heteroptera) via an endocrine gland, corpus allatum. J Insect Physiol 48: 1009-1019.
93. Overgaard J, Sørensen JG, Petersen SO, Loeschke V, Holmstrup M, (2005) Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. J Insect Physiol 51: 1173-1182.
94. Overgaard J, Sørensen JG, Petersen SO, Loeschke V, Holmstrup M, (2006) Reorganization of membrane lipids during fast and slow cold hardening in Drosophila melanogaster. Physiol Entomol 31: 328-335.