Anhydrobiotic abilities of tardigrades

Topics in Current Genetics

Volumn 21, Issue , 2010, Pages 133-146

  Schill, Ralph O ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77955931739     PISSN: 16102096     EISSN: 16106970     Source Type: Book Series    
DOI: 10.1007/978-3-642-12422-8_8     Document Type: Article

References (101)

1. Alpert P (2000) The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecol 151:5-17
2. Bahrndorff S, Tunnacliffe A, Wise MJ, McGee B, Holmstrup M, Loeschcke V (2009) Bioinformatics and protein expression analyses implicate LEA proteins in the drought response of Collembola. J Insect Physiol 55:210-217
3. Battista JR, Park MJ, McLemore AE (2001) Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology 43:133-139
4. Baumann H (1922) Die Anabiose der Tardigraden. Zool Jahrb 45:501-556
5. Baumann H (1927) Anabiosis of tardigrades. Zool Anz 72:175-179
6. Browne J, Tunnacliffe A, Burnell A (2002) Anhydrobiosis - plant desiccation gene found in a nematode. Nature 416:38
7. Carpenter JF, Crowe LM, Crowe JH (1987) Stabilization of phosphofructokinase with sugars during freeze-drying characterization of enhanced protection in the presence of divalent cations. Biochim Biophys Acta 923:109-115
8. Chandler J, Bartels D (1999) Plant desiccation. In: Lerner HR (ed) Plant Responses to Environmental Stresses: From Phytohormones to Genome Reorganization. Marcel Dekker, New York, pp 575-590
9. Clegg JS (1965) Origin of trehalose and its significance during formation of encysted dormant embryos of Artemia salina. Comp Biochem Physiol 14:135-143
10. Clegg JS (1967) Metabolic studies of crytobiosis in encysted embryos of Artemia salina. Comp Biochem Physiol 20:801-809
11. Clegg JS (1974) Biochemical adaptations associated with the embryonic dormancy of Artemia salina. Trans Am Microsc Soc 93:481-490
12. Clegg JS (1986) The physical properties and metabolic status of Artemia cysts at low water contents: the water replacement hypothesis. In: Leopold AC (ed) Membranes, Metabolism and Dry Organisms Cornell University Press, New York, pp 169-187
13. Clegg JS, Jackson SA, Warner AH (1994) Extensive intracellular translocations of a major protein accompany anoxia in embryos of Artemia franciscana. Exp Cell Res 212:77-83
14. Clegg JS, Jackson SA, Liang P, Macrae TH (1995) Nuclear-cytoplasmic translocations of protein p26 during aerobic-anoxic transitions in embryos of Artemia franciscana. Exp Cell Res 219:1-7
15. Crowe JH (1975) The physiology of cryptobiosis in tardigrades. Memorie dell'Istituto Italiano di Idrobiologia Dott Marco de Marchi 32:37-59
16. Crowe LM (2002) Lessons from nature: The role of sugars in anhydrobiosis. Comp Biochem Physiol A Mol Integr Physiol 131:505-513
17. Crowe JH, Clegg JS (1973) Anhydrobiosis dowden. Hutchinson and Ross, Stroudsburg, PA, p 477
18. Crowe JH, Clegg JS (eds) (1978) Dry biological systems. Academic, New York
19. Crowe JH, Madin KAC (1975) Anhydrobiosis in nematodes evaporative water loss and survival. J Exp Zool 193:323-334
20. Crowe JH, Crowe LM, Carpenter JF, Wistrom CA (1987) Stabilization of dry phospholipidbilayers and proteins by sugars. Biochem J 242:1-10
21. Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73-103
22. Crowe JH, Crowe LM, Petrelski S, Hoekstra FA, Araujo PD, Panek AD (1997) Anhydrobiosis: cellular adaptation to extreme dehydration. In: Dantzler WH (ed) Handbook of Physiology. Oxford University Press, New York
23. Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579-599
24. de Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the alpha-crystallin-small heatshock protein superfamily. Int J Biol Macromol 22:151-162
25. Doyère PLN (1842) Memoires sur les Tardigrades. Sur le facilité que possedent les Tardigrades, les rotiferes, les anguillules des toits et quelques autres animalcules, de revenir à la vie après été completement desséchées. Ann Sci Nat Zool Biol Anim 2e:5-35
26. Ehrenberg CG (1834) €Uber das Wiederaufleben der Moosfauna. Okens Isis 6(7):710-713
27. Eichhorn JC (1781) Beytr€age zur Naturgeschichte der kleinsten Wasserthiere, die mit blossem Auge nicht können gesehen werden und die sich in den Gew€assern in und um Danzig befinden. F. Nicolai, Berlin and Stettin
28. Ellis JR (2004) From chloroplasts to chaperones: How one thing led to another. Photosynth Res 80:333-343
29. Franceschi T (1948) Anabiosi nei tardigradi. Boll Mus Ist Biol Univ Genova 22:47-49
30. Galau GA, Hughes DW, Dure L III (1986) Abscisic-acid induction of cloned cotton gossypium- hirsutum late embryogenesis-abundant lea messenger rna species. Plant Mol Biol 7:155-170
31. Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33-45
32. Gladyshev E, Meselson M (2008) Extreme resistance of bdelloid rotifers to ionizing radiation. Proc Natl Acad Sci USA 105:5139-5144
33. Gnaiger E,MéndezG, Hand SC (2000) High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proc Natl Acad Sci USA 97:11080-11085
34. Goeze JAE (1773) Herrn Karl Bonnets Abhandlungen aus der Insektologie aus d. Franz. €ubers. u. mit einigen Zus€atzen hrsg. v. Joh. August Ephraim Goeze Gebauer, Halle. p 414
35. Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J, Tunnacliffe A (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem 278:12977-12984
36. Goyal K, Pinelli C, Maslen SL, Rastogi RK, Stephens E, Tunnacliffe A (2005) Dehydrationregulated processing of late embryogenesis abundant protein in a desiccation-tolerant nematode. FEBS Lett 579:4093-4098
37. Grzelezak ZF, Sattalo MH, Hanley-Bowdoin LK, Kennedy TD, Lane BG (1982) Synthesis and turnover of proteins and mRNA in germinating wheat embryos. Can J Biochem Physiol 60(3): 389-397
38. Guidetti R, Jönsson KI (2002) Long-term anhydrobiotic survival in semi-terrestrial micrometazonas.
39. J Zool (1987) 257:181-187
40. Hand SC (1998) Quiescence in Artemia franciscana embryos: reversible arrest of metabolism and gene expression at low oxygen levels. J Exp Biol 201:1233-1242
41. Hand SC, Hardewig I (1996) Downregulation of cellular metabolism during environmental stress: Mechanisms and implications. Annu Rev Physiol 58:539-563
42. Hengherr S, Br€ummer F, Schill RO (2008a) Anhydrobiosis in tardigrades and its effects on longevity traits. J Zool (1987) 275:216-220
43. Hengherr S, Heyer AG, Br€ummer F, Schill RO (2008b) Trehalose as protecting agent in aquatic invertebrates during dormancy induced by desiccation. Comp Biochem Physiol A Comp Physiol 151:S34
44. Hengherr S, Heyer AG, Köhler HR, Schill RO (2008c) Trehalose and anhydrobiosis in tardigrades - evidence for divergence in responses to dehydration. FEBS J 275:281-288
45. Hengherr S, Worland MR, Reuner A, Br€ummer F, Schill RO (2009) High-temperature tolerance in anhydrobiotic tardigrades is limited by glass transition. Physiol Biochem Zool 82:749-755
46. Hightower LEH (1993) A brief perspective on the heat-shock response and stress proteins. Mar Environ Res 35:79-83
47. Hoekstra FA, Crowe JH, Crowe LM (1992a) Germination and ion leakage are linked with phase transitions ofmembrane lipids during imbibition of Typha latifolia pollen. Physiol Plant 84:29-34
48. Hoekstra FA, Crowe JH, Crowe LM, van Roekel T, Vermeer E (1992b) Do phospholipids and sucrose determine membrane phase transitions in dehydrating pollen species? Plant Cell Environ 15(5):601-606
49. Horikawa DD, Sakashita T, Katagiri C, Watanabe M, Kikawada T, Nakahara Y, Hamada N, Wada S, Funayama T, Higashi S, Kobayashi Y, Okuda T, Kuwabara M (2006) Radiation tolerance in the tardigrade Milnesium tardigradum. Int J Radiat Biol 82:843-848
50. Hufeland CW (1817) Makrobiotik - Die Kunst das menschliche Leben zu verl€angern. Fleischhauer, Reutlingen Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377-403
51. Jönsson KI, Bertolani R (2001) Facts and fiction about long-term survival in tardigrades. J Zool (Lond) 255:121-123
52. Jönsson KI, Schill RO (2007) Induction of Hsp70 by desiccation, ionising radiation and heat-shock in the eutardigrade Richtersius coronifer. J Comp Physiol B 146:456-460
53. Jönsson KI, Harms-Ringdahl M, Torudd J (2005) Radiation tolerance in the eutardigrade Richtersius coronifer. Int J Radiat Biol 81:649-656
54. Jørgensen A, Møbjerg N, Kristensen RM (2007) A molecular study of the tardigrade Echiniscus testudo (Echiniscidae) reveals low DNA sequence diversity over a large geographical area. J Limnol 66:77-83
55. Keilin D (1959) The Leeuwenhoek Lecture. The problem of anabiosis or latent life: History and current concept. Proc R Soc Lond B Biol Sci 150:149-191
56. Kikawada T, Nakahara Y, Kanamori Y, Iwata K, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem Biophys Res Commun 348:56-61
57. Lapinski J, Tunnacliffe A (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett 553:387-390
58. Liang P, MacRae TH (1999) The synthesis of a small heat shock/alpha-crystallin protein in Artemia and its relationship to stress tolerance during development. Dev Biol 207:445-456
59. Liang P, Amons R, Clegg JS, MacRae TH (1997a) Molecular characterization of a small heat shock alpha-crystallin protein in encysted Artemia embryos. J Biol Chem 272:19051-19058
60. Liang P, Amons R, Macrae TH, Clegg JS (1997b) Purification, structure and in vitro molecularchaperone activity of Artemia p26, a small heat-shock/alpha-crystallin protein. Eur J Biochem 243:225-232
61. Madin KAC, Crowe JH (1975) Anhydrobiosis in nematodes - carbohydrate and lipid-metabolism during dehydration. J Exp Zool 193:335-342
62. McGee B, Schill RO, Tunnacliffe A (2004) Hydrophilic proteins in invertebrate anhydrobiosis. Integr Comp Biol 44:679-679
63. Neumann S, Reuner A, Br€ummer F, Schill RO (2009) DNA damage in storage cells of anhydrobiotic tardigrades. Comp Biochem Physiol A Mol Integr Physiol 153(4):425-429
64. Okuda T, Watanabe M, Kikawada T, Fujita A, Forczek E (2004) Cryptobiosis in the african chironomid: Physiological mechanism to survive complete dehydration. Proc Arthropod Embryol Soc Jpn 39:1-7
65. Potts M (2001) Desiccation tolerance: a simple process? Trends Microbiol 9:553-559 O
66. rstan A (1998) Factors affecting long-term survival of dry bdelloid rotifers: a preliminary study. Hydrobiologia 387/388:327-331
67. Rahm P (1921) Effect of very low temperatures on the fauna of moss. Proc K Ned Akad Wet Ser C Biol Med Sci 23:235-248
68. Ramløv H, Westh P (2001) Cryptobiosis in the eutardigrade Adorybiotus (Richtersius) coronifer: Tolerance to alcohols, temperature and de novo protein synthesis. Zool Anz 240:517-523
69. Rebecchi L, Guidetti R, Borsari S, Altiero T, Bertolani R (2006) Dynamics of long-term anhydrobiotic survival of lichen-dwelling tardigrades. Hydrobiologia 558:23-30
70. Ricci C (1998) Anhydrobiotic capabilities of bdelloid rotifers. Hydrobiologia 387(388):321-326
71. Ricci C, Caprioli M (1998) Stress during dormancy: Effect on recovery rates and life-history traits of anhydrobiotic animals. Aquat Ecol 32:353-359
72. Ricci C, Caprioli M (2005) Anhydrobiosis in bdelloid species, populations and individuals. Integr Comp Biol 45:759-763
73. Ricci C, Covino C (2005) Anhydrobiosis of Adineta ricciae: Costs and Benefits. Hydrobiologia 546:307-314
74. Ricci C, Pagani M (1997) Desiccation of Panagrolaimus rigidus (nematoda): Survival, reproduction and the influence on the internal clock. Hydrobiologia 347:1-13
75. Ricci C, Vaghi L, Manzini ML (1987) Desiccation of rotifers (Macrotrachela quadricornifera): Survival and reproduction. Ecology 68:1488-1494
76. Sakurai M, Furuki T, K-i A, Tanaka D, Nakahara Y, Kikawada T, Watanabe M, Okuda T (2008) Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. Proc Natl Acad Sci USA 105:5093-5098
77. Schill RO, Fritz GB (2008) Desiccation tolerance in embryonic stages of the tardigrade Milnesium tardigradum. J Zool (Lond) 276:103-107
78. Schill R, Steinbr€uck G, Köhler H (2004) Stress gene (hsp70) sequences and quantitative expression in Milnesium tardigradum (Tardigrada) during active and cryptobiotic stages. J Exp Biol 207:1607-1613
79. Schill RO, Neumann S, Reuner A, Br€ummer F (2008) Detection of DNA damage with single-cell gel electrophoresis in anhydrobiotic tardigrades. Comp Biochem Physiol A Comp Physiol 151:S32
80. Schöneich C (1999) Reactive oxygen species and biological aging: amechanistical approach. Exp Gerontol 34:19-34
81. Schultze CAS (1834) Macrobiotus hufelandii, animale e crustaceorum classe novum, Berlin, p 8
82. Spallanzani L (1776) Opuscoli di Fisica Animale e Vegetabile. Modena: Società Tipografica, pp 203-285
83. Sun Y, MacRae TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62:2460-2476
84. Sun WQ, Irving TC, Leopold AC (1984) The role of sugar, vitrification and membrane phase transition in seed desiccation tolerance. Physiol Plant 90(4):621-628
85. Tomos D (1992) Life without water. Curr Biol 2:594-596
86. Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791-812
87. Tunnacliffe A, Lapinski J, McGee B (2005) A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546:315-321
88. van Breukelen F, Hand SC (2000) Characterization of ATP-dependent proteolysis in embryos of the brine shrimp, Artemia franciscana. J Comp Physiol B 170:125-133
89. van Breukelen F, Maier R, Hand SC (2000) Depression of nuclear transcription and extension of mRNA half-life under anoxia in Artemia franciscana embryos. J Exp Biol 203:1123-1130
90. van Leeuwenhoek A (1702) On certain animalcules found in the sediments in gutters of the roofs of houses. Letter 144. The Selected Works of Anton van Leeuwenhoek, London, pp 207-213
91. Vertucci CW, Farrant JM (1995) Acquisition and loss of desiccation Marcel Dekker: New York
92. Watanabe M, Kikawada T, Minagawa N, Yukuhiro F, Okuda T (2002) Mechanism allowing an insect to survive complete dehydration and extreme temperatures. J Exp Biol 205:2799-2802
93. Watanabe M, Kikawada T, Okuda T (2003) Increase of internal ion concentration triggers trehalose synthesis associated with cryptobiosis in larvae of Polypedilum vanderplanki. J Exp Biol 206:2281-2286
94. Webb SJ (1964) Bound water, metabolites and genetic continuity. Nature 203:374-377
95. Webb SJ, Dumasia MD, Bhorjee JS (1965) Bound Water, Inositol, and the Biosynthesis of Temperate and Virulent Bacteriophages by Air-Dried Escherichia coli. Can J Microbiol 11:141-150
96. Westh P, Ramlov H (1991) Trehalose accumulation in the tardigrade Adorybiotus coronifer during anhydrobiosis. J Exp Zool 258:303-311
97. Westh P, Ramløv H (1988) Cryptobiosis in Arctic tardigrades with special attention to the appearance of trehalose. In: Höpner Petersen G (ed) Grönland Exkursion 2.-25., August 1987. Institut f€ur Polarökologie, Kiel, pp 227-245
98. Wharton DA (2002) Nematode survival strategies. In: Lee DL (ed) The biology of nematodes. Taylor and Francis, London, pp 389-411
99. Womersley C (1981) Biochemical and physiological aspects of anhydrobiosis. Comp Biochem Physiol B Biochem Mol Biol 70:669-678
100. Wright JC, Westh P, Ramlov H (1992) Cryptobiosis in Tardigrada. Biol Rev 67:1-29
101. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214-1222