Desiccation tolerance in the tardigrade Richtersius coronifer relies on muscle mediated structural reorganization

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Halberg, Kenneth Agerlin ^a   Jørgensen, Aslak ^a   Møbjerg, Nadja ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACCLIMATIZATION; ANIMALS; BODY PATTERNING; BODY SIZE; DEHYDRATION; ENERGY METABOLISM; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MITOCHONDRIA; MUSCLES; TARDIGRADA;

EID: 84894060840     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085091     Document Type: Article

References (37)

1. Keilin D (1959) The problem of anabiosis or latent life: history and current concepts. Proc R Soc Lond B 150: 149-191. doi:10.1098/rspb.1959.0013. PubMed: 13633975.
2. Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409: 1092-1101. doi:10.1038/35059215. PubMed: 11234023. (Pubitemid 32204065)
3. Clegg JS (2001) Cryptobiosis - a peculiar state of biological organization. Comp Biochem Physiol B Biochem Mol Biol 128: 613-624. doi:10.1016/S1096-4959(01)00300-1. PubMed: 11290443.
4. Campbell LI, Rota-Stabelli O, Edgecombe GD, Marchioro T, Longhorn SJ et al. (2011) MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda. Proc Natl Acad Sci U S A 108: 15920-15924. doi:10.1073/pnas.1105499108. PubMed: 21896763.
5. Goldstein B, Blaxter M (2002) Tardigrades. Curr Biol 12: R475. doi:10.1016/S0960-9822(02)00959-4. PubMed: 12176341.
6. Nelson DR (2002) Current status of the Tardigrada: evolution and ecology. Integr Comp Biol 42: 652-659. doi:10.1093/icb/42.3.652. PubMed: 21708761.
7. Persson DK, Halberg KA, Jørgensen A, Møbjerg N, Kristensen RM (2012) Neuroanatomy of Halobiotus crispae (Eutardigrada: Hypsibiidae): Tardigrade brain structure supports the clade Panarthropoda. J Morphol 273: 1227-1245. doi:10.1002/jmor.20054. PubMed: 22806919.
8. 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. (Pubitemid 47215172)
9. Guidetti R, Altiero T, Rebecchi L (2011) On dormancy strategies in tardigrades. J Insect Physiol 57: 567-576. doi:10.1016/j.jinsphys.2011.03.003. PubMed: 21402076.
10. Møbjerg N, Halberg KA, Jørgensen A, Persson D, Bjørn M et al. (2011) Survival in extreme environments - on the current knowledge of adaptations in tardigrades. Acta Physiol Scand 202: 409-420.
11. Wełnicz W, Grohme MA, Kaczmarek L, Schill RO, Frohme M (2011) Anhydrobiosis in tardigrades - the last decade. J Insect Physiol 57: 577-583. doi:10.1016/j.jinsphys.2011.03.019. PubMed: 21440551.
12. Clegg JS (1965) The origin of trehalose and its significance during formation of encysted dormant embryos of Artemia salina. Comp Biochem Physiol 14: 135-143. doi:10.1016/0010-406X(65)90014-9. PubMed: 14288194.
13. Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54: 579-599. doi:10.1146/annurev.ph.54.030192.003051. PubMed: 1562184.
14. Crowe LM (2002) Lessons from nature: the role of sugars in anhydrobiosis. Comp Biochem Physiol A 13: 505-513. PubMed: 11867276.
15. Halberg KA, Larsen KW, Jørgensen A, Ramløv H, Møbjerg N (2013) Inorganic ion composition in Tardigrada: cryptobionts contain large fraction of unidentified organic solutes. J Exp Biol 216: 1235-1243. doi:10.1242/jeb.075531. PubMed: 23239888.
16. Hengherr S, Heyer AG, Köhler HR, Schill RO (2008) Trehalose and anhydrobiosis in tardigrades - evidence for divergence in response to dehydration. FEBS 275: 281-288.
17. Reuner A, Hengherr S, Brahim M, Förster F, Arndt D et al. (2010) Stress response in tardigrades: differential gene expression of molecular chaperones. Cell Stress Chap 15: 423-430. doi:10.1007/s12192-009-0158-1. PubMed: 19943197.
18. Rizzo AM, Negroni M, Altiero T, Montorfano G, Corsetto P et al. (2010) Antioxidant defenses in hydrated and desiccated states of the tardigrade Paramacrobiotus richtersi. Comp Biochem Physiol B 156: 115-121. doi:10.1016/j.cbpb.2010.02.009. PubMed: 20206711.
19. Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94: 791-812. doi:10.1007/s00114-007-0254-y. PubMed: 17479232. (Pubitemid 47367664)
20. Crowe JH, Madin KA (1974) Anhydrobiosis in tardigrades and nematodes. Trans Am Microsc Soc 93: 513-524. doi:10.2307/3225155.
21. Ricci C, Melone G, Santo N, Caprioli M (2003) Morphological response of a bdelloid rotifer to desiccation. J Morphol 257: 246-253. doi:10.1002/jmor. 10120. PubMed: 12833383. (Pubitemid 36922347)
22. Crowe JH (1975) The physiology of cryptobiosis in tardigrades. Mem 1st Ital Idrobiol 32: 37-59
23. Wright JC (1989a) Desiccation tolerance and water-retentive mechanisms in tardigrades. J Exp Biol 142: 267-292.
24. Wright JC (1989b) The tardigrade cuticle. II. Evidence for a dehydration-dependent permeability barrier in the intracuticle. Tissue Cell 21: 263-279. doi:10.1016/0040-8166(89)90071-2.
25. Ricci C, Caprioli M, Fontaneto D, Melone G (2008) Volume and morphology changes of a bdelloid rotifer species (Macrotrachela quadricornifera) during anhydrobiosis. J Morphol 269: 233-239. doi:10.1002/jmor.10579. PubMed: 17957710. (Pubitemid 351156112)
26. Wharton DA, Barrett J (1985) Ultrastructural changes during recovery from anabiosis in the plant parasitic nematode, Ditylenchus. Tissue Cell 17: 79-96. doi:10.1016/0040-8166(85)90017-5. PubMed: 4002213.
27. 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. PubMed: 12177145. (Pubitemid 35180886)
28. Persson D, Halberg KA, Jørgensen A, Ricci C, Møbjerg N et al. (2011) Extreme stress tolerance in tardigrades: Surviving space conditions in low earth orbit. J Zool Syst Evol Res 49: 90-97. doi:10.1111/j.1439-0469. 2010.00605.x.
29. Jönsson IK, Rabbow E, Schill RO, Harms-Ringdahl M, Rettberg P (2008) Tardigrades survive exposure to space in low Earth orbit. Curr Biol 18: R729-R731. doi:10.1016/j.cub.2008.06.048. PubMed: 18786368.
30. Loomis WF, Lipmann F (1948) Reversible inhibition of the coupling between phosphorylation and oxidation. J Biol Chem 173: 807-808. PubMed: 18910739.
31. Halberg KA, Møbjerg N (2012) First evidence of epithelial transport in tardigrades: Comparative investigation of organic anion transport. J Exp Biol 215: 497-507. doi:10.1242/jeb.065987. PubMed: 22246258.
32. Barden JA, Miki M, Hambly BD, Dos Remedios CG (1987) Localization of the phalloidin and nucleotide-binding sites on actin. Eur J Biochem 162: 583-588. doi:10.1111/j.1432-1033.1987.tb10679.x. PubMed: 3830158. (Pubitemid 17023111)
33. Ramazzotti G, Maucci W (1983) Il Phylum Tardigrada. Terza edizione riveduta e corretta.Mem Insti Ital Idro Dott Marco de Marchi 41: 1-1012.
34. Halberg KA, Persson D, Ramløv H, Westh P, Kristensen RM et al. (2009) Cyclomorphosis in Tardigrada: Adaptation to environmental constraints. J Exp Biol 212: 2803-2811. doi:10.1242/jeb.029413. PubMed: 19684214.
35. Møbjerg N, Jørgensen A, Eibye-Jacobsen J, Halberg KA, Persson D et al. (2007) New records on cyclomorphosis in the marine eutardigrade Halobiotus crispae. J Limnol 66: 132-140. (Pubitemid 47215179)
36. Schmidt-Rhaesa A, Kulessa J (2007) Muscular architecture of Milnesium tardigradum and Hypsibius sp. (Eutardigrada, Tardigrada) with some data on Ramazzottius oberhaeuseri. Zoomorphology 126: 265-281. doi:10.1007/s00435-007- 0046-0. (Pubitemid 50001691)
37. Halberg KA, Persson D, Møbjerg N, Wanninger A, Kristensen RM (2009) Myoanatomy of the marine tardigrade Halobiotus crispae (Eutardigrada: Hypsibiidae). J Morphol 270: 996-1013. doi:10.1002/jmor.10734. PubMed: 19274743.