1932

Abstract

Tardigrades are ubiquitous meiofauna that are especially renowned for their exceptional extremotolerance to various adverse environments, including pressure, temperature, and even ionizing radiation. This is achieved through a reversible halt of metabolism triggered by desiccation, a phenomenon called anhydrobiosis. Recent establishment of genome resources for two tardigrades, and , accelerated research to uncover the molecular mechanisms behind anhydrobiosis, leading to the discovery of many tardigrade-unique proteins. This review focuses on the history, methods, discoveries, and current state and challenges regarding tardigrade genomics, with an emphasis on molecular anhydrobiology. Remaining questions and future perspectives regarding prospective approaches to fully elucidate the molecular machinery of this complex phenomenon are discussed.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-animal-021419-083711
2022-02-15
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/animal/10/1/annurev-animal-021419-083711.html?itemId=/content/journals/10.1146/annurev-animal-021419-083711&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Guidetti R, Altiero T, Rebecchi L 2011. On dormancy strategies in tardigrades. J. Insect Physiol. 57:567–76
    [Google Scholar]
  2. 2. 
    Hibshman JD, Clegg JS, Goldstein B. 2020. Mechanisms of desiccation tolerance: themes and variations in brine shrimp, roundwords, and tardigrades. Front. Physiol. 11:592016
    [Google Scholar]
  3. 3. 
    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. 202:409–20
    [Google Scholar]
  4. 4. 
    Wełnicz W, Grohme MA, Kaczmarek L, Schill RO, Frohme M. 2011. Anhydrobiosis in tardigrades—the last decade. J. Insect Physiol. 57:577–83
    [Google Scholar]
  5. 5. 
    Clegg JS. 2001. Cryptobiosis—a peculiar state of biological organization. Comp. Biochem. Physiol. B 128:613–24
    [Google Scholar]
  6. 6. 
    Neuman Y. 2006. Cryptobiosis: a new theoretical perspective. Prog. Biophys. Mol. Biol. 92:258–67
    [Google Scholar]
  7. 7. 
    Crowe JH. 1971. Anhydrobiosis: an unsolved problem. Am. Nat. 105:563–73
    [Google Scholar]
  8. 8. 
    Crowe JH, Hoekstra FA, Crowe LM. 1992. Anhydrobiosis. Annu. Rev. Physiol. 54:579–99
    [Google Scholar]
  9. 9. 
    Keilin D. 1959. The problem of anabiosis or latent life: history and current concept. Proc. R. Soc. Lond. B 150:149–91
    [Google Scholar]
  10. 10. 
    Guidetti R, Jönsson KI. 2002. Long-term anhydrobiotic survival in semi-terrestrial micrometazoans. J. Zool. 257:181–87
    [Google Scholar]
  11. 11. 
    Watanabe M. 2006. Anhydrobiosis in invertebrates. Appl. Entomol. Zool. 41:15–31
    [Google Scholar]
  12. 12. 
    Tsujimoto M, Imura S, Kanda H. 2016. Recovery and reproduction of an Antarctic tardigrade retrieved from a moss sample frozen for over 30 years. Cryobiology 72:78–81
    [Google Scholar]
  13. 13. 
    Becquerel P. 1950. La suspension de la vie au dessous de 1/20 K absolu par demagnetization adiabatique de l'alun de fer dans le vide les plus eleve. C. R. Hebd. Seance Acad. Sci. Paris 231:26
    [Google Scholar]
  14. 14. 
    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. 82:749–55
    [Google Scholar]
  15. 15. 
    Horikawa DD, Yamaguchi A, Sakashita T, Tanaka D, Hamada N et al. 2012. Tolerance of anhydrobiotic eggs of the Tardigrade Ramazzottius varieornatus to extreme environments. Astrobiology 12:283–89
    [Google Scholar]
  16. 16. 
    Ono F, Mori Y, Takarabe K, Fujii A, Saigusa M et al. 2016. Effect of ultra-high pressure on small animals, tardigrades, and Artemia. . Cogent Phys. 3:1167575
    [Google Scholar]
  17. 17. 
    Ramløv H, Westh P. 2001. Cryptobiosis in the eutardigrade Adorybiotus (Richtersius) coronifer: tolerance to alcohols, temperature and de novo protein synthesis. Zool. Anz. J. Comp. Zool. 240:517–23
    [Google Scholar]
  18. 18. 
    Horikawa DD, Kunieda T, Abe W, Watanabe M, Nakahara Y et al. 2008. Establishment of a rearing system of the extremotolerant tardigrade Ramazzottius varieornatus: a new animal model for astrobiology. Astrobiology 8:549–56
    [Google Scholar]
  19. 19. 
    Beltrán-Pardo E, Jönsson KI, Harms-Ringdahl M, Haghdoost S, Wojcik A 2015. Tolerance to gamma radiation in the Tardigrade Hypsibius dujardini from embryo to adult correlate inversely with cellular proliferation. PLOS ONE 10:e0133658
    [Google Scholar]
  20. 20. 
    Horikawa DD, Sakashita T, Katagiri C, Watanabe M, Kikawada T et al. 2006. Radiation tolerance in the tardigrade Milnesium tardigradum. . Int. J. Radiat. Biol. 82:843–48
    [Google Scholar]
  21. 21. 
    Jönsson KI, Harms-Ringdahl M, Torudd J. 2005. Radiation tolerance in the eutardigrade Richtersius coronifer. . Int. J. Radiat. Biol. 81:649–56
    [Google Scholar]
  22. 22. 
    Jönsson KI, Rabbow E, Schill RO, Harms-Ringdahl M, Rettberg P. 2008. Tardigrades survive exposure to space in low Earth orbit. Curr. Biol. 18:R729–31
    [Google Scholar]
  23. 23. 
    Arakawa K. 2020. Simultaneous metabarcoding of eukaryotes and prokaryotes to elucidate the community structures within tardigrade microhabitats. Diversity 12:110
    [Google Scholar]
  24. 24. 
    Degma P, Bertolani R, Guidetti R. 2020. Actual checklist of Tardigrada species (2009–2020, 38th Edition: 18-08-2020) Database, Inst. Res. Inf. Syst http://dx.doi.org/10.25431/11380_1178608
    [Crossref]
  25. 25. 
    Schill RO 2018. Water Bears: The Biology of Tardigrades Cham, Switz: Springer
  26. 26. 
    Gross V, Mayer G. 2015. Neural development in the tardigrade Hypsibius dujardini based on anti-acetylated α-tubulin immunolabeling. EvoDevo 6:12
    [Google Scholar]
  27. 27. 
    Gross V, Treffkorn S, Reichelt J, Epple L, Lüter C, Mayer G. 2019. Miniaturization of tardigrades (water bears): morphological and genomic perspectives. Arthropod Struct. Dev. 48:12–19
    [Google Scholar]
  28. 28. 
    Martin C, Gross V, Hering L, Tepper B, Jahn H et al. 2017. The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives. J. Comp. Physiol. A 203:565–90
    [Google Scholar]
  29. 29. 
    Nielsen C. 2012. Animal Evolution: Interrelationships of the Living Phyla Oxford, UK: Oxford Univ. Press
  30. 30. 
    Schmidt-Rhaesa A, Bartolomaeus T, Lemburg C, Ehlers U, Garey JR. 1998. The position of the Arthropoda in the phylogenetic system. J. Morphol. 238:263–85
    [Google Scholar]
  31. 31. 
    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. PNAS 108:15920–24
    [Google Scholar]
  32. 32. 
    Rota-Stabelli O, Kayal E, Gleeson D, Daub J, Boore JL et al. 2010. Ecdysozoan mitrogenomics: evidence for a common origin of the legged invertebrates, the Panarthropoda. Genome Biol. Evol. 2:425–40
    [Google Scholar]
  33. 33. 
    Telford MJ, Bourlat SJ, Economou A, Papillon D, Rota-Stabelli O. 2008. The evolution of the Ecdysozoa. Philos. Trans. R. Soc. Lond. B 363:1529–37
    [Google Scholar]
  34. 34. 
    Yoshida Y, Koutsovoulos G, Laetsch DR, Stevens L, Kumar S et al. 2017. Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus. . PLOS Biol 15:e2002266
    [Google Scholar]
  35. 35. 
    Fleming JF, Kristensen RM, Sørensen MV, Park TS, Arakawa K et al. 2018. Molecular palaeontology illuminates the evolution of ecdysozoan vision. Proc. Biol. Sci. 285:20182180
    [Google Scholar]
  36. 36. 
    Tunnacliffe A, Lapinski J. 2003. Resurrecting Van Leeuwenhoek's rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Philos. Trans. R. Soc. Lond. B 358:1755–71
    [Google Scholar]
  37. 37. 
    Greven H. 2018. From Johann August Ephraim Goeze to Ernst Marcus: a ramble through the history of early Tardigrade research (1773 until 1929). Water Bears: The Biology of Tardigrades RO Schill 1–55 Cham, Switz: Springer
    [Google Scholar]
  38. 38. 
    Madin KAC, Crowe JH. 1975. Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during dehydration. J. Exp. Zool. 193:335–42
    [Google Scholar]
  39. 39. 
    Crowe LM. 2002. Lessons from nature: the role of sugars in anhydrobiosis. Comp. Biochem. Physiol. A 131:505–13
    [Google Scholar]
  40. 40. 
    Crowe JH, Carpenter JF, Crowe LM. 1998. The role of vitrification in anhydrobiosis. Annu. Rev. Physiol. 60:73–103
    [Google Scholar]
  41. 41. 
    Kikawada T, Minakawa N, Watanabe M, Okuda T. 2005. Factors inducing successful anhydrobiosis in the African chironomid Polypedilum vanderplanki: significance of the larval tubular nest. Integr. Comp. Biol. 45:710–14
    [Google Scholar]
  42. 42. 
    Sakurai M, Furuki T, Akao K, Tanaka D, Nakahara Y et al. 2008. Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki. . PNAS 105:5093–98
    [Google Scholar]
  43. 43. 
    Erkut C, Penkov S, Khesbak H, Vorkel D, Verbavatz JM et al. 2011. Trehalose renders the dauer larva of Caenorhabditis elegans resistant to extreme desiccation. Curr. Biol. 21:1331–36
    [Google Scholar]
  44. 44. 
    Lapinski J, Tunnacliffe A. 2003. Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett 553:387–90
    [Google Scholar]
  45. 45. 
    Mali B, Grohme MA, Förster F, Dandekar T, Schnölzer M et al. 2010. Transcriptome survey of the anhydrobiotic tardigrade Milnesium tardigradum in comparison with Hypsibius dujardini and Richtersius coronifer. . BMC Genom 11:168
    [Google Scholar]
  46. 46. 
    Morek W, Suzuki AC, Schill RO, Georgiev D, Yankova M et al. 2019. Redescription of Milnesium alpigenum Ehrenberg, 1853 (Tardigrada: Apochela) and a description of Milnesium inceptum sp. Nov., a tardigrade laboratory model. Zootaxa 4586:35–64
    [Google Scholar]
  47. 47. 
    Wright JC. 1989. Desiccation tolerance and water-retentive mechanisms in tardigrades. J. Exp. Biol. 142:267–92
    [Google Scholar]
  48. 48. 
    Roszkowska M, Wojciechowska D, Kmita H, Cerbin S, Dziuba MK et al. 2021. Tips and tricks how to culture water bears: simple protocols for culturing eutardigrades (Tardigrada) under laboratory conditions. Eur. Zool. J. 88:449–65
    [Google Scholar]
  49. 49. 
    Altiero T, Rebecchi L. 2001. Rearing tardigrades: results and problems. Zool. Anz. J. Comp. Zool. 240:217–21
    [Google Scholar]
  50. 50. 
    Guidetti R, Cesari M, Bertolani R, Altiero T, Rebecchi L 2019. High diversity in species, reproductive modes and distribution within the Paramacrobiotus richtersi complex (Eutardigrada, Macrobiotidae). Zool. Lett. 5:1
    [Google Scholar]
  51. 51. 
    Suzuki AC. 2003. Life history of Milnesium tardigradum Doyère (Tardigrada) under a rearing environment. Zool. Sci. 20:49–57
    [Google Scholar]
  52. 52. 
    Gabriel WN, McNuff R, Patel SK, Gregory TR, Jeck WR et al. 2007. The tardigrade Hypsibius dujardini, a new model for studying the evolution of development. Dev. Biol. 312:545–59
    [Google Scholar]
  53. 53. 
    Gąsiorek P, Stec D, Morek W, Michalczyk Ł. 2018. An integrative redescription of Hypsibius dujardini (Doyère, 1840), the nominal taxon for Hypsibioidea (Tardigrada: Eutardigrada). Zootaxa 4415:45–75
    [Google Scholar]
  54. 54. 
    Koutsovoulos G, Kumar S, Laetsch DR, Stevens L, Daub J et al. 2016. No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini. . PNAS 113:5053–58
    [Google Scholar]
  55. 55. 
    Förster F, Beisser D, Grohme MA, Liang C, Mali B et al. 2012. Transcriptome analysis in tardigrade species reveals specific molecular pathways for stress adaptations. Bioinform. Biol. Insights 6:69–96
    [Google Scholar]
  56. 56. 
    Förster F, Liang C, Shkumatov A, Beisser D, Engelmann JC et al. 2009. Tardigrade workbench: comparing stress-related proteins, sequence-similar and functional protein clusters as well as RNA elements in tardigrades. BMC Genom 10:469
    [Google Scholar]
  57. 57. 
    Reuner A, Hengherr S, Mali B, Förster F, Arndt D et al. 2010. Stress response in tardigrades: differential gene expression of molecular chaperones. Cell Stress Chaperones 15:423–30
    [Google Scholar]
  58. 58. 
    Schokraie E, Hotz-Wagenblatt A, Warnken U, Mali B, Frohme M et al. 2010. Proteomic analysis of tardigrades: towards a better understanding of molecular mechanisms by anhydrobiotic organisms. PLOS ONE 5:e9502
    [Google Scholar]
  59. 59. 
    Wang C, Grohme MA, Mali B, Schill RO, Frohme M. 2014. Towards decrypting cryptobiosis—analyzing anhydrobiosis in the tardigrade Milnesium tardigradum using transcriptome sequencing. PLOS ONE 9:e92663
    [Google Scholar]
  60. 60. 
    Schill RO, Steinbrück GH, Köhler HR. 2004. Stress gene (hsp70) sequences and quantitative expression in Milnesium tardigradum (Tardigrada) during active and cryptobiotic stages. J. Exp. Biol. 207:1607–13
    [Google Scholar]
  61. 61. 
    Boothby TC, Tenlen JR, Smith FW, Wang JR, Patanella KA et al. 2015. Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. PNAS 112:15976–81
    [Google Scholar]
  62. 62. 
    Salzberg SL. 2017. Horizontal gene transfer is not a hallmark of the human genome. Genome Biol 18:85
    [Google Scholar]
  63. 63. 
    Steinegger M, Salzberg SL. 2020. Terminating contamination: large-scale search identifies more than 2,000,000 contaminated entries in GeneBank. Genome Biol 21:115
    [Google Scholar]
  64. 64. 
    Yoshida Y, Nowell RW, Arakawa K, Blaxter M 2019. Horizontal gene transfer in Metazoa: examples and methods. Horizontal Gene Transfer: Breaking Borders Between Living Kingdoms TG Villa, M Viñas 203–26 Cham, Switz: Springer Int. Publ.
    [Google Scholar]
  65. 65. 
    Laetsch D, Blaxter M 2017. BlobTools: interrogation of genome assemblies. F1000Research 6:1287
    [Google Scholar]
  66. 66. 
    Bemm F, Weiß CL, Schultz J, Förster F. 2016. Genome of a tardigrade: Horizontal gene transfer or bacterial contamination?. PNAS 113:E3054–56
    [Google Scholar]
  67. 67. 
    Delmont TO, Eren AM. 2016. Identifying contamination with advanced visualization and analysis practices: metagenomic approaches for eukaryotic genome assemblies. PeerJ 4:e1839
    [Google Scholar]
  68. 68. 
    Arakawa K, Yoshida Y, Tomita M 2016. Genome sequencing of a single tardigrade Hypsibius dujardini individual. Sci. Data 3:160063
    [Google Scholar]
  69. 69. 
    Yoshida Y, Konno S, Nishino R, Murai Y, Tomita M, Arakawa K. 2018. Ultralow input genome sequencing library preparation from a single tardigrade specimen. J. Vis. Exp. 137:e57615
    [Google Scholar]
  70. 70. 
    Arakawa K. 2016. No evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. PNAS 113:E3057
    [Google Scholar]
  71. 71. 
    Laumer CE. 2018. Inferring ancient relationships with genomic data: a commentary on current practices. Integr. Comp. Biol. 58:623–39
    [Google Scholar]
  72. 72. 
    Maderspacher F. 2016. Zoology: the walking heads. Curr. Biol. 26:R194–97
    [Google Scholar]
  73. 73. 
    Hashimoto T, Horikawa DD, Saito Y, Kuwahara H, Kozuka-Hata H et al. 2016. Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein. Nat. Commun. 7:12808
    [Google Scholar]
  74. 74. 
    Carrero D, Pérez-Silva JG, Quesada V, López-Otín C. 2019. Differential mechanisms of tolerance to extreme environmental conditions in tardigrades. Sci. Rep. 9:14938
    [Google Scholar]
  75. 75. 
    Mapalo MA, Arakawa K, Baker CM, Persson DK, Mirano-Bascos D, Giribet G 2020. The unique antimicrobial recognition and signaling pathways in tardigrades with a comparison across Ecdysozoa. G3 10:1137–48
    [Google Scholar]
  76. 76. 
    Giribet G, Edgecombe GD. 2017. Current understanding of Ecdysozoa and its internal phylogenetic relationships. Integr. Comp. Biol. 57:455–66
    [Google Scholar]
  77. 77. 
    Guijarro-Clarke C, Holland PWH, Paps J. 2020. Widespread patterns of gene loss in the evolution of the animal kingdom. Nat. Ecol. Evol. 4:519–23
    [Google Scholar]
  78. 78. 
    Laumer CE, Fernández R, Lemer S, Combosch D, Kocot KM et al. 2019. Revisiting metazoan phylogeny with genomic sampling of all phyla. Proc. Biol. Sci. 286:20190831
    [Google Scholar]
  79. 79. 
    Tenlen JR. 2018. Microinjection of dsRNA in tardigrades. Cold Spring Harb. Protoc. https://doi.org/10.1101/pdb.prot102368
    [Crossref] [Google Scholar]
  80. 80. 
    Tenlen JR, McCaskill S, Goldstein B. 2013. RNA interference can be used to disrupt gene function in tardigrades. Dev. Genes Evol. 223:171–81
    [Google Scholar]
  81. 81. 
    Kamilari M, Jørgensen A, Schiøtt M, Møbjerg N. 2019. Comparative transcriptomics suggest unique molecular adaptations within tardigrade lineages. BMC Genom 20:607
    [Google Scholar]
  82. 82. 
    Stec D, Krzywański Ł, Arakawa K, Michalczyk Ł 2020. A new redescription of Richtersius coronifer, supported by transcriptome, provides resources for describing concealed species diversity within the monotypic genus Richtersius (Eutardigrada). Zool. Lett. 6:2
    [Google Scholar]
  83. 83. 
    Murai Y, Yagi-Utsumi M, Fujiwara M, Tomita M, Kato K, Arakawa K. 2021. Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada. BMC Genom 22:813
    [Google Scholar]
  84. 84. 
    Hara Y, Shibahara R, Kondo K, Abe W, Kunieda T 2021. Parallel evolution of trehalose production machinery in anhydrobiotic animals via recurrent gene loss and horizontal transfer. Open Biol 11:200413
    [Google Scholar]
  85. 85. 
    Hoencamp C, Dudchenko O, Elbatsh AMO, Brahmachari S, Raaijmakers JA et al. 2021. 3D genomics across the tree of life reveals condensing II as a determinant of architecture type. Science 372:984–89
    [Google Scholar]
  86. 86. 
    Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA. 2008. The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6–24
    [Google Scholar]
  87. 87. 
    Goyal K, Walton LJ, Browne JA, Burnell AM, Tunnacliffe A. 2005. Molecular anhydrobiology: identifying molecules implicated in invertebrate anhydrobiosis. Integr. Comp. Biol. 45:702–9
    [Google Scholar]
  88. 88. 
    Hand SC, Menze MA, Toner M, Boswell L, Moore D. 2011. LEA proteins during water stress: not just for plants anymore. Annu. Rev. Physiol. 73:115–34
    [Google Scholar]
  89. 89. 
    Chakrabortee S, Boschetti C, Walton LJ, Sarkar S, Rubinsztein DC, Tunnacliffe A. 2007. Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. PNAS 104:18073–78
    [Google Scholar]
  90. 90. 
    Furuki T, Sakurai M. 2014. Group 3 LEA protein model peptides protect liposomes during desiccation. Biochim. Biophys. Acta 1838:2757–66
    [Google Scholar]
  91. 91. 
    Reyes JL, Rodrigo M-J, Colmenero-Flores JM, Gil J-V, Garay-Arroyo A et al. 2005. Hydrophilins from distant organisms can protect enzymatic activities from water limitation effects in vitro. Plant Cell Environ. 28:709–18
    [Google Scholar]
  92. 92. 
    Erkut C, Vasilj A, Boland S, Habermann B, Shevchenko A, Kurzchalia TV. 2013. Molecular strategies of the Caenorhabditis elegans Dauer larva to survive extreme desiccation. PLOS ONE 8:e82473
    [Google Scholar]
  93. 93. 
    Gal TZ, Glazer I, Koltai H. 2004. An LEA group 3 family member is involved in survival of C. elegans during exposure to stress. FEBS Lett 577:21–26
    [Google Scholar]
  94. 94. 
    Hunault G, Jaspard E 2010. LEAPdb: a database for the late embryogenesis abundant proteins. BMC Genom 11:221
    [Google Scholar]
  95. 95. 
    Campos F, Cuevas-Velazquez C, Fares MA, Reyes JL, Covarrubias AA 2013. Group 1 LEA proteins, an ancestral plant protein. Mol. Genet. Genom. 288:503–17
    [Google Scholar]
  96. 96. 
    Amara I, Odena A, Oliveira E, Moreno A, Masmoudi K et al. 2012. Insights into maize LEA proteins: from proteomics to functional approaches. Plant Cell Physiol 53:312–29
    [Google Scholar]
  97. 97. 
    Russouw PS, Farrant J, Brandt W, Maeder D, Lindsey GG 1995. Isolation and characterization of a heat-soluble protein from pea (Pisum sativum) embryos. Seed Sci. Res. 5:137–44
    [Google Scholar]
  98. 98. 
    Yamaguchi A, Tanaka S, Yamaguchi S, Kuwahara H, Takamura C et al. 2012. Two novel heat-soluble protein families abundantly expressed in an anhydrobiotic tardigrade. PLOS ONE 7:e44209
    [Google Scholar]
  99. 99. 
    Tanaka S, Tanaka J, Miwa Y, Horikawa DD, Katayama T et al. 2015. Novel mitochondria-targeted heat-soluble proteins identified in the anhydrobiotic tardigrade improve osmotic tolerance of human cells. PLOS ONE 10:e0118272
    [Google Scholar]
  100. 100. 
    Kondo K, Kubo T, Kunieda T. 2015. Suggested involvement of PP1/PP2A activity and de novo gene expression in anhydrobiotic survival in a tardigrade, Hypsibius dujardini, by chemical genetic approach. PLOS ONE 10:e0144803
    [Google Scholar]
  101. 101. 
    Boothby TC, Tapia H, Brozena AH, Piszkiewicz S, Smith AE et al. 2017. Tardigrades use intrinsically disordered proteins to survive desiccation. Mol. Cell 65:975–84
    [Google Scholar]
  102. 102. 
    Piszkiewicz S, Gunn KH, Warmuth O, Propst A, Mehta A et al. 2019. Protecting activity of desiccated enzymes. Protein Sci 28:941–51
    [Google Scholar]
  103. 103. 
    Esterly HJ, Crilly CJ, Piszkiewicz S, Shovlin DJ, Pielak GJ, Christian BE. 2020. Toxicity and immunogenicity of a tardigrade cytosolic abundant heat soluble protein in mice. Front. Pharmacol. 11:565969
    [Google Scholar]
  104. 104. 
    Fukuda Y, Miura Y, Mizohata E, Inoue T. 2017. Structural insights into a secretory abundant heat-soluble protein from an anhydrobiotic tardigrade, Ramazzottius varieornatus. . FEBS Lett 591:2458–69
    [Google Scholar]
  105. 105. 
    Levi AJ, Gatmaitan Z, Arias IM. 1969. Two hepatic cytoplasmic protein fractions, Y and Z, and their possible role in the hepatic uptake of bilirubin, sulfobromophthalein, and other anions. J. Clin. Investig. 48:2156–67
    [Google Scholar]
  106. 106. 
    Vincent SH, Muller-Eberhard U. 1985. A protein of the Z class of liver cytosolic proteins in the rat that preferentially binds heme. J. Biol. Chem. 260:14521–28
    [Google Scholar]
  107. 107. 
    Fukuda Y, Inoue T. 2018. Crystal structure of secretory abundant heat soluble protein 4 from one of the toughest “water bears” micro-animals Ramazzottius varieornatus. Protein Sci 27:993–99
    [Google Scholar]
  108. 108. 
    Yoshida Y, Sugiura K, Tomita M, Matsumoto M, Arakawa K 2019. Comparison of the transcriptomes of two tardigrades with different hatching coordination. BMC Dev. Biol. 19:24
    [Google Scholar]
  109. 109. 
    Wojciechowska D, Karachitos A, Rosźkowska M, Rzezniczak W, Sobkowiak R et al. 2021. Mitochondrial alternative oxidase contributes to successful tardigrade anhydrobiosis. Front. Zool. 18:15
    [Google Scholar]
  110. 110. 
    Richaud M, Le Goff E, Cazevielle C, Ono F, Mori Y et al. 2020. Ultrastructural analysis of the dehydrated tardigrade Hypsibius exemplaris unveils an anhydrobiotic-specific architecture. Sci. Rep 10:4324
    [Google Scholar]
  111. 111. 
    Yoshida Y, Satoh T, Ota C, Tanaka S, Horikawa DD et al. 2020. A novel Mn-dependent peroxidase contributes to tardigrade anhydrobiosis. bioRxiv 370643. https://doi.org/10.1101/2020.11.06.370643
    [Google Scholar]
  112. 112. 
    Kirke J, Jin XL, Zhang XH 2020. Expression of a tardigrade Dsup gene enhances genome protection in plants. Mol. Biotechnol. 62:563–71
    [Google Scholar]
  113. 113. 
    Chavez C, Cruz-Becerra G, Fei J, Kassavetis GA, Kadonaga, JT 2019. The tardigrade damage suppressor protein binds to nucleosomes and protects DNA from hydroxyl radicals. eLife 8:e47682
    [Google Scholar]
  114. 114. 
    Jönsson KI. 2019. Radiation tolerance in tardigrades: current knowledge and potential applications in medicine. Cancers 11:1333
    [Google Scholar]
  115. 115. 
    Yoshida Y, Horikawa DD, Sakashita T, Yokota Y, Kobayashi Y et al. 2021. RNA sequencing data for gamma radiation response in the extremotolerant tardigrade Ramazzottius varieornatus. . Data Brief 36:107111
    [Google Scholar]
  116. 116. 
    Carmona A, Deves G, Roudeau S, Cloetens P, Bohic S, Ortega R 2010. Manganese accumulates within Golgi apparatus in dopaminergic cells as revealed by synchrotron X-ray fluorescence nanoimaging. ACS Chem. Neurosci. 1:194–203
    [Google Scholar]
  117. 117. 
    Hirata Y. 2002. Manganese-induced apoptosis in PC12 cells. Neurotoxicol. Teratol. 24:639–53
    [Google Scholar]
  118. 118. 
    Alborzinia H, Ignashkova TI, Dejure FR, Gendarme M, Theobald J et al. 2018. Golgi stress mediates redox imbalance and ferroptosis in human cells. Commun. Biol. 1:210
    [Google Scholar]
  119. 119. 
    Jiang Z, Hu Z, Zeng L, Lu W, Zhang H et al. 2011. The role of the Golgi apparatus in oxidative stress: Is this organelle less significant than mitochondria? Free Radic. . Biol. Med. 50:907–17
    [Google Scholar]
  120. 120. 
    Yoshida H. 2009. ER stress response, peroxisome proliferation, mitochondrial unfolded protein response and Golgi stress response. IUBMB Life 61:871–79
    [Google Scholar]
  121. 121. 
    Horikawa DD, Arakawa K. 2015. Tardigrades—ultimate animals surviving extreme environments. SFCJ 15:246–60
    [Google Scholar]
  122. 122. 
    Alpert P. 2006. Constraints of tolerance: Why are desiccation-tolerant organisms so small or rare?. J. Exp. Biol. 209:1575–84
    [Google Scholar]
  123. 123. 
    Einset J, Collins AR. 2018. Genome size and sensitivity to DNA damage by X-rays: Plant comets tell the story. Mutagenesis 33:49–51
    [Google Scholar]
  124. 124. 
    Kondo K, Mori M, Tomita M, Arakawa K. 2019. AMPK activity is required for the induction of anhydrobiosis in a tardigrade Hypsibius exemplaris, and its potential up-regulator is PP2A. Genes Cells 24:768–80
    [Google Scholar]
  125. 125. 
    Hardie DG. 2014. AMP-activated protein kinase: maintaining energy homeostasis at the cellular and whole-body levels. Annu. Rev. Nutr. 34:31–55
    [Google Scholar]
  126. 126. 
    Kondo K, Mori M, Tomita M, Arakawa K. 2020. Pre-treatment with D942, a furancarboxylic acid derivative, increases desiccation tolerance in an anhydrobiotic tardigrade Hypsibius exemplaris. . FEBS Open Bio 10:1774–81
    [Google Scholar]
  127. 127. 
    Bemm F, Burleigh L, Förster F, Schmucki R, Ebeling M et al. 2017. Draft genome of the Eutardigrade Melnesium tardigradum sheds light on ecdysozoan evolution. bioRxiv. 122309. https://doi.org/10.1101/122309
    [Crossref]
  128. 128. 
    Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT. 2004. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337:635–45
    [Google Scholar]
  129. 129. 
    Brenner SE, Koehl P, Levitt M. 2000. The ASTRAL compendium for protein structure and sequence analysis. Nucleic Acids Res 28:254–56
    [Google Scholar]
  130. 130. 
    Chandonia J-M, Hon G, Walker NS, Lo Conte L, Koehl P et al. 2004. The ASTRAL Compendium in 2004. Nucleic Acids Res 32:D189–92
    [Google Scholar]
  131. 131. 
    Brown CJ, Johnson AK, Daughdrill GW 2010. Comparing models of evolution for ordered and disordered proteins. Mol. Biol. Evol. 27:609–21
    [Google Scholar]
  132. 132. 
    Radivojac P, Obradovic Z, Brown CJ, Dunker AK. 2002. Improving sequence alignments for intrinsically disordered proteins. Pac. Symp. Biocomput. 2002 589–600
    [Google Scholar]
  133. 133. 
    Trivedi R, Nagarajaram HA. 2019. Amino acid substitution scoring matrices specific to intrinsically disordered regions in proteins. Sci. Rep. 9:16380
    [Google Scholar]
  134. 134. 
    Tsuboyama K, Osaki T, Matsuura-Suzuki E, Kozuka-Hata H, Okada Y et al. 2020. A widespread family of heat-resistant obscure (Hero) proteins protect against protein instability and aggregation. PLOS Biol 18:e3000632
    [Google Scholar]
  135. 135. 
    Regier JC, Shultz JW, Kambic RE, Nelson DR. 2004. Robust support for tardigrade clades and their ages from three protein-coding nuclear genes. Invertebr. Biol. 123:93–100
    [Google Scholar]
  136. 136. 
    Sanders KL, Lee MSY. 2010. Arthropod molecular divergence times and the Cambrian origin of petastomids. Syst. Biodivers. 8:63–74
    [Google Scholar]
  137. 137. 
    Deng W, Henriet S, Chourrout D 2018. Prevalence of mutation-prone microhomology-mediated end joining in a chordate lacking the c-NHEJ DNA repair pathway. Curr. Biol. 28:3337–41
    [Google Scholar]
  138. 138. 
    Jönsson KI, Hygum TL, Andersen KN, Clausen LK, Møbjerg N. 2016. Tolerance to gamma radiation in the marine heterotardigrade, Echiniscoides sigismundi. PLOS ONE 11:e0168884
    [Google Scholar]
  139. 139. 
    Ingram J, Bartels D 1996. The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:377–403
    [Google Scholar]
  140. 140. 
    Oliver MJ, Farrant JM, Hilhorst HWM, Mundree S, Williams B, Bewley JD. 2020. Desiccation tolerance: avoiding cellular damage during drying and rehydration. Annu. Rev. Plant Biol. 71:435–60
    [Google Scholar]
  141. 141. 
    Hatos A, Hajdu-Soltész B, Monzon AM, Palopoli N, Álvarez L et al. 2020. DisProt: intrinsic protein disorder annotation in 2020. Nucleic Acids Res 48:D269–76
    [Google Scholar]
  142. 142. 
    Wright PE, Dyson HJ. 1999. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293:321–31
    [Google Scholar]
  143. 143. 
    Yagi-Utsumi M, Aoki K, Watanabe H, Song C, Nishimura S et al. 2021. Desiccation induced fibrous condensation of CAHS protein in an anhydrobiotic tardigrade. Sci. Rep 11:21328
    [Google Scholar]
  144. 144. 
    Arakawa K, Numata K. 2021. Reconsidering the “glass transition” hypothesis of intrinsically unstructured CAHS proteins in desiccation tolerance of tardigrades. Mol. Cell 81:409–10
    [Google Scholar]
  145. 145. 
    Shimizu T, Kanamori Y, Furuki T, Kikawada T, Okuda T et al. 2010. Desiccation-induced structuralization and glass formation of group 3 late embryogenesis abundant protein model peptides. Biochemistry 49:1093–104
    [Google Scholar]
  146. 146. 
    Wolkers WF, McCready S, Brandt WF, Lindsey GG, Hoekstra FA 2001. Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochim. Biophys. Acta 1544:196–206
    [Google Scholar]
  147. 147. 
    Belott C, Janis B, Menze MA 2020. Liquid-liquid phase separation promotes animal desiccation tolerance. PNAS 117:27676–84
    [Google Scholar]
  148. 148. 
    Dignon GL, Best RB, Mittal J. 2020. Biomolecular phase separation: from molecular driving forces to macroscopic properties. Annu. Rev. Phys. Chem. 71:53–75
    [Google Scholar]
  149. 149. 
    Alberti S, Gladfelter A, Mittag T. 2019. Considerations and challenges in studying liquid-liquid phase separation and biomolecular condensates. Cell 176:419–34
    [Google Scholar]
/content/journals/10.1146/annurev-animal-021419-083711
Loading
/content/journals/10.1146/annurev-animal-021419-083711
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error