Abstract
The invertebrate phylum Tardigrada has received much attention for containing species adapted to the most challenging environmental conditions where an ability to survive complete desiccation or freezing in a cryptobiotic state is necessary for persistence. Although research on tardigrades has a long history, the last decade has seen a dramatic increase in molecular biological (“omics”) studies, most of them with the aim to reveal the biochemical mechanisms behind desiccation tolerance of tardigrades. Several other aspects of tardigrade cell biology have been studied, and we review some of them, including karyology, embryology, the role of storage cells, and the question of whether tardigrades are eutelic animals. We also review some of the theories about how anhydrobiotic organisms are able to maintain cell integrity under dry conditions, and our current knowledge on the role of vitrification and DNA protection and repair. Many aspects of tardigrade stress tolerance have relevance for human medicine, and the first transfers of tardigrade stress genes to human cells have now appeared. We expect this field to develop rapidly in the coming years, as more genomic information becomes available. However, many basic cell biological aspects remain to be investigated, such as immunology, cell cycle kinetics, cell metabolism, and culturing of tardigrade cells. Such development will be necessary to allow tardigrades to move from a nonmodel organism position to a true model organism with interesting associations with the current models C. elegans and D. melanogaster.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Notes
- 1.
The species referred to Hypsibius dujardini in many studies reviewed in this chapter originates from the same strain/population collected from a pond in England, and has recently been described by Gąsiorek et al. (2018) as a new species, Hypsibius exemplaris, distinguished from the originally described species Hypsibius dujardini. In this chapter, we have chosen to consistently use the new name, H. exemplaris, although the publications referred to use H. dujardini.
References
Altiero T, Rebecchi L (2003) First evidence of achiasmatic male meiosis in the water bears Richtersius coronifer and Macrobiotus richtersi (Eutardigrada, Macrobiotidae). Hereditas 139:116–120
Arakawa K (2016) No evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc Natl Acad Sci USA 113(22):E3057
Arakawa K, Yoshida Y, Tomita M (2016) Genome sequencing of a single tardigrade Hypsibius dujardini individual. Sci Data 3:160063
Baumann H (1920) Mitteilungen zum feineren bau der tardigraden. Zool Anz 52:56–66
Beltrán-Pardo EA, Jönsson KI, Wojcik A, Haghdoost S, Bermúdez Cruz RM, Bernal Villegas JE (2013) Sequence analysis of the DNA-repair gene rad51 in the tardigrades Milnesium cf. tardigradum, Hypsibius dujardini and Macrobiotus cf. harmsworthi. J Limnol 72(s1):80–91
Bertolani R (1970a) Mitosi somatiche e costanza cellular numerica nei Tardigradi. Atti Accad Naz Lincei Rc Ser 8a 48:739–742
Bertolani R (1970b) Variabilità numerica cellulare in alcuni tessuti di Tardigradi. Atti Accad Naz Lincei Rc Ser 8a 49:442–446
Bertolani R (1994) Tardigrada. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates. Asexual propagation and reproductive strategies, vol VI. Oxford and IBH, New Delhi, pp 25–37
Bertolani R (2001) Evolution of the reproductive mechanisms in tardigrades – a review. Zool Anz 240:247–252
Bertolani R, Rebecchi L (2018) Cytologi and cytogenetics. In: Schill RO (ed) Water bears: the biology of tardigrades. Springer, New York, pp 145–161
Boothby TC, Tapia H, Brozena AH, Piszkiewicz S, Smith AE, Giovannini I, Rebecchi L, Pielak GJ, Koshland D, Goldstein B (2017) Tardigrades use intrinsically disordered proteins to survive desiccation. Mol Cell 65(6):975–984.e5
Campbell LI, Rota-Stabelli O, Edgecombe GD, Marchioro T, Longhorn SJ, Telford MJ 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 USA 108(38):15920–15924
Collares-Pereira MJ, Matos I, Morgado-Santos M, Coelho MM (2013) Natural pathways towards polyploidy in animals: the Squalius alburnoides fish complex as a model system to study genome size and genome reorganization in polyploids. Cytogenet Genome Res 140:97–116
Crowe JH (1975) The physiology of cryptobiosis in tardigrades. Mem Ist Idrobiol 32(Suppl):37–59
Crowe JH (2008) Trehalose as a “chemical chaperone”: fact and fantasy. Adv Exp Med Biol 594:143–158
Crowe JH (2015) Anhydrobiosis: an unsolved problem with applications in human welfare. In: Disalvo EA (ed) Membrane hydration: the role of water in the structure and function of biological membranes. Subcellular biochemistry 71. Springer, Basel, pp 263–280
Crowe JH, Madin KA (1974) Anhydrobiosis in tardigrades and nematodes. Trans Am Microsc Soc 93:513–524
Crowe JH, Carpenter IE, Crowe LM (1998a) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73–103
Crowe JH, Clegg JS, Crowe LM (1998b) Anhydrobiosis: the water replacement hypothesis. In: Reid DS (ed) The properties of water in foods. Chapman & Hall, New York, pp 440–455
Cunha A, Azevedo RBR, Emmons SW, Leroi AM (1999) Variable cell number in nematodes. Nature 402(6759):253
Czernekova M, Jönsson KI (2016) Experimentally induced repeated anhydrobiosis in the eutardigrade Richtersius coronifer. PLoS One 11(11):e0164062
Czernekova M, Jönsson KI, Chajec L, Student S, Poprawa I (2017) The structure of the desiccated Richtersius coronifer (Richters, 1903). Protoplasma 254(3):1367–1377
Czernekova M, Janelt K, Student S, Jönsson KI, Poprawa I (2018) A comparative ultrastructure study of storage cells in the eutardigrade Richtersius coronifer in the hydrated state and after desiccation and heating stress. PLoS One 13(8):e0201430
Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A (2003) Protein carbonylation in human diseases. Trends Mol Med 9:169–176
Daly MJ (2012) Death by protein damage in irradiated cells. DNA Repair 11(1):12–21
Degma P, Bertolani R, Guidetti R (2018) Actual checklist of Tardigrada species. Ver. 25: 10 05-2014, p 48. http://www.tardigrada.modena.unimo.it/miscellanea/Actual%20checklist%20of%20Tardigrada.pdf. Accessed 7 Nov 2018
Dewel RA, Nelson DR, Dewel WC (1993) Tardigrada. In: Harrison FW, Rice EM (eds) Microscopic anatomy of invertebrates, Onychophora, Chilopoda and Lesser Protostomata, vol 12. Wiley-Liss, New York, pp 143–183
Eibye-Jacobsen J (1997) New observations on the embryology of the Tardigrada. Zool Anz 235:201–216
Erkut C, Penkov S, Khesbak H, Vorkel D, Verbavatz JM, Fahmy K, Kurzchalia TV (2011) Trehalose renders the dauer larva of Caenorhabditis elegans resistant to extreme desiccation. Curr Biol 21:1331–1336
Fedorova M, Bollineni RC, Hoffmann R (2014) Protein carbonylation as a major hallmark of oxidative damage: update of analytical strategies. Mass Spectrom Rev 33:79–97
Förster F, Beisser D, Grohme MA, Liang C, Mali B, Siegl AM, Engelmann JC, Shkumatov AV, Schokraie E, Müller T, Schnölzer M, Schill RO, Frohme M, Dandekar T (2012) Transcriptome analysis in tardigrade species reveals specific molecular pathways for stress adaptations. Bioinform Biol Insights 6:69–96
França MB, Panek AD, Eleutherio ECA (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A 146:621–631
Gabriel WN, Goldstein B (2007) Segmental expression of Pax3/7 and engrailed homologs in tardigrade development. Dev Genes Evol 217:421–433
Gabriel WN, McNuff R, Patel SK, Gregory TR, Jeck WR, Jones CD, Goldstein B (2007) The tardigrade Hypsibius dujardini, a new model for studying the evolution of development. Dev Biol 312:545–559
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(1):45
Gilbert JJ (1983) Rotifera. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, Oogenesis, oviposition, and oosorption, vol I. Wiley, Chichester, pp 181–209
Gross V, Bährle R, Mayer G (2018) Detection of cell proliferation in adults of the water bear Hypsibius dujardini (Tardigrada) via incorporation of a thymidine analog. Tissue Cell 51:77–83
Hashimoto T, Kunieda T (2017) DNA protection protein, a novel mechanism of radiation tolerance: lessons from tardigrades. Life 7(2):26
Hashimoto T, Horikawa DD, Saito Y, Kuwahara H, Kozuka-Hata H, Shin-I T, Minakuchi Y, Ohishi K, Motoyama A, Aizu T, Enomoto A, Kondo K, Tanaka S, Hara Y, Koshikawa S, Sagara H, Miura T, Yokobori S-I, Miyagawa K, Suzuki Y, Kubo T, Oyama M, Kohara Y, Fujiyama A, Arakawa K, Katayama T, Toyoda A, Kunieda T (2016) Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein. Nat Commun 7:12808
Hejnol A, Schnabel R (2005) The eutardigrade Thulinia stephaniae has an indeterminate development and the potential to regulate early blastomere ablations. Development 132:1349–1361
Hengherr S, Heyer AG, Köhler HR, Schill RO (2008) Trehalose and anhydrobiosis in tardigrades – evidence for divergence in response to dehydration. FEBS J 275:281–288
Horikawa DD (2008) The Tardigrade Ramazzottius varieornatus as a model animal for astrobiological studies. Biol Sci Space 22(3):93–98
Hyra M, Rost-Roszkowska MM, Student S, Włodarczyk A, Deperas M, Janelt K, Poprawa I (2016) Body cavity cells of Parachela during their active life. Zool J Linnean Soc 178(4):878–887
Jönsson KI (2007) Tardigrades as a potential model organism in space research. Astrobiology 7:757–766
Jönsson KI, Persson O (2010) Trehalose in three species of desiccation tolerant tardigrades. Open Zool J 3:1–5
Jönsson KI, Rebecchi L (2002) Experimentally induced anhydrobiosis in the tardigrade Richtersius coronifer: phenotypic factors affecting survival. J Exp Zool 293:578–584
Jönsson KI, Schill RO (2007) Induction of Hsp70 by desiccation, ionising radiation and heat-shock in the eutardigrade Richtersius coronifer. Comp Biochem Physiol B Biochem Mol Biol 146:456–460
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–R731
Jönsson KI, Levine EB, Wojcik A, Haghdoost S, Harms-Ringdahl M (2018) Environmental adaptations – radiation tolerance. In: Schill RO (ed) Water bears: the biology of tardigrades. Springer, New York, pp 311–330
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(Suppl 1):77–83
Keilin D (1959) The problem of anabiosis or latent life: history and current concept. Proc R Soc Lond B 150:149–191
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(12):e0144803
Koutsovoulos G, Kumar S, Laetsch DR, Stevens L, Daub J, Conlon C, Maroon H, Thomas F, Aboobaker AA, Blaxter M (2016) No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini. Proc Natl Acad Sci USA 113(18):5053–5058
Krisko A, Leroya M, Radman M, Meselson M (2012) Extreme anti-oxidant protection against ionizing radiation in bdelloid rotifers. Proc Natl Acad Sci USA 109(7):2354–2357
Kuzmic M, Richaud M, Cuq P, Frelon S, Galas S (2018) Carbonylation accumulation of the Hypsibius exemplaris anhydrobiote reveals age-associated marks. PLoS One 13(12):e0208617
Leprince O, Buitink J (2010) Desiccation tolerance: from genomics to the field. Plant Sci 179:554–564
Levin DA (1983) Polyploidy and novelty in flowering plants. Am Nat 122(1):1–25
Madin KAC, Crowe J (1975) Anhydrobiosis in nematodes: carbohydrate and lipid metabolism during drying. J Exp Zool 193:335–342
Marcus E (1929) Tardigrada. In: Bronns HG (ed) Klassen und Ordungen des Tierreichs, vol 5, Section 4, Part 3. Akademische Verlagsgesellschaft, Leipzig, pp 1–608
Martini E (1923) Die zellkonstanz und ihre beziehungen zu anderen zoologischen vorwürfen. Z Anat Entwicklungsgesch 70(1–3):179–259
Mayer MP, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62(6):670–684
Møbjerg N, Halberg KA, Jørgensen A, Persson D, Bjørn M, Ramløv H, Kristensen RM (2011) Survival in extreme environments – on the current knowledge of adaptations in tardigrades. Acta Physiol 202:409–420
Nakhleh J, El Moussawi L, Osta MA (2017) The melanization response in insect immunity. Adv Insect Physiol 52:83–109
Neiman M, Beaton MJ, Hessen DO, Jeyasingh PD, Weider LJ (2017) Endopolyploidy as a potential driver of animal ecology and evolution. Biol Rev 92(1):234–247
Nelson DR, Guidetti R, Rebecchi L (2015) Phylum Tardigrada. In: Thorp J, Rogers DC (eds) Ecology and general biology: Thorp and Covich’s freshwater invertebrates. Academic, London, pp 347–380
Neumann S, Reuner A, Brümmer F, Schill RO (2009) DNA damage in storage cells of anhydrobiotic tardigrades. Comp Biochem Physiol A Mol Integr Physiol 153:425–429
Pandita TK, Higashikubo R, Hunt CR (2004) HSP70 and genomic stability. Cell Cycle 3(5):591–592
Parfrey LW, Lahr DJG, Katz LA (2008) The dynamic nature of eukaryotic genomes. Mol Biol Evol 25(4):787–794
Poprawa I, Hyra M, Rost-Roszkowska MM (2015) Germ cell cluster organization and oogenesis in the tardigrade Dactylobiotus parthenogeneticus Bertolani, 1982 (Eutardigrada, Murrayidae). Protoplasma 252:1019–1029
Rebecchi L (2013) Dry up and survive: the role of antioxidant defences in anhydrobiotic organisms. J Limnol 72(s1):62–72
Rebecchi L, Rossi V, Altiero T, Frigieri A, Bertolani R, Menozzi P (2003) Reproductive modes and genetic polymorphism in the tardigrade Richtersius coronifer (Eutardigrada, Macrobiotidae). Invertebr Biol 122(1):19–27
Rebecchi L, Cesari M, Altiero T, Frigieri A, Guidetti R (2009a) Survival and DNA degradation in anhydrobiotic tardigrades. J Exp Biol 212:4033–4039
Rebecchi L, Boschini D, Cesari M, Lencioni V, Bertolani R, Guidetti R (2009b) Stress response of a boreo-alpine species of tardigrade, Borealibius zetlandicus (Eutardigrada, Hypsibiidae). J Limnol 68(1):64–70
Reisz JA, Bansal N, Qian J, Zhao W, Furdui CM (2014) Effects of ionizing radiation on biological molecules – mechanisms of damage and emerging methods of detection. Antioxid Redox Signal 21(2):260–291
Reuner A, Hengherr S, Brümmer F, Schill RO (2010) Comparative studies on storage cells in tardigrades during starvation and anhydrobiosis. Curr Zool 56(2):259–263
Rizzo AM, Negroni M, Altiero T, Montorfano G, Corsetto P, Berselli P, Berra B, Guidetti R, Rebecchi L (2010) Antioxidant defences in hydrated and desiccated states of the tardigrade Paramacrobiotus richtersi. Comp Biochem Physiol B Biochem Mol Biol 156:115–121
Rosati F (1968) Ricerche di microscopia elettronica sui Tardigradi, 2. I globuli cavitari. Atti Accad Fisiocritici, Siena 17:1439–1452
Schill RO, Jönsson KI, Brümmer F, Pfannkuchen M (2011) Food of tardigrades: a case study to understand food choice, intake and digestion. J Zool Syst Evol Res 49(Suppl 1):66–70
Schoenfelder KP, Fox DT (2015) The expanding implications of polyploidy. J Cell Biol 209:485–491
Schokraie E, Warnken U, Hotz-Wagenblatt A, Grohme MA, Hengherr S, Förster F, Schill RO, Frohme M, Dandekar T, Schnölzer M (2012) Comparative proteome analysis of Milnesium tardigradum in early embryonic state versus adults in active and anhydrobiotic state. PLoS One 7:e45682
Smith FW, Boothby TC, Giovannini I, Rebecchi L, Jockusch EL, Goldstein B (2016) The compact body plan of tardigrades evolved by the loss of a large body region. Curr Biol 26:224–229
Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100(1):64–119
Szymańska B (1994) Interdependence between storage bodies and egg developmental stages in Macrobiotus richtersi Murray, 1911 (Tardigrada). Acta Biol Cracov 36:41–48
Tanaka S, Tanaka J, Miwa Y, Horikawa DD, Katayama T, Arakawa K, Toyoda A, Kubo T, Kunieda T (2015) Novel mitochondria-targeted heat-soluble proteins identified in the anhydrobiotic tardigrade improve osmotic tolerance of human cells. PLoS One 10(2):e0118272
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
Van Cleave HJ (1932) Eutely or cell constancy in its relation to body size. Q Rev Biol 7(1):59–67
Volkmann A, Greven H (1993) Ultrastructural localization of tyrosinase in the tardigrade cuticle. Tissue Cell 25:435–438
von Erlanger R (1895) Beiträge zur Morphologie der Tardigraden: I. Zur Embryologie eines Tardigraden: Macrobiotus macronyx Dujardin. Morph Jb 22:491–513
von Wenck W (1914) Entwicklungsgeschichtliche Untersuchungen an Tardigraden (Macrobiotus lacustris Duj.). Zool Jb Anat 37:465–514
Walsh EJ, Zhang L (1992) Polyploidy and body size variation in a natural population of the rotifer Euchlanis dilatata. J Evol Biol 5:345–353
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(3):e92663
Węglarska B (1975) Studies on the morphology of Macrobiotus richtersi Murray, 1911. Mem Ist Ital Idrobiol 32:445–464
Westh P, Ramløv H (1991) Trehalose accumulation in the tardigrade Adorybiotus coronifer during anhydrobiosis. J Exp Zool 258:303–311
Wright JC (2001) Cryptobiosis 300 years from van Leuwenhoek: what have we learned about tardigrades? Zool Anz 240:563–582
Yoshida Y, Koutsovoulos G, Laetsch DR, Stevens L, Kumar S, Horikawa DD, Ishino K, Komine S, Kunieda T, Tomita M, Blaxter M, Arakawa K (2017) Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus. PLoS Biol 15(7):e2002266
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Jönsson, K.I., Holm, I., Tassidis, H. (2019). Cell Biology of the Tardigrades: Current Knowledge and Perspectives. In: Tworzydlo, W., Bilinski, S. (eds) Evo-Devo: Non-model Species in Cell and Developmental Biology. Results and Problems in Cell Differentiation, vol 68. Springer, Cham. https://doi.org/10.1007/978-3-030-23459-1_10
Download citation
DOI: https://doi.org/10.1007/978-3-030-23459-1_10
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-23458-4
Online ISBN: 978-3-030-23459-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)