Protoplasma

, Volume 254, Issue 3, pp 1367–1377 | Cite as

The structure of the desiccated Richtersius coronifer (Richters, 1903)

  • Michaela Czerneková
  • K. Ingemar Jönsson
  • Lukasz Chajec
  • Sebastian Student
  • Izabela Poprawa
Original Article

Abstract

Tun formation is an essential morphological adaptation for entering the anhydrobiotic state in tardigrades, but its internal structure has rarely been investigated. We present the structure and ultrastructure of organs and cells in desiccated Richtersius coronifer by transmission and scanning electron microscopy, confocal microscopy, and histochemical methods. A 3D reconstruction of the body organization of the tun stage is also presented. The tun formation during anhydrobiosis of tardigrades is a process of anterior-posterior body contraction, which relocates some organs such as the pharyngeal bulb. The cuticle is composed of epicuticle, intracuticle and procuticle; flocculent coat; and trilaminate layer. Moulting does not seem to restrict the tun formation, as evidenced from tardigrade tuns that were in the process of moulting. The storage cells of desiccated specimens filled up the free inner space and surrounded internal organs, such as the ovary and digestive system, which were contracted. All cells (epidermal cells, storage cells, ovary cells, cells of the digestive system) underwent shrinkage, and their cytoplasm was electron dense. Lipids and polysaccharides dominated among reserve material of storage cells, while the amount of protein was small. The basic morphology of specific cell types and organelles did not differ between active and anhydrobiotic R. coronifer.

Keywords

Anhydrobiosis Cryptobiosis Tardigrades Tun Ultrastructure 

References

  1. Avdonina AM, Biserova NM, Bertolani R, Rebecchi L (2007) Ultrastructure of the digestive system of Ramazzottius tribulosus and Macrobiotus richtersi (Eutardigrada) in relation with diet. J Limnol 66:5–11CrossRefGoogle Scholar
  2. Baccetti B, Rosati F (1969) Electron microscopy on tardigrades. I. Connective tissue. J submicr Cytol 1:197–205Google Scholar
  3. Baccetti B, Rosati F (1971) Electron microscopy on tardigrades. III. The integument. J Ultrastruct Res 34:214–243CrossRefPubMedGoogle Scholar
  4. Baumann H (1922) Die anabiose der tardigraden. Zool Jahrb Abt Syst 45:501–556Google Scholar
  5. Baumann H (1961) Der Lebenslauf von Hypsibius (H.) convergens Urbanowicz (Tardigrada). Zool Anz 167:362–381Google Scholar
  6. Biserova NM, Mustafina AR (2015) Comparative midgut ultrastructure in three species of Tardigrada. Arthropoda Sel 24:373–385Google Scholar
  7. Crowe JH, Newell IM, Thomson WW (1971) Fine structure and chemical composition of the cuticle of the tardigrade Macrobiotus areolatus Murray. J Microsc 11:107–120Google Scholar
  8. Crowe JH, Madin KA (1974) Anhydrobiosis in tardigrades and nematodes. Trans Am Microsc Soc 93(4):513–524CrossRefGoogle Scholar
  9. Crowe JH, Madin KA (1975) Anhydrobiosis in nematodes: evaporative water loss and survival. J Exp Zool 193:323–334CrossRefGoogle Scholar
  10. Crowe JH (1975) The physiology of cryptobiosis in tardigrades. Mem Ist Ital Idrobiol 32:37–59Google Scholar
  11. Crowe JH, Crowe LM, Wolkers WF, Oliver AE, Ma X, Auh JH, Tang M, Zhu S, Norris J, Tablin F (2005) Stabilization of dry mammalian cells: lessons from nature. Integr Comp Biol 45:810–820CrossRefPubMedGoogle Scholar
  12. Dewel RA, Nelson DR, Dewel WC (1993) Tardigrada. Microscopic anatomy of invertebrates 12: Onychophora, Chilopoda, and Lesser Protostomata., pp 143–183Google Scholar
  13. Dykstra MJ (1992) Biological electron microscopy. Theory, techniques and troubleshooting. Plenum Press, New York & London, p 171Google Scholar
  14. Falk M, Lukášová E, Kozubek S (2008) Chromatin structure influence the sensitivity of DNA to γ-radiation. Biochim Biophys Acta 1783:2398–2414CrossRefPubMedGoogle Scholar
  15. Gaur HS, Perry RN (1991) The role of the moulted cuticles in the desiccation survival of adults of Rotylenchulus reniformis. Revue Nématol 14(4):491–496Google Scholar
  16. Greven H (1974) New results and considerations regarding the fine structure of the cuticle in Tardigrades. In Higgins: International Symposium on Tardigrades. Mem Istit Ital Idrobiol 32: 113–131Google Scholar
  17. Greven H, Dastych H, Kraus H (2005) Notes on the integument of the glacier-dwelling tardigrade Hypsibius klebelbergi Mihelčič, 1959 (Tardigrada). Mitt Hambg Zool Mus Inst 102:11–20Google Scholar
  18. Greven H (1976) Some ultrastructural observations on the midgut epithelium of Isohypsibius augusti (Murray, 1907) (Eutardigrada). Cell and Tissue Res 166:339–351CrossRefGoogle Scholar
  19. Greven H (1980) Die Bärtierchen. Die Neue Brehm-Bucherei, Vol. 537. Ziemsen VerlagGoogle Scholar
  20. Grigoryeva LA (2010) Morpho-functional changes in the midgut of Ixodid ticks (Acari: Ixodidae) during the life cycle. Entomol Rev 90(3):405–409CrossRefGoogle Scholar
  21. Grigorieva LA, Amosova LI (2004) Peculiarities of the peritrophic matrix in the midgut of tick females of the genus Ixodes (Acarina: Ixodidae). Parazitologia 38:3–11Google Scholar
  22. Guidetti R, Bertolani R, Rebecchi L (2000) Cuticle structure and systematics of the Macrobiotidae (Tardigrada; Eutardigrada). Acta Zool 81:27–36CrossRefGoogle Scholar
  23. Halberg KA, Jørgensen A, Møbjerg N (2013) Desiccation tolerance in the tardigrade Richtersius coronifer relies on muscle mediated structural reorganization. PLOS ONE 8(12):1–10CrossRefGoogle Scholar
  24. Hyra M, Poprawa I, Włodarczyk A, Student S, Sonakowska L, Kszuk-Jendrysik M, Rost-Roszkowska MM (2016a) Ultrastructural changes in the midgut epithelium of Hypsibius dujardini (Doyére, 1840) (Tardigrada, Eutardigrada, Hypsibiidae) in relation to oogenesis. Zool J Lin Soc. doi:10.1111/zoj.12467 Google Scholar
  25. Hyra M, Rost-Roszkowska MM, Student S, Włodarczyk A, Deperas M, Janelt K, Poprawa I (2016b) Body cavity cells of Parachela during their active life. Zool J Lin Soc. doi:10.1111/zoj.12463 Google Scholar
  26. Jönsson KI (2001) The nature of selection on anhydrobiotic capacity in tardigrades. Zool Anz 240:409–417CrossRefGoogle Scholar
  27. Jönsson KI, Rabbow E, Schill RO, Harms-Ringdahl RP (2008) Tardigrades survive exposure to space in low Earth orbit. Cur Biol 18(17):R729–R731CrossRefGoogle Scholar
  28. Keilin D (1959) The Leeuwenhoek lecture. The problem of anabiosis or latent life: history and current concept. Proc Roy Soc London B150:149–191CrossRefGoogle Scholar
  29. Kinchin IM (1993) An observation on body cavity cells of Ramazzottius (Hypsibiidae, Eutardigrada). Quekett J Microsc 37:52–55Google Scholar
  30. Kinchin IM (1994) The biology of tardigrades. Portland Press Ltd, PortlandGoogle Scholar
  31. 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 45:710–714CrossRefPubMedGoogle Scholar
  32. Litwin JA (1985) Light microscopic histochemistry on plastic sections. Program Histochem Cytochem 16:1–84Google Scholar
  33. Loeb MJ, Martin PAW, Narang N, Hakim RS, Goto S, Takeda M (2001) Control of life, death, and differentiation in cultured midgut cells of the lepidopteran, Heliothis virescens. Vitro Cel Dev Biol Anim 37(6):348–352Google Scholar
  34. Marotta R, Leasi F, Uggetti A, Ricci C, Melone G (2010) Dry and survive: morphological changes during anhydrobiosis in a bdelloid rotifer. J Struct Biol 171:11–17CrossRefPubMedGoogle Scholar
  35. Martin GG, Simcox R, Nguyen A, Chilingaryan A (2006) Peritrophic membrane of the penaeid shrimp Sicyonia ingentis: structure, formation, and permeability. Biol Bull 211:275–285CrossRefPubMedGoogle Scholar
  36. May RM (1949) Cytologie de la revivscence. Proc. 6th Int. Congr. Exp. Cytol. Suppl. 1 390Google Scholar
  37. Poprawa I (2005a) The ovary structure, previtellogenic and vitellogenic stages in parthenogenetic species Dactylobiotus dispar (Murray, 1097) (Tardigrada: Eutardigrada). Tissue Cell 37:385–392CrossRefPubMedGoogle Scholar
  38. Poprawa I (2005b) The structure and the formation of egg shells in parthenogenetic species Dactylobiotus dispar Murray, 1097 (Tardigrada: Eutardigrada). Folia Biol (Cracow) 53:173–177CrossRefGoogle Scholar
  39. Poprawa I (2006) Ultrastructural changes of the storage cells during oogenesis in Dactylobiotus dispar (Murray, 1907) (Tardigrada: Eutardigrada). Zool Pol 51(1–4):13–18Google Scholar
  40. Poprawa I, Hyra M, Kszuk-Jendrysik M, Rost-Roszkowska MM (2015a) Ultrastructural changes and programmed cell death of trophocytes in the gonad of Isohypsibius granulifer granulifer Thulin, 1928 (Tardigrada, Eutardigrada, Isohypsibiidae). Micron 70:26–33CrossRefPubMedGoogle Scholar
  41. Poprawa I, Hyra M, Rost-Roszkowska MM (2015b) Germ cell cluster organization and oogenesis in the tardigrade Dactylobiotus parthenogeneticus Bertolani, 1982 (Eutardigrada, Murrayidae). Protoplasma 252:1019–1029CrossRefPubMedGoogle Scholar
  42. Poprawa I, Schlechte-Welnicz W, Hyra M (2015c) Ovary organization and oogenesis in the tardigrade Macrobiotus polonicus Pilato, Michalczyk & Lisi, 2003 (Eutardigrada, Macrobiotidae): ultrastructural and histochemical analysis. Protoplasma 252:857–865CrossRefPubMedGoogle Scholar
  43. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58(4):755–805PubMedPubMedCentralGoogle Scholar
  44. Ramazotti G, Maucci W (1983) II Phylum Tardigrada. Terza edizione riveduta e corretta. Mem Insti Ital Idro Dott Marco de Marchi 41:1–1012Google Scholar
  45. Ramløv H, Westh P (1992) Survival of the cryptobiotic eutardigrade Adorybiotus coronifer during cooling to −196 °C: effect of cooling rate, trehalose level, and short-term acclimation. Cryobiology 29:125–130CrossRefGoogle Scholar
  46. Rebecchi L, Rossi V, Altiero T, Bertolani R, Menozzi P (2003) Reproductive modes and genetic polymorphism in the tardigrade Richtersius coronifer (Eutardigrada, Macrobiotidae). Invertebr Biol 122(1):19–27CrossRefGoogle Scholar
  47. Reuner A, Hengherr S, Brümmer F, Schill RO (2010) Comparative studies on storage cells in tardigrades during starvation and anhydrobiosis. Curr Zool 56(2):259–263Google Scholar
  48. Reynolds E (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208–212CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ricci C, Melone G, Santo N, Caprioli M (2003) Morphological response of a bdelloid rotifer to desiccation. J Morphol 257:246–253CrossRefPubMedGoogle Scholar
  50. Rosati F (1968) Ricerche di microscopia electronica sui Tardigradi II. I Globuli cavitari. Atti Accad Fisiocrit Siena 17:1439–1452Google Scholar
  51. Rost-Roszkowska MM, Undrul A (2008) Fine structure and differentiation of the midgut epithelium of Allacma fusca (Insecta: Collembola: Symphypleona). Zool Stud 47(2):200–206Google Scholar
  52. Rost-Roszkowska MM, Vilimowa J, Chajec Ł (2010) Fine structure of the midgut epithelium of Nicoletia phytophila Gervais, 1844 (Zygentoma: Nicoletiidae: Nicoletiinae) with special emphasis on its degeneration. Fol Biol 58(3–4):217–227CrossRefGoogle Scholar
  53. Rost-Roszkowska MM, Poprawa I, Kaczmarek Ł (2013a) Autophagy as the cell survival in response to a microsporidian infection of the midgut epithelium of Isohypsibius granulifer granulifer (Eutardigrada: Hypsibiidae). Acta Zool 94:273–279CrossRefGoogle Scholar
  54. Rost-Roszkowska MM, Poprawa I, Hyra M, Marek-Swedzioƚ M, Kaczmarek Ł (2013b) The fine structure of the midgut epithelium in Xerobiotus pseudohufelandi (Iharos, 1966) (Tardigrada, Eutardigrada, Macrobiotidae). J Limnol 72(s1):54–61Google Scholar
  55. Suzuki A (2006) Ovarian structure in Milnesium tardigradum (Tardigrada: Milnesiidae) during early vitellogenesis. Hydrobiologia 558:61–66CrossRefGoogle Scholar
  56. Szymańska B (1994) Interdependence between storage bodies and egg developmental stages in Macrobiotus richtersis Murray, 1911 (Tardigrada). Acta Biol Cracov ser Zool 36:41–50Google Scholar
  57. Szymańska B (1995) Encystment in the tardigrade Dactylobiotus dispar (MURRAY 1907) (Tardigrada: Eutardigrada). Zool Pol 40:91–102Google Scholar
  58. Terra WR (2001) The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch Insect Biochem Physiol 47:47–61CrossRefPubMedGoogle Scholar
  59. Walz B, Newell IM, Thomson WW (1971) Cuticle formation in the tardigrade Macrobiotus areolatus Murray. J Microsc 11:121–132Google Scholar
  60. Walz B (1979) The morphology of cells and cell organelles in the anhydrobiotic tardigrade, Macrobiotus hufelandi. Protoplasma 99:19–30CrossRefGoogle Scholar
  61. Walz B (1982) Molting in Tardigrada. A review including new results on cuticle formation in Macrobiotus hufelandi. Proceedings of the Third International Symposium on Tardigrada: 129–148Google Scholar
  62. Watanabe M (2006) Anhydrobiosis in invertebrates. Appl Entomol Zool 41(1):15–31CrossRefGoogle Scholar
  63. Węglarska B (1957) On the encystation in tardigrada. Zool Pol 4:315–325Google Scholar
  64. Węglarska B (1975) Studies on the morphology of Macrobiotus richtersi Murray, 1911. Mem Istit Ital Idrobiol 32:445–464Google Scholar
  65. Węglarska B (1979) Electron microscope study of previtellogenesis and vitellogenesis in Macrobiotus richtersi. Zesz Nauk Uniw Jagiellon Pr Zool J Murr (Eutardigrada) 25:169–189Google Scholar
  66. Węglarska B (1982) Ultrastructural study of the formation of egg envelope in Macrobiotus richtersi (Eutardigrada). In “Proceedings of the Third International Symposium on Tardigrada” Ed by DR Nelson, East Tennessee State University Press, 115–128Google Scholar
  67. Węglarska B (1987) Yolk formation in Isohypsibius (Eutardigrada). Zoomorphology 107:287–292CrossRefGoogle Scholar
  68. Westh P, Ramløv H (1991) Trehalose accumulation in tardigrade Adorybiotus coronifer during anhydrobiosis. J Exp Zool 258:303–311CrossRefGoogle Scholar
  69. Westh P, Kristensen RM (1992) Ice formation in the freeze-tolerant eutardigrades Adorybiotus coronifer and Amphibolus nebulosus studied by differential scanning calorimetry. Polar Biol 12:693–699CrossRefGoogle Scholar
  70. Wharton DA, Lemmon J (1998) Ultrastructural changes during desiccation of the anhydrobiotic nematode Dictylenchus dipsaci. Tissue Cell 30(3):312–313CrossRefPubMedGoogle Scholar
  71. Wright JC (1988) Structural correlates of permeability and Tun formation in tardigrade cuticle: an image analysis study. J Ultrastruct Mol Struct Res 101:23–39CrossRefGoogle Scholar
  72. Ząbczyk I (2000) Ultrastructural studies on the midgut of Dactylobiotus dispar (Murray, 1907) (Macrobiotidae, Eutardigrada). Acta Biol Cracov Ser Zool 42:9–16Google Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  • Michaela Czerneková
    • 1
    • 2
    • 3
  • K. Ingemar Jönsson
    • 1
  • Lukasz Chajec
    • 4
  • Sebastian Student
    • 5
  • Izabela Poprawa
    • 4
  1. 1.School of Education and EnvironmentKristianstad UniversityKristianstadSweden
  2. 2.Institute of PhysiologyAcademy of Sciences of the Czech RepublicPragueCzech Republic
  3. 3.Faculty of MedicineCharles UniversityPragueCzech Republic
  4. 4.Department of Animal Histology and EmbryologySilesian UniversityKatowicePoland
  5. 5.Institute of Automatic ControlSilesian University of TechnologyGliwicePoland

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