Anhydrobiosis without trehalose in bdelloid rotifers
Abstract
Eukaryotes able to withstand desiccation enter a state of suspended animation known as anhydrobiosis, which is thought to require accumulation of the non‐reducing disaccharides trehalose (animals, fungi) and sucrose (plants), acting as water replacement molecules and vitrifying agents. We now show that clonal populations of bdelloid rotifers Philodina roseola and Adineta vaga exhibit excellent desiccation tolerance, but that trehalose and other disaccharides are absent from carbohydrate extracts of dried animals. Furthermore, trehalose synthase genes (tps) were not found in rotifer genomes. This first observation of animal anhydrobiosis without trehalose challenges our current understanding of the phenomenon and calls for a re‐evaluation of existing models.
Number of times cited: 70
- Thomas C. Boothby and Gary J. Pielak, Intrinsically Disordered Proteins and Desiccation Tolerance: Elucidating Functional and Mechanistic Underpinnings of Anhydrobiosis, BioEssays, 39, 11, (2017).
- Thomas C. Boothby, Hugo Tapia, Alexandra H. Brozena, Samantha Piszkiewicz, Austin E. Smith, Ilaria Giovannini, Lorena Rebecchi, Gary J. Pielak, Doug Koshland and Bob Goldstein, Tardigrades Use Intrinsically Disordered Proteins to Survive Desiccation, Molecular Cell, 65, 6, (975), (2017).
- Yoichiro Sogame and Takahiro Kikawada, Current findings on the molecular mechanisms underlying anhydrobiosis in Polypedilum vanderplanki, Current Opinion in Insect Science, 19, (16), (2017).
- Cláudia Carolina Silva Evangelista, Giovanna Vieira Guidelli, Gustavo Borges, Thais Fenz Araujo, Tiago Alves Jorge de Souza, Ubiraci Pereira da Costa Neves, Alan Tunnacliffe and Tiago Campos Pereira, Multiple genes contribute to anhydrobiosis (tolerance to extreme desiccation) in the nematode Panagrolaimus superbus, Genetics and Molecular Biology, 40, 4, (790), (2017).
- Alina Ryabova, Kyosuke Mukae, Alexander Cherkasov, Richard Cornette, Elena Shagimardanova, Tetsuya Sakashita, Takashi Okuda, Takahiro Kikawada and Oleg Gusev, Genetic background of enhanced radioresistance in an anhydrobiotic insect: transcriptional response to ionizing radiations and desiccation, Extremophiles, 10.1007/s00792-016-0888-9, 21, 1, (109-120), (2016).
- Claudia Ricci, Bdelloid rotifers: ‘sleeping beauties’ and ‘evolutionary scandals’, but not only, Hydrobiologia, 796, 1, (277), (2017).
- Anna C. Seybold, David A. Wharton, Michael A. S. Thorne and Craig J. Marshall, Investigating trehalose synthesis genes after cold acclimation in the Antarctic nematode Panagrolaimus sp. DAW1 , Biology Open, 6, 12, (1953), (2017).
- Yoichiro SOGAME and Takahiro KIKAWADA, Molecular Mechanisms Underpinning Anhydrobiosis in the Sleeping Chironomid: What Do We Know So Far?, Kagaku To SeibutsuKAGAKU TO SEIBUTSU, 10.1271/kagakutoseibutsu.54.248, 54, 4, (248-253), (2016).
- Anirban Banerjee, Soumabrota Poddar, Subha Manna and Samar Kumar Saha, Mutualistic association of rotiferPhilodina roseolawith the branchiuran fish ectoparasiteArgulus bengalensisat its embryonic stage, Biology Letters, 12, 3, (20151043), (2016).
- L. Szydlowski, C. Boschetti, A. Crisp, E.G.G. Barbosa and A. Tunnacliffe, Multiple horizontally acquired genes from fungal and prokaryotic donors encode cellulolytic enzymes in the bdelloid rotifer Adineta ricciae, Gene, 566, 2, (125), (2015).
- Boris Hespeels, Xiang Li, Jean-François Flot, Lise-Marie Pigneur, Jeremy Malaisse, Corinne Da Silva, Karine Van Doninck and Richard A Wilson, Against All Odds: Trehalose-6-Phosphate Synthase and Trehalase Genes in the Bdelloid Rotifer Adineta vaga Were Acquired by Horizontal Gene Transfer and Are Upregulated during Desiccation, PLOS ONE, 10, 7, (e0131313), (2015).
- Hugo Tapia, Lindsey Young, Douglas Fox, Carolyn R. Bertozzi and Douglas Koshland, Increasing intracellular trehalose is sufficient to confer desiccation tolerance toSaccharomyces cerevisiae, Proceedings of the National Academy of Sciences, 112, 19, (6122), (2015).
- Trisha L. Bailey, Mian Wang, Jason Solocinski, Britto P. Nathan, Nilay Chakraborty and Michael A. Menze, Protective effects of osmolytes in cryopreserving adherent neuroblastoma (Neuro-2a) cells, Cryobiology, 10.1016/j.cryobiol.2015.08.015, 71, 3, (472-480), (2015).
- Koyuki Kondo, Takeo Kubo, Takekazu Kunieda and Houhui Xia, 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), (2015).
- Antoaneta V. Popova, Saskia Rausch, Michaela Hundertmark, Yves Gibon and Dirk K. Hincha, The intrinsically disordered protein LEA7 from Arabidopsis thaliana protects the isolated enzyme lactate dehydrogenase and enzymes in a soluble leaf proteome during freezing and drying, Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1854, 10, (1517), (2015).
- Jantina Toxopeus, Alden H. Warner and Thomas H. MacRae, Group 1 LEA proteins contribute to the desiccation and freeze tolerance of Artemia franciscana embryos during diapause, Cell Stress and Chaperones, 19, 6, (939), (2014).
- Chong Wang, Markus A. Grohme, Brahim Mali, Ralph O. Schill, Marcus Frohme and Cynthia Gibas, Towards Decrypting Cryptobiosis—Analyzing Anhydrobiosis in the Tardigrade Milnesium tardigradum Using Transcriptome Sequencing, PLoS ONE, 9, 3, (e92663), (2014).
- Leaf C. Boswell, Michael A. Menze and Steven C. Hand, Group 3 Late Embryogenesis Abundant Proteins from Embryos ofArtemia franciscana: Structural Properties and Protective Abilities during Desiccation, Physiological and Biochemical Zoology, 87, 5, (640), (2014).
- B. Hespeels, M. Knapen, D. Hanot‐Mambres, A.‐C. Heuskin, F. Pineux, S. Lucas, R. Koszul and K. Doninck, Gateway to genetic exchange? DNA double‐strand breaks in the bdelloid rotifer dineta vaga submitted to desiccation, Journal of Evolutionary Biology, 27, 7, (1334-1345), (2014).
- Elizabeth J. Walsh, Hilary A. Smith and Robert L. Wallace, Rotifers of temporary waters, International Review of Hydrobiology, 99, 1-2, (3-19), (2014).
- Chihiro Ito, Shin G. Goto and Hideharu Numata, Desiccation and Heat Tolerance of Eggs of the Asian Tadpole Shrimp, Triops granarius , Zoological Science, 10.2108/zsj.30.760, 30, 9, (760-766), (2013).
- Jacek Radzikowski, Resistance of dormant stages of planktonic invertebrates to adverse environmental conditions, Journal of Plankton Research, 35, 4, (707), (2013).
- M. Dmitryjuk, M. Dopieralska, E. Łopieńska-Biernat and R.J. Frączek, Purification and partial biochemical–genetic characterization of trehalose 6-phosphate synthase from muscles of adult female Ascaris suum, Journal of Helminthology, 87, 02, (212), (2013).
- Michele Cesari, Tiziana Altiero and Lorena Rebecchi, Identification of the trehalose-6-phosphate synthase (tps) gene in desiccation tolerant and intolerant tardigrades, Italian Journal of Zoology, 79, 4, (530), (2012).
- I. Julca, M. Alaminos, J. González-López and M. Manzanera, Xeroprotectants for the stabilization of biomaterials, Biotechnology Advances, 30, 6, (1641), (2012).
- Diego Fontaneto, Nils Bunnefeld and Martin Westberg, Long-Term Survival of Microscopic Animals Under Desiccation Is Not So Long, Astrobiology, 12, 9, (863), (2012).
- Chiara Boschetti, Adrian Carr, Alastair Crisp, Isobel Eyres, Yuan Wang-Koh, Esther Lubzens, Timothy G. Barraclough, Gos Micklem, Alan Tunnacliffe and Jianzhi Zhang, Biochemical Diversification through Foreign Gene Expression in Bdelloid Rotifers, PLoS Genetics, 8, 11, (e1003035), (2012).
- Brande L. Jones, Dana M. Schneider and Terry W. Snell, Thermostable proteins in the diapausing eggs of Brachionus manjavacas (Rotifera), Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 162, 3, (193), (2012).
- Richard Cornette and Takahiro Kikawada, The induction of anhydrobiosis in the sleeping chironomid: Current status of our knowledge, IUBMB Life, 63, 6, (419-429), (2011).
- Cihan Erkut, Sider Penkov, Hassan Khesbak, Daniela Vorkel, Jean-Marc Verbavatz, Karim Fahmy and Teymuras V. Kurzchalia, Trehalose Renders the Dauer Larva of Caenorhabditis elegans Resistant to Extreme Desiccation, Current Biology, 21, 15, (1331), (2011).
- Steffen Hengherr and Ralph O. Schill, Dormant stages in freshwater bryozoans—An adaptation to transcend environmental constraints, Journal of Insect Physiology, 57, 5, (595), (2011).
- David A. Wharton, Anhydrobiosis: The Model Worm as a Model?, Current Biology, 21, 15, (R578), (2011).
- , Literature Citations, Ecology and Classification of North American Freshwater Invertebrates, 10.1016/B978-0-12-374855-3.00027-3, (1022-1194), (2010).
- Alden H. Warner, Olga Miroshnychenko, Anna Kozarova, Panayiotis O. Vacratsis, Thomas H. MacRae, Jinnie Kim and James S. Clegg, Evidence for multiple group 1 late embryogenesis abundant proteins in encysted embryos of Artemia and their organelles, The Journal of Biochemistry, 10.1093/jb/mvq091, 148, 5, (581-592), (2010).
- E. A. Gladyshev and I. R. Arkhipova, Genome Structure of Bdelloid Rotifers: Shaped by Asexuality or Desiccation?, Journal of Heredity, 101, Supplement 1, (S85), (2010).
- E. J. Charlotta Nilsson, K. Ingemar Jönsson and Jan Pallon, Tolerance to proton irradiation in the eutardigradeRichtersius coronifer– a nuclear microprobe study, International Journal of Radiation Biology, 86, 5, (420), (2010).
- Oleg Gusev, Yuichi Nakahara, Veronica Vanyagina, Ludmila Malutina, Richard Cornette, Tetsuya Sakashita, Nobuyuki Hamada, Takahiro Kikawada, Yasuhiko Kobayashi, Takashi Okuda and Zhongjun Zhou, Anhydrobiosis-Associated Nuclear DNA Damage and Repair in the Sleeping Chironomid: Linkage with Radioresistance, PLoS ONE, 5, 11, (e14008), (2010).
- Kanako Mitsumasu, Yasushi Kanamori, Mika Fujita, Ken‐ichi Iwata, Daisuke Tanaka, Shingo Kikuta, Masahiko Watanabe, Richard Cornette, Takashi Okuda and Takahiro Kikawada, Enzymatic control of anhydrobiosis‐related accumulation of trehalose in the sleeping chironomid, Polypedilum vanderplanki, The FEBS Journal, 277, 20, (4215-4228), (2010).
- Ralph OLIVER Schill, Bärtierchen und die Kunst des Überlebens. Von Biodiversität bis Biotechnologie, Biologie in unserer Zeit, 40, 4, (254-259), (2010).
- Ralph O. Schill, Brahim Mali, Thomas Dandekar, Martina Schnölzer, Dirk Reuter and Marcus Frohme, Molecular mechanisms of tolerance in tardigrades: New perspectives for preservation and stabilization of biological material, Biotechnology Advances, 27, 4, (348), (2009).
- T.C. Pereira and I. Lopes-Cendes, Cryptic anhydrobiotic potential in man: Implications in medicine, Medical Hypotheses, 73, 4, (506), (2009).
- Marcelo Baeza, Patricio Retamales, Dionisia Sepúlveda, Patricia Lodato, Antonio Jiménez and Víctor Cifuentes, Isolation, characterization and long term preservation of mutant strains ofXanthophyllomyces dendrorhous, Journal of Basic Microbiology, 49, 2, (135), (2009).
- Michelle A. Sharon, Anna Kozarova, James S. Clegg, Panayiotis O. Vacratsis and Alden H. Warner, Characterization of a group 1 late embryogenesis abundant protein in encysted embryos of the brine shrimp Artemia franciscana, Biochemistry and Cell Biology, 87, 2, (415), (2009).
- C. Ricci and D. Fontaneto, The importance of being a bdelloid: Ecological and evolutionary consequences of dormancy, Italian Journal of Zoology, 76, 3, (240), (2009).
- Joe R. Clopton, From Observation to Theory with Resurrected Rotifers, The American Biology Teacher, 70, 3, (158), (2008).
- Steffen Hengherr, Arnd G. Heyer, Heinz-R. Köhler and Ralph O. Schill, Trehalose and anhydrobiosis in tardigrades - evidence for divergence in responses to dehydration, FEBS Journal, 275, 2, (281), (2008).
- E. A. Gladyshev, M. Meselson and I. R. Arkhipova, Massive Horizontal Gene Transfer in Bdelloid Rotifers, Science, 320, 5880, (1210), (2008).
- M. Sakurai, T. Furuki, K.-i. Akao, D. Tanaka, Y. Nakahara, T. Kikawada, M. Watanabe and T. Okuda, Vitrification is essential for anhydrobiosis in an African chironomid, Polypedilum vanderplanki, Proceedings of the National Academy of Sciences, 105, 13, (5093), (2008).
- Cristina S. Pereira and Philippe H. Hünenberger, Effect of Trehalose on a Phospholipid Membrane under Mechanical Stress, Biophysical Journal, 10.1529/biophysj.108.131656, 95, 8, (3525-3534), (2008).
- Claudia Ricci, Manuela Caprioli, Diego Fontaneto and Giulio Melone, Volume and morphology changes of a bdelloid rotifer species (Macrotrachela quadricornifera) during anhydrobiosis, Journal of Morphology, 269, 2, (233-239), (2007).
- T. Kikawada, A. Saito, Y. Kanamori, Y. Nakahara, K.-i. Iwata, D. Tanaka, M. Watanabe and T. Okuda, Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells, Proceedings of the National Academy of Sciences, 104, 28, (11585), (2007).
- S. Chakrabortee, C. Boschetti, L. J. Walton, S. Sarkar, D. C. Rubinsztein and A. Tunnacliffe, Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function, Proceedings of the National Academy of Sciences, 104, 46, (18073), (2007).
- Koushirou Suga, David Mark Welch, Yukari Tanaka, Yoshitaka Sakakura, Atsushi Hagiwara and Hans Ellegren, Analysis of Expressed Sequence Tags of the Cyclically Parthenogenetic Rotifer Brachionus plicatilis, PLoS ONE, 2, 8, (e671), (2007).
- M.B. França, A.D. Panek and E.C.A. Eleutherio, Oxidative stress and its effects during dehydration, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 146, 4, (621), (2007).
- Constança Cacela and Dirk K. Hincha, Low Amounts of Sucrose Are Sufficient to Depress the Phase Transition Temperature of Dry Phosphatidylcholine, but Not for Lyoprotection of Liposomes, Biophysical Journal, 90, 8, (2831), (2006).
- Masahiko Watanabe, Tetsuya Sakashita, Akihiko Fujita, Takahiro Kikawada, Yuichi Nakahara, Nobuyuki Hamada, Daiki D. Horikawa, Seiichi Wada, Tomoo Funayama, Yasuhiko Kobayashi and Takashi Okuda, Estimation of radiation tolerance to high LET heavy ions in an anhydrobiotic insect,Polypedilum vanderplanki, International Journal of Radiation Biology, 82, 12, (835), (2006).
- John Crowe, Nelly Tsvetkova, Ann Oliver, Chad Leidy, Josette Ricker and Lois Crowe, Stabilization of Liposomes by Freeze-Drying, Liposome Technology, Volume I, 10.1201/9780849397264.ch13, (261-284), (2009).
- Dirk K. Hincha, Antoaneta V. Popova and Constança Cacela, Chapter 6 Effects of Sugars on the Stability and Structure of Lipid Membranes During Drying, Advances in Planar Lipid Bilayers and Liposomes Volume 3, 10.1016/S1554-4516(05)03006-1, (189-217), (2006).
- Alan H. Haines, Non-equivalence of d- and l-trehalose in stabilising alkaline phosphatase against freeze-drying and thermal stress. Is chiral recognition involved?, Organic & Biomolecular Chemistry, 4, 4, (702), (2006).
- Zebo Huang and Alan Tunnacliffe, Cryptobiosis, Aging, and Cancer: Yin-Yang Balancing of Signaling Networks, Rejuvenation Research, 9, 2, (292), (2006).
- Masahiko Watanabe, Anhydrobiosis in invertebrates, Applied Entomology and Zoology, 10.1303/aez.2006.15, 41, 1, (15-31), (2006).
- Sooraj Ratnakumar and Alan Tunnacliffe, Intracellular trehalose is neither necessary nor sufficient for desiccation tolerance in yeast, FEMS Yeast Research, 6, 6, (902-913), (2006).
- Natalia N. Pouchkina-Stantcheva and Alan Tunnacliffe, Spliced Leader RNA–Mediated trans-Splicing in Phylum Rotifera, Molecular Biology and Evolution, 22, 6, (1482), (2005).
- K. Goyal, J.A. Browne, A.M. Burnell and A. Tunnacliffe, Dehydration-induced tps gene transcripts from an anhydrobiotic nematode contain novel spliced leaders and encode atypical GT-20 family proteins, Biochimie, 87, 6, (565), (2005).
- Julia Buitink and Olivier Leprince, Glass formation in plant anhydrobiotes: survival in the dry state, Cryobiology, 48, 3, (215), (2004).
- Manuela Caprioli, Agnete Krabbe Katholm, Giulio Melone, Hans Ramløv, Claudia Ricci and Nadia Santo, Trehalose in desiccated rotifers: a comparison between a bdelloid and a monogonont species, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 139, 4, (527), (2004).
- Masahiko WATANABE, Takahiro KIKAWADA, Akihiko FUJITA, Ewa FORCZEK, Taro ADATI and Takashi OKUDA, Physiological traits of invertebrates entering cryptobiosis in a post-embryonic stage, European Journal of Entomology, 101, 3, (439), (2004).
- Claudia Ricci, Manuela Caprioli and Nadia Santo, Feeding and anhydrobiosis in bdelloid rotifers: a preparatory study for an experiment aboard the International Space Station, Invertebrate Biology, 123, 4, (283-288), (2005).
- Zebo Huang and Alan Tunnacliffe, Response of human cells to desiccation: comparison with hyperosmotic stress response, The Journal of Physiology, 558, 1, (181-191), (2004).
- Brett Janis, Clinton Belott and Michael A. Menze, Role of Intrinsic Disorder in Animal Desiccation Tolerance, PROTEOMICS, 1800067, (2018).




