Free Access

Trehalose and anhydrobiosis in tardigrades – evidence for divergence in responses to dehydration

Steffen Hengherr

Animal Physiological Ecology, Zoological Institute, University of Tübingen, Germany

Department of Zoology, Biological Institute, Universität of Stuttgart, Germany

Search for more papers by this author
Arnd G. Heyer

Department of Botany, Biological Institute, Universität of Stuttgart, Germany

Search for more papers by this author
Heinz‐R. Köhler

Animal Physiological Ecology, Zoological Institute, University of Tübingen, Germany

Search for more papers by this author
Ralph O. Schill

Department of Zoology, Biological Institute, Universität of Stuttgart, Germany

Search for more papers by this author
First published: 07 December 2007
Cited by: 77
R. O. Schill, Department of Zoology, Biological Institute, Universität of Stuttgart, Pfaffenwaldring 57, D‐70569 Stuttgart, Germany
Fax: +49 711 685 6 5096
Tel: +49 711 685 6 9143
E‐mail: ralph.schill@bio.uni‐stuttgart.de

Abstract

To withstand desiccation, many invertebrates such as rotifers, nematodes and tardigrades enter a state known as anhydrobiosis, which is thought to require accumulation of compatible osmolytes, such as the non‐reducing disaccharide trehalose to protect against dehydration damage. The trehalose levels of eight tardigrade species comprising Heterotardigrada and Eutardigrada were observed in five different states of hydration and dehydration. Although many species accumulate trehalose during dehydration, the data revealed significant differences between the species. Although trehalose accumulation was found in species of the order Parachela (Eutardigrada), it was not possible to detect any trehalose in the species Milnesium tardigradum and no change in the trehalose level has been observed in any species of Heterotardigrada so far investigated. These results expand our current understanding of anhydrobiosis in tardigrades and, for the first time, demonstrate the accumulation of trehalose in developing tardigrade embryos, which have been shown to have a high level of desiccation tolerance.

Number of times cited: 77

  • , Structural insights into a secretory abundant heat‐soluble protein from an anhydrobiotic tardigrade, Ramazzottius varieornatus, FEBS Letters, 591, 16, (2458-2469), (2017).
  • , Tardigrades Use Intrinsically Disordered Proteins to Survive Desiccation, Molecular Cell, 65, 6, (975), (2017).
  • , 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).
  • , Intrinsically Disordered Proteins and Desiccation Tolerance: Elucidating Functional and Mechanistic Underpinnings of Anhydrobiosis, BioEssays, 39, 11, (2017).
  • , The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives, Journal of Comparative Physiology A, 203, 8, (565), (2017).
  • , Dry Preservation of Spermatozoa: Considerations for Different Species, Biopreservation and Biobanking, 15, 2, (158), (2017).
  • , High-throughput mass spectrometry analysis revealed a role for glucosamine in potentiating recovery following desiccation stress in Chironomus, Scientific Reports, 10.1038/s41598-017-03572-5, 7, 1, (2017).
  • , Can the tardigrade Hypsibius dujardini survive in the absence of the geomagnetic field?, PLOS ONE, 12, 9, (e0183380), (2017).
  • , How Do Animals Survive Extreme Temperature Amplitudes? The Role of Natural Deep Eutectic Solvents, ACS Sustainable Chemistry & Engineering, 5, 11, (9542), (2017).
  • , Compatible Solutes in the Akinetes of the Terrestrial Cyanobacterium <i>Nostoc</i> sp. HK-01 Contribute to Its Heat Tolerance, American Journal of Plant Sciences, 08, 11, (2695), (2017).
  • , First detailed observations on tardigrade mating behaviour and some aspects of the life history of Isohypsibius dastychi Pilato, Bertolani & Binda 1982 (Tardigrada, Isohypsibiidae), Zoological Journal of the Linnean Society, 178, 4, (856-862), (2016).
  • , Stress tolerance during diapause and quiescence of the brine shrimp, Artemia, Cell Stress and Chaperones, 10.1007/s12192-015-0635-7, 21, 1, (9-18), (2015).
  • , A combination of hydroxypropyl cellulose and trehalose as supplementation for vitrification of human oocytes: a retrospective cohort study, Journal of Assisted Reproduction and Genetics, 33, 3, (413), (2016).
  • , Liposomes with diverse compositions are protected during desiccation by LEA proteins from Artemia franciscana and trehalose, Biochimica et Biophysica Acta (BBA) - Biomembranes, 1858, 1, (104), (2016).
  • , 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).
  • , Responses of invertebrates to temperature and water stress: A polar perspective, Journal of Thermal Biology, 10.1016/j.jtherbio.2014.05.004, 54, (118-132), (2015).
  • , Novel Mitochondria-Targeted Heat-Soluble Proteins Identified in the Anhydrobiotic Tardigrade Improve Osmotic Tolerance of Human Cells, PLOS ONE, 10, 2, (e0118272), (2015).
  • , Trehalose hydrogels for stabilization of enzymes to heat, Polymer Chemistry, 10.1039/C5PY00121H, 6, 18, (3443-3448), (2015).
  • , Direct and Indirect Drivers of Moss Community Structure, Function, and Associated Microfauna Across a Successional Gradient, Ecosystems, 10.1007/s10021-014-9819-8, 18, 1, (154-169), (2014).
  • , The Heat Tolerance of Dry Colonies of a Terrestrial Cyanobacterium, Nostoc sp. HK-01, Biological Sciences in Space, 29, 0, (12), (2015).
  • , Dissolved Gases and Ice Fracturing During the Freezing of a Multicellular Organism: Lessons from Tardigrades, BioResearch Open Access, 4, 1, (209), (2015).
  • , Functional screening of a cDNA library from the desiccation-tolerant plant Selaginella lepidophylla in yeast mutants identifies trehalose biosynthesis genes of plant and microbial origin, Journal of Plant Research, 10.1007/s10265-014-0663-x, 127, 6, (803-813), (2014).
  • , 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).
  • , Disaccharides Impact the Lateral Organization of Lipid Membranes, Journal of the American Chemical Society, 136, 46, (16167), (2014).
  • , Effect of the cosolutes trehalose and methanol on the equilibrium and phase-transition properties of glycerol-monopalmitate lipid bilayers investigated using molecular dynamics simulations, European Biophysics Journal, 10.1007/s00249-014-0982-9, 43, 10-11, (517-544), (2014).
  • , Molecular Analysis of the Cold Tolerant Antarctic Nematode, Panagrolaimus davidi, PLoS ONE, 9, 8, (e104526), (2014).
  • , Towards Decrypting Cryptobiosis—Analyzing Anhydrobiosis in the Tardigrade Milnesium tardigradum Using Transcriptome Sequencing, PLoS ONE, 9, 3, (e92663), (2014).
  • , Desiccation Tolerance in the Tardigrade Richtersius coronifer Relies on Muscle Mediated Structural Reorganization, PLoS ONE, 8, 12, (e85091), (2013).
  • , 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).
  • , Uses of Phage Display in Agriculture: A Review of Food-Related Protein-Protein Interactions Discovered by Biopanning over Diverse Baits, Computational and Mathematical Methods in Medicine, 2013, (1), (2013).
  • , Phase-transition properties of glycerol-monopalmitate lipid bilayers investigated by molecular dynamics simulation: influence of the system size and force-field parameters, Molecular Simulation, 10.1080/08927022.2012.755526, 39, 7, (563-583), (2013).
  • , Transcriptome Analysis in Tardigrade Species Reveals Specific Molecular Pathways for Stress Adaptations, Bioinformatics and Biology Insights, 6, (BBI.S9150), (2012).
  • , Trehalose Glycopolymers for Stabilization of Protein Conjugates to Environmental Stressors, Journal of the American Chemical Society, 134, 20, (8474), (2012).
  • , Identification of the trehalose-6-phosphate synthase (tps) gene in desiccation tolerant and intolerant tardigrades, Italian Journal of Zoology, 79, 4, (530), (2012).
  • , Trehalose as an indicator of desiccation stress in Drosophila melanogaster larvae: A potential marker of anhydrobiosis, Biochemical and Biophysical Research Communications, 419, 4, (638), (2012).
  • , Thermostable proteins in the diapausing eggs of Brachionus manjavacas (Rotifera), Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 162, 3, (193), (2012).
  • , Integrated pathway modules using time-course metabolic profiles and EST data from Milnesium tardigradum, BMC Systems Biology, 6, 1, (72), (2012).
  • , Inelastic neutron scattering study of dynamical properties of bioprotectant solutions against temperature, Journal of Non-Crystalline Solids, 358, 18-19, (2635), (2012).
  • , Late embryogenesis abundant proteins protect human hepatoma cells during acute desiccation, Proceedings of the National Academy of Sciences, 109, 51, (20859), (2012).
  • , Xeroprotectants for the stabilization of biomaterials, Biotechnology Advances, 30, 6, (1641), (2012).
  • , Survival in extreme environments – on the current knowledge of adaptations in tardigrades, Acta Physiologica, 202, 3, (409-420), (2011).
  • , The induction of anhydrobiosis in the sleeping chironomid: Current status of our knowledge, IUBMB Life, 63, 6, (419-429), (2011).
  • , Resistance of the anhydrobiotic eutardigrade Paramacrobiotus richtersi to space flight (LIFE–TARSE mission on FOTON‐M3), Journal of Zoological Systematics and Evolutionary Research, 49, s1, (98-103), (2011).
  • , Bioinformatics identifies tardigrade molecular adaptations including the DNA‐j family and first steps towards dynamical modelling, Journal of Zoological Systematics and Evolutionary Research, 49, s1, (120-126), (2011).
  • , Ultraviolet radiation tolerance in hydrated and desiccated eutardigrades, Journal of Zoological Systematics and Evolutionary Research, 49, s1, (104-110), (2011).
  • , Solvent Interactions with Proteins and Other Macromolecules, Amino Acids, Peptides and Proteins in Organic Chemistry, (277-360), (2011).
  • , LEA Proteins During Water Stress: Not Just for Plants Anymore, Annual Review of Physiology, 73, 1, (115), (2011).
  • , Long-Term Cold Acclimation Extends Survival Time at 0°C and Modifies the Metabolomic Profiles of the Larvae of the Fruit Fly Drosophila melanogaster, PLoS ONE, 6, 9, (e25025), (2011).
  • , Artemin as an Efficient Molecular Chaperone, The Protein Journal, 30, 8, (549), (2011).
  • , Mechanisms associated with cellular desiccation tolerance of Artemia encysted embryos from locations around the world, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 160, 2, (137), (2011).
  • , Dormant stages in freshwater bryozoans—An adaptation to transcend environmental constraints, Journal of Insect Physiology, 57, 5, (595), (2011).
  • , Extreme stress tolerance in tardigrades: surviving space conditions in low earth orbit, Journal of Zoological Systematics and Evolutionary Research, 49, s1, (90-97), (2011).
  • , Life‐history traits of the bisexual tardigrades Paramacrobiotus tonollii and Macrobiotus sapiens, Journal of Zoological Systematics and Evolutionary Research, 49, s1, (58-61), (2011).
  • , On dormancy strategies in tardigrades, Journal of Insect Physiology, 57, 5, (567), (2011).
  • , Trehalose Has a Protective Effect on Human Brain-Type Creatine Kinase During Thermal Denaturation, Applied Biochemistry and Biotechnology, 165, 2, (476), (2011).
  • , Enzymatic control of anhydrobiosis‐related accumulation of trehalose in the sleeping chironomid, Polypedilum vanderplanki, The FEBS Journal, 277, 20, (4215-4228), (2010).
  • , Bärtierchen und die Kunst des Überlebens. Von Biodiversität bis Biotechnologie, Biologie in unserer Zeit, 40, 4, (254-259), (2010).
  • , Stress response in tardigrades: differential gene expression of molecular chaperones, Cell Stress and Chaperones, 10.1007/s12192-009-0158-1, 15, 4, (423-430), (2009).
  • , 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).
  • , Antioxidant defences in hydrated and desiccated states of the tardigrade Paramacrobiotus richtersi, Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 156, 2, (115), (2010).
  • , Literature Citations, Ecology and Classification of North American Freshwater Invertebrates, 10.1016/B978-0-12-374855-3.00027-3, (1022-1194), (2010).
  • , Using compensatory base change analysis of internal transcribed spacer 2 secondary structures to identify three new species in Paramacrobiotus (Tardigrada), Organisms Diversity & Evolution, 10, 4, (287), (2010).
  • , Tolerance to proton irradiation in the eutardigradeRichtersius coronifer– a nuclear microprobe study, International Journal of Radiation Biology, 86, 5, (420), (2010).
  • , 32. Sub-Kelvin resistance, impact resistance, and neutron dose of the tardigrade: Ramazzottius varieoranatus, Cryobiology, 61, 3, (371), (2010).
  • , Anhydrobiosis-Associated Nuclear DNA Damage and Repair in the Sleeping Chironomid: Linkage with Radioresistance, PLoS ONE, 5, 11, (e14008), (2010).
  • , Ice crystallization and freeze tolerance in embryonic stages of the tardigrade Milnesium tardigradum, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 156, 1, (151), (2010).
  • , Interaction of the disaccharides trehalose and gentiobiose with lipid bilayers: A comparative molecular dynamics study, Journal of Molecular Graphics and Modelling, 10.1016/j.jmgm.2010.09.013, 29, 3, (331-346), (2010).
  • , Identification of Anhydrobiosis-related Genes from an Expressed Sequence Tag Database in the Cryptobiotic MidgePolypedilum vanderplanki(Diptera; Chironomidae), Journal of Biological Chemistry, 285, 46, (35889), (2010).
  • , High Hydrostatic Pressure Tolerance of Four Different Anhydrobiotic Animal Species, Zoological Science, 26, 3, (238), (2009).
  • , Molecular mechanisms of tolerance in tardigrades: New perspectives for preservation and stabilization of biological material, Biotechnology Advances, 27, 4, (348), (2009).
  • , DNA damage in storage cells of anhydrobiotic tardigrades, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 153, 4, (425), (2009).
  • , Desiccation tolerance in embryonic stages of the tardigrade, Journal of Zoology, 276, 1, (103-107), (2008).
  • , Anhydrobiosis in tardigrades and its effects on longevity traits, Journal of Zoology, 275, 3, (216-220), (2008).
  • , The Tardigrade Ramazzottius varieornatus as a Model Animal for Astrobiological Studies, Biological Sciences in Space, 22, 3, (93), (2008).
  • , Tardigrada, eLS, (2012).
  • , Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus, PLOS Biology, 10.1371/journal.pbio.2002266, 15, 7, (e2002266), (2017).
  • , Role of Intrinsic Disorder in Animal Desiccation Tolerance, PROTEOMICS, 1800067, (2018).