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Restart capability of resting-states of Euglena gracilis after 9 months of dormancy: preparation for autonomous space flight experiments

Published online by Cambridge University Press:  29 May 2017

Sebastian M. Strauch Open the ORCID record for Sebastian M. Strauch [Opens in a new window] ,
Ina Becker ,
Laura Pölloth ,
Peter R. Richter ,
Ferdinand W. M. Haag Open the ORCID record for Ferdinand W. M. Haag [Opens in a new window] ,
Jens Hauslage  and
Michael Lebert
Sebastian M. Strauch*
Affiliation:
Department of Biology, Cell Biology Division, Gravitational Biology Group, Friedrich-Alexander-University Erlangen-Nürnberg, Staudtstr. 5, 91058 Erlangen, Germany
Ina Becker
Affiliation:
Department of Biology, Cell Biology Division, Gravitational Biology Group, Friedrich-Alexander-University Erlangen-Nürnberg, Staudtstr. 5, 91058 Erlangen, Germany
Laura Pölloth
Affiliation:
Department of Biology, Cell Biology Division, Gravitational Biology Group, Friedrich-Alexander-University Erlangen-Nürnberg, Staudtstr. 5, 91058 Erlangen, Germany
Peter R. Richter
Affiliation:
Department of Biology, Cell Biology Division, Gravitational Biology Group, Friedrich-Alexander-University Erlangen-Nürnberg, Staudtstr. 5, 91058 Erlangen, Germany
Ferdinand W. M. Haag
Affiliation:
Department of Biology, Cell Biology Division, Gravitational Biology Group, Friedrich-Alexander-University Erlangen-Nürnberg, Staudtstr. 5, 91058 Erlangen, Germany
Jens Hauslage
Affiliation:
Deutsches Zentrum für Luft- und Raumfahrt e.V. (DLR), Institut für Luft- und Raumfahrtmedizin, Biomedizinisches Wissenschafts-Unterstützungszentrum, Linder Höhe, 51147 Köln, Germany
Michael Lebert
Affiliation:
Department of Biology, Cell Biology Division, Gravitational Biology Group, Friedrich-Alexander-University Erlangen-Nürnberg, Staudtstr. 5, 91058 Erlangen, Germany
*
e-mail: [email protected]
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Abstract

Dormant states of organisms are easier to store than the living state because they tolerate larger variations in temperature, light, storage space etc., making them attractive for laboratory culture stocks and also for experiments under special circumstances, especially space flight experiments. Like several other organisms, Euglena gracilis is capable of forming desiccation tolerant resting states in order to survive periods of unfavourable environmental conditions. In earlier experiments it was found that dormant Euglena cells must not become completely desiccated. Some residual moisture is required to ensure recovery of the resting states. To analyse the water demand in recovery of Euglena resting states, cells were transferred to a defined amount of cotton wool (0.5 g). Subsequently different volumes of medium (1, 2, 3, 4, 5, 8, 10 and 20 ml) were added in order to supply humidity; a control was set up without additional liquid. Samples were sealed in transparent 50 ml falcon tubes and stored for 9 months under three different conditions:

  • • Constant low light conditions in a culture chamber at 20°C,

  • • In a black box, illuminated with short light emitting diode-light pulses provided by joule thieves and

  • • In darkness in a black box.

After 9 months, cells were transferred to fresh medium and cell number, photosynthetic efficiency and movement behavior was monitored over 3 weeks. It was found that cells recovered under all conditions except in the control, where no medium was supplied. Transcription levels of 21 genes were analysed with a Multiplex-polymerase chain reaction. One hour after rehydration five of these genes were found to be up-regulated: ubiquitin, heat shock proteins HSP70, HSP90, the calcium-sensor protein frequenin and a distinct protein kinase, which is involved in gravitaxis. The results indicate a transient general stress response of the cells.

Keywords

dormancyEuglena gracilisfrequeninHSP70HSP90Multiplex-PCRPKArecoveryresting statesubiquitin
Type
Research Article
Information
International Journal of Astrobiology , Volume 17 , Issue 2 , April 2018 , pp. 101 - 111
Copyright
Copyright © Cambridge University Press 2017 

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References

Allen, A.E., LaRoche, J., Maheswari, U., Lommer, M., Schauer, N., Lopez, P.J., Finazzi, G., Fernie, A.R. & Bowler, C. (2008). Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. PNAS 105(30), 10438–10443.Google Scholar
Allen, M.J. & Crane, A.E. (1976). Null potential voltammetry – an approach to the study of plant photosystems. Bioelectrochem. Bioenergetics 3, 84–91.Google Scholar
Alpert, P. (2006). Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J. Exp. Biol. 209(Pt. 9), 1575–1584.Google Scholar
Checcucci, A. (1976). Molecular sensory physiology of Euglena. Naturwissenschaften 63(9), 412–417.Google Scholar
Ciechanover, A. (1994). The ubiquitin-proteasome proteolytic pathway. Cell 79(1), 13–21.Google Scholar
Farrant, J.M., Cooper, K., Hilgart, A., Abdalla, K.O., Bentley, J., Thomson, J.A., Dace, H.J.W., Peton, N., Mundree, S.G. & Rafudeen, M.S. (2015). A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker). Planta 242(2), 407–426.Google Scholar
Finley, D., Özkaynak, E. & Varshavsky, A. (1987). The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses. Cell 48(6), 1035–1046.Google Scholar
Häder, D.-P., Richter, P. & Lebert, M. (2006). Signal transduction in gravisensing of flagellates. Signal Transduction 6(6), 422–431.CrossRefGoogle Scholar
Hill, D.R., Peat, A. & Potts, M. (1994) Biochemistry and structure of the glycan secreted by desiccation-tolerant Nostoc commune (cyanobacteria). Protoplasma 182, 126–148, from On CD1.Google Scholar
Hu, C., Zhang, D., Huang, Z. & Liu, Y. (2003) The vertical microdistribution of cyanobacteria and green algae within desert crusts and the development of the algal crusts. Plant Soil 257(1), 97–111.Google Scholar
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
Jayakumar, A., Hwang, S.J., Fabiny, J.M., Chinault, A.C. & Barnes, E. M. Jr. (1989) Isolation of an ammonium or methylammonium ion transport mutant of Escherichi coli and complementation of the cloned gene. J. Bacteriol. 171, 996–1001, from On CD1.Google Scholar
Kalaji, H.M. et al. (2014). Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth. Res 122(2), 121–158.Google Scholar
Kaprelyants, A.S., Gottschal, J.C. & Kell, D.B. (1993). Dormancy in non-sporulating bacteria. FEMS Microbiol. Lett. 104(3–4), 271–286.Google Scholar
Knight, H. (2005). Calcium signaling during abiotic stress in plants. Int. Rev. Cytol. 195, 269–324.Google Scholar
Kosová, K., Vítámvás, P., Prášil, I.T. & Renaut, J. (2011). Plant proteome changes under abiotic stress – Contribution of proteomics studies to understanding plant stress response. J. Proteomics 74(8), 1301–1322.Google Scholar
Lebert, M. & Häder, D.-P. (1999). Image analysis: a versatile tool for numerous applications. G.I.T. Imaging Microscopy 1, 5–6.Google Scholar
LeBlanc, J.C., Goncalves, E.R. & Mohn, W.W. (2008). Global response to desiccation stress in the soil actinomycete Rhodococcus jostii RHA1. Appl. Environ. Microbiol. 74(9), 2627–2636, viewed 28 November 2016.Google Scholar
Li, H., Rao, B., Wang, G., Shen, S., Li, D., Hu, C. & Liu, Y. (2014). Spatial heterogeneity of cyanobacteria-inoculated sand dunes significantly influences artificial biological soil crusts in the Hopq Desert (China). Environ. Earth Sci. 71(1), 245–253.Google Scholar
Malik, K.A. (1990). A simplified liquid-drying method for the preservation of microorganisms sensitive to freezing and freeze-drying. J. Microbiol. Methods 12(2), 125–132.Google Scholar
Malik, K.A. (1993). Preservation of unicellular gree algae by a liquid-drying method. J. Microbiol. Methods 18(1), 41–49, from http://www.sciencedirect.com/science/article/pii/016770129390070X.Google Scholar
Malik, K.A. (1995) A convenient method to maintain unicellular green algae for long times as standing liquid cultures. J. Microbiol. Methods 22, 221–227.Google Scholar
Nasir, A. et al. (2014). The influence of microgravity on Euglena gracilis as studied on Shenzhou 8. Plant Biol. (Stuttgart, Germany) 16 (Suppl. 1), 113–119.Google Scholar
O'Mahony, P.J. & Oliver, M.J. (1999). The involvement of ubiquitin in vegetative desiccation tolerance. Plant Mol. Biol. 41, 657–667, viewed 28 November 2016.Google Scholar
Poovaiah, B.W. & Reddy, A.S.N. (1990). Turnover of inositol phospholipids and calcium-dependent protein phosphorylation in signal transduction. Inositol Metab. Plants 9, 335–349.Google Scholar
Rao, B., Liu, Y., Wang, W., Hu, C., Dunhai, L. & Lan, S. (2009). Influence of dew on biomass and photosystem II activity of cyanobacterial crusts in the Hopq Desert, northwest China. Soil Biol. Biochem. 41(12), 2387–2393.Google Scholar
Reddy, A.S., Ali, G.S., Celesnik, H. & Day, I.S. (2012). Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23(6), 2010–2032, viewed 29 November 2016.Google Scholar
Richter, P.R., Schuster, M., Meyer, I., Lebert, M. & Häder, D.-P. (2006). Indications for acceleration-dependent changes of membrane potential in the flagellate Euglena gracilis . Protoplasma 229(2–4), 101–108.Google Scholar
Richter, P.R., Schuster, M., Lebert, M., Streb, C. & Häder, D.-P. (2007). Gravitaxis of Euglena gracilis depends only partially on passive buoyancy. Adv. Space Res. 39(7), 1218–1224.Google Scholar
Rio, D.C., Ares, M. Jr., Hannon, G.J. & Nilsen, T.W. (2010). RNA: A laboratory manual. Cold Spring Harbor Laboratory Press, New York.Google Scholar
Rojas-Triana, M., Bustos, R., Espinosa-Ruiz, A., Prat, S., Paz-Ares, J. & Rubio, V. (2013). Roles of Ubiquitination in the control of phosphate starvation responses in plants F. J. Integrative Plant Biol. 55(1), 40–53.Google Scholar
Rosowski, J.R. (1977). Development of mucilaginous surfaces in Euglenoids. II. Flagellated, creeping and palmelloid cells of Euglena. J. Phycol. 13(4), 323–328.CrossRefGoogle Scholar
Sandgren, C.D. (1988) Growth and reproductive strategies of freshwater phytoplankton. 1st edn. Cambridge University Press, Cambridge.Google Scholar
Scherer, S. & Potts, M. (1989). Novel water stress protein from a desiccation-tolerant cyanobacterium. Purification and partial characterization. J. Biol. Chem. 264, 12546–12553.Google Scholar
Starr, R.C. (1964) The culture collection of Algae at Indiana University. Am. J. Bot. 51(9), 1013–1044, from http://www.jstor.org/stable/2440254.Google Scholar
Tahedl, H. & Häder, D.P. (2001). Automated biomonitoring using real time movement analysis of Euglena gracilis . Ecotoxicol. Environ. Saf. 48(2), 161–169.Google Scholar
Tahedl, H.A. (2000) Entwicklung eines vollautomatischen Analysesystems für ökotoxikologische Untersuchungen. Doctoral Thesis, Ökophysiologie der Pflanzen, Friedrich-Alexander University, Erlangen-Nürnberg.Google Scholar
Takenaga, S., Kondo, T., Nazeri, S., Tamura, Y., Tokunaga, M., Tsuyama, S., Miyatake, K. & Nakano, Y. (1997). Accumulation of trehalose as a compatible solute under osmotic stress in Euglena gracilis Z. J. Eukaryot. Microbiol. 44(6), 609–613.Google Scholar
Timperio, A.M., Egidi, M.G. & Zolla, L. (2008). Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J. Proteomics 71(4), 391–411.Google Scholar
Toroser, D. & Huber, S.C. (1997). Protein phosphorylation as a mechanism for osmotic-stress activation of sucrose-phosphate synthase in spinach leaves. Plant Physiol. 114, 947–955, viewed 28 November 2016.Google Scholar
Vaishampayan, A., Sinha, R.P., Häder, D.-P., Dey, T., Gupta, A.K., Bhan, U. & Rao, A.L. (2001). Cyanobacterial biofertilizers in rice agriculture. Bot. Rev. 67, 453–516.Google Scholar
Vinocur, B. & Altman, A. (2005). Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr. Opin. Biotechnol. 16(2), 123–132.Google Scholar
Wang, W., Liu, Y., Li, D., Hu, C. & Rao, B. (2009). Feasibility of cyanobacterial inoculation for biological soil crusts formation in desert area. Soil Biol. Biochem. 41(5), 926–929.Google Scholar
Wang, W., Vinocur, B., Shoseyov, O. & Altman, A. (2004). Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9(5), 244–252.CrossRefGoogle ScholarPubMed
Xie, Z., Liu, Y., Hu, C., Chen, L. & Li, D. (2007). Relationships between the biomass of algal crusts in fields and their compressive strength. Soil Biol. Biochem. 39(2), 567–572.Google Scholar