Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-27T21:36:39.517Z Has data issue: false hasContentIssue false
  • English
  • Français

Cyanobacteria isolated from the high-intertidal zone: a model for studying the physiological prerequisites for survival in low Earth orbit

Published online by Cambridge University Press:  29 May 2013

Karen Olsson-Francis ,
Jonathan S. Watson  and
Charles S. Cockell
Karen Olsson-Francis*
Affiliation:
Centre for Earth, Planetary, Space and Astronomical Research, The Open University, Walton Hall, Milton Keynes MK7 6AA, UK
Jonathan S. Watson
Affiliation:
Centre for Earth, Planetary, Space and Astronomical Research, The Open University, Walton Hall, Milton Keynes MK7 6AA, UK
Charles S. Cockell
Affiliation:
Centre for Earth, Planetary, Space and Astronomical Research, The Open University, Walton Hall, Milton Keynes MK7 6AA, UK
*
e-mail: k.olsson-francis@open.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Cyanobacteria are capable of surviving the adverse conditions of low Earth orbit (LEO). We have previously demonstrated that Gloeocapsa strain OU_20, Chroococcidiopsis and akinetes of Anabaena cylindrica were able to survive 548 days of exposure to LEO. Motivated by an interest to understand how cyanobacteria can survive in LEO, we studied the strategies that Gloeocapsa strain OU_20 employs to survive in its natural environment, the upper region of the intertidal zone. Here, cyanobacteria are exposed to fluctuations in temperature, UV radiation, desiccation and salinity. We demonstrated that an increase in salinity from 6.5‰ (BG-11 medium) to 35.7‰ (similar to that of seawater), resulted in increased resistance to UV radiation (254 nm), vacuum (0.7×10−3±0.01 kPa) and cold temperatures (–20 °C). Concomitantly, biochemical analyses demonstrated that the amount of fatty acids and mycosporine-like amino acids (a UV absorbing pigment) were higher in the stressed cells. Morphological analysis demonstrated that the electron density and thickness of the mucilaginous sheath were also greater than in the control cells. Yet, the control and stressed cells both formed aggregates. As a result of studying the physiological adaptation of Gloeocapsa strain OU_20 in response to salinity, we postulate that survival in the high-intertidal zone and LEO involves a dense extracellular mucilaginous sheath and the formation of aggregates. We conclude that studying the physiological adaptation of cyanobacteria in the intertidal zone provides insight into understanding survival in LEO.

Keywords

Cyanobacteriasurvivaladverse conditions
Type
Research Article
Information
International Journal of Astrobiology , Volume 12 , Issue 4 , October 2013 , pp. 292 - 303
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abed, R.M.M., Kohls, K., Schoon, R., Scherf, A.K., Schacht, M., Palinska, K.A., Al-Hassani, H., Hamza, W., Rullkotter, J. & Golubic, S. (2008). Lipid biomarkers, pigments and cyanobacterial diversity of microbial mats across intertidal flats of the arid coast of the Arabian Gulf (Abu Dhabi, UAE). FEMS Microbiol. Ecol. 65, 449–462.CrossRefGoogle ScholarPubMed
Allakhverdiev, S., Kinoshita, M., Inaba, M., Suzuki, I. & Murata, N. (2001). Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. Plant Physiol. 125, 1842–1853.Google Scholar
Bauersachs, T., Compaore, J., Severin, I., Hopmans, E.C., Schouten, S., Stal, L.J. & Damste, J.S.S. (2011). Diazotrophic microbial community of coastal microbial mats of the southern North Sea. Geobiology 9, 349–359.Google Scholar
Billi, D., Friedmann, E.I., Hofer, K.G., Caiola, M.G. & Ocampo-Friedmann, R. (2000). Ionizing radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl. Environ. Microbiol. 66, 1489–1492.CrossRefGoogle ScholarPubMed
Billi, D., Viaggiu, E., Cockell, C.S., Rabbow, E., Horneck, G. & Onofri, S. (2011). Damage escape and repair in dried Chroococcidiopsis sp. from hot and cold deserts exposed to simulated space and martian conditions. Astrobiology 11, 65–73.CrossRefGoogle Scholar
Bligh, E.G. & Dyer, W.J. (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917.Google Scholar
Böhm, G.A., Pfleiderer, W., Böger, P. & Scherer, S. (1995). Structure of a novel oligosaccharide-mycosporine amino acid ultraviolet A/B sunscreen pigment from the terrestrial cyanobacterium Nostoc commune. J. Biol. Chem. 270, 8536–8539.Google Scholar
Cockell, C.S., Schuerger, A.C., Billi, D., Imre Friedmann, E. & Panitz, C. (2005). Effects of a simulated martian UV flux on the cyanobacterium Chroococcidiopsis sp. 029. Astrobiology 5, 127–140.CrossRefGoogle ScholarPubMed
Cockell, C.S., Mckay, C.P., Warren-Rhodes, K. & Horneck, G. (2008). Ultraviolet radiation-induced limitation to epilithic microbial growth in and deserts – dosimetric experiments in the hyperarid core of the Atacama Desert. J. Photochem. Photobiol. B: Biol. 90, 79–87.Google Scholar
Cockell, C.S., Rettberg, P., Rabbow, E. & Olsson-Francis, K. (2011). Exposure of phototrophs to 548 days in low Earth orbit: microbial selection pressures in outer space and on early earth. ISME J. 5, 1671–1682.Google Scholar
de la Torre, R. et al. (2010). Likelihood of interplanetary transfer of rock-inhabiting microbial communities: results from the space experiment Lithopanspermia. Icarus 208, 735–748.CrossRefGoogle Scholar
Dillon, J.G. & Castenholz, R.W. (1999). Sytonemin, a cyanobacterial sheath pigment, protects against UVC radiation: implications for early photosythetic life. J. Phycol. 35, 673–681.Google Scholar
Dillon, J.G., Tatsumi, C.M., Tandingan, P.G. & Castenholz, R.W. (2002). Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis sp.). Arch. Microbiol. 177, 322–331.Google Scholar
Ehling-Schulz, M. & Scherer, S. (1999). UV protection in cyanobacteria. Eur. J. Phycol. 34, 329–338.CrossRefGoogle Scholar
Fleming, E.D. & Castenholz, R.W. (2007). Effects of periodic desiccation on the synthesis of the UV-screening compound, scytonemin, in cyanobacteria. Environ. Microbiol. 9, 1448–1455.Google Scholar
Friedmann, E.I. (1980). Endolithic microbial life in hot and cold deserts. Orig. Life Evol. Biosph. 10, 223–235.Google Scholar
Gao, Q. & Garcia-Pichel, F. (2011). Microbial ultraviolet sunscreens. Nature Rev. Microbiol. 9, 1740–1526.CrossRefGoogle ScholarPubMed
Garbary, D.J. (2007). The margins of the sea: survival at the top of the tide. In Algae and Cyanobacteria in Extreme Environments, ed. Seckbachs, J.Springer, The Netherlands.Google Scholar
Garcia-Pichel, F. & Castenholz, R.W. (1991). Characterization and biological implications of scytonemin, a cyanobacterial sheath pigment. J. Phycol. 27, 395–409.CrossRefGoogle Scholar
Garcia-Pichel, F. & Castenholz, R.W. (1993). Occurrence of UV absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl. Environ. Microbiol. 59, 163–169.Google Scholar
Garcia-Pichel, F., Wingard, C.E. & Castenholz, R.W. (1993). Evidence regarding the UV sunscreen role of a mycosporine-like compound in the cyanobacterium Gloeocapsa sp. Appl. Environ. Microbiol. 59, 170–176.Google Scholar
Gombos, Z., Wada, H. & Murata, N. (1992). Unsaturation of fatty acids in membrane lipids enhances tolerance of the cyanobacterium Synechocystis PCC 6803 to low temperature photoinhibition. Proc. Natl. Acad. Sci. U.S.A. 89, 9959–9963.CrossRefGoogle Scholar
Griffiths, J. (2000). Engineering geomorphological mapping of the upper greensand escarpment near Honiton, Devon. Geosci. South-West England 10, 64–67.Google Scholar
Gupta, R., Bhadauriya, P., Chauhan, V.S. & Bisen, P.S. (2008). Impact of UV-B radiation on thylakoid membrane and fatty acid profile of Spirulina platensis. Curr. Microbiol. 56, 156–161.CrossRefGoogle ScholarPubMed
Kester, D.R., Duedall, I.W., Connors, D.N. & Pytkowic, R. (1967). Preparation of artificial seawater. Limnol. Oceanograph. 12, 176–179.Google Scholar
Knudson, G.B. (1986). Photoreactivation of ultraviolet irradiated, plasmid-bearing, and plasmid free strains of Bacillus Anthracis. Appl. Environ. Microbiol. 52, 444–449.Google Scholar
Mancinelli, R.L., White, M.R. & Rothschild, L.J. (1998). Biopan-survival I: exposure of the osmophiles Synechococcus sp. (Nageli) and Haloarcula sp. to the space environment. Adv. Space Res. 22, 327–334.CrossRefGoogle Scholar
Markwell, M.A.K., Haas, S.M., Bieber, L.L. & Tolbert, N.E. (1978). Modification of Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87, 206–210.Google Scholar
Morris, C.E., Monier, J.M. & Jacques, M.A. (1998). A technique to quantify the population size and composition of the biofilm component in communities of bacteria in the phyllosphere. Appl. Environ. Microbiol. 64, 4789–4795.Google Scholar
Olie, J.J. & Potts, M. (1986). Purification and biochemical analysis of the cytoplasmic membrane from the desiccation tolerant cyanobacterium Nostoc commune UTEX 584. Appl. Environ. Microbiol. 52, 706–710.Google Scholar
Olsson-Francis, K., de la Torre, R., Towner, M.C. & Cockell, C.S. (2009). Survival of akinetes (resting state cells of cyanobacteria) in low Earth orbit and simulated extraterrestrial conditions. Orig. Life Evol. Biosph. 39, 565–579.Google Scholar
Olsson-Francis, K., de la Torre, R. & Cockell, C.S. (2010). Isolation of novel extreme tolerant cyanobacteria from a rock-dwelling microbial community by using exposure to low Earth orbit. Appl. Environ. Microbiol. 76, 2115–2121.Google Scholar
Omelon, C.R. (2008). Endolithic microbial communities in polar desert habitats. Geomicrobiol. J. 25, 404–414.CrossRefGoogle Scholar
Oren, A. & Gunde-Cimerman, N. (2007). Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol. Lett. 269, 1–10.Google Scholar
Ozturk, S. & Aslim, B. (2010). Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environ. Sci. Pollut. Res. 17, 595–602.Google Scholar
Ozturk, S., Aslim, B. & Suludere, Z. (2009). Evaluation of chromium(VI) removal behaviour by two isolates of Synechocystis sp in terms of exopolysaccharide (EPS) production and monomer composition. Bioresource Technol. 100, 5588–5593.Google Scholar
Pierson, B.K., Mitchell, H.K. & Ruff-Roberts, A. (1993). Chloroflexus aurantiacus and ultraviolet radiation: implications for Archean shallow-water stromatolites. Orig. Life Evol. Biosph. 23, 243–260.CrossRefGoogle Scholar
Pirt, S.J. (1978). Principles of microbe and cell cultivation. In Principles of Microbe and Cell Cultivation. John Wiley and Sons, New York, p. 274.Google Scholar
Potts, M. (1999). Mechanisms of desiccation tolerance in cyanobacteria. Eur. J. Phycol. 34, 319–328.Google Scholar
Proteau, P.J., Gerwick, W.H., Garcia-Pichel, F. & Castenholz, R. (1993). The structure of scytonemin, an ultravioletn suncreen pigment from the sheaths of cyanobacteria. Experientia 49, 825–829.Google Scholar
Rothrock, M.J. & Garcia-Pichel, F. (2005). Microbial diversity of benthic mats along a tidal desiccation gradient. Environ. Microbiol. 7, 593–601.CrossRefGoogle ScholarPubMed
Sagan, C. (1973). Ultraviolet selection pressure on the earliest organisms. J. Theor. Biol. 39, 195–200.Google Scholar
Tamaru, Y., Takani, Y., Yoshida, T. & Sakamoto, T. (2005). Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Appl. Environ. Microbiol. 71, 7327–7333.Google Scholar
Tasaka, Y., Gombos, Z., Nishiyama, Y., Mohanty, P., Ohba, T., Okhi, K. & Murata, N. (1996). Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J. 15, 6416–6425.Google Scholar
Tauscher, C., Schuerger, A.C. & Nicholson, W.L. (2006). Survival and germinability of Bacillus subtilis spores exposed to simulated Mars solar radiation: implications for life detection and planetary protection. Astrobiology 6, 592–605.Google Scholar
Wierzchos, J., Ascaso, C. & McKay, C.P. (2006). Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama Desert. Astrobiology 6, 415–422.Google Scholar
Wright, D.J., Smith, S.C., Joardar, V., Scherer, S., Jervis, J., Warren, A., Helm, R.F. & Potts, M. (2005). UV irradiation and desiccation modulate the three-dimensional extracellular matrix of Nostoc commune (cyanobacteria). J. Biol. Chem. 280, 40271–40281.Google Scholar