Abstract
Desert cyanobacteria of the genus Chroococcidiopsis are extremely resistant to desiccation and ionizing radiation. When an endolithic strain was exposed to UVC radiation cell lysis, genome damage, photosynthetic pigment bleaching and reduced photochemical performance occurred. Nevertheless, survivors were scored after UVC doses as high as 13 kJ/m2 and their endurance ascribed to multicellular aggregates enveloped in thick envelopes, so that attenuated UVC radiation reached the inner cells. In addition, the accumulation of carotenoids contributed to UVC resistance by providing protection against oxidative stress. Finally, in survivors repair mechanisms were responsible for the recovery of the induced damage to genome and photosynthetic apparatus.
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Abbreviations
- DAPI:
-
4′,6-Diamidino-2-phenylindole
- FITC:
-
Fluorescein isothiocyanate
- HIP1:
-
Highly iterated palindromic sequences, type1
- RAPD:
-
Random amplification of polymorphic DNA
- qPCR:
-
Quantitative polymerase chain reaction
References
Adhikary SP, Sahu JK (1998) UV protecting pigments of the terrestrial cyanobacterium Tolypothrix byssoidea. J Plant Physiol 153:770–773
Amorim JH, Vidal RO, Lacerda-Junior GV, Dias JC, Brendel M, Rezende RP, Cascardo JC (2012) A simple boiling-based DNA extraction for RAPD profiling of landfarm soil to provide representative metagenomic content. Genet Mol Res 11:182–189
Antony CP, Cockell CS, Shouche YS (2012) Life in (and on) the rocks. J Biosci 37:3–11
Aráoz R, Häder DP (1997) Ultraviolet radiation induces both degradation and synthesis of phycobilisomes in Nostoc sp.: a spectroscopic and biochemical approach. FEMS Microbiol Ecol 23:301–313
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
Battista JR (1997) Against all odds: the survival strategies of Deinococcus radiodurans. Annu Rev Microbiol 51:203–224
Bauermeister A, Moeller R, Reitz G, Sommer S, Rettberg P (2011) Effect of relative humidity on Deinococcus radioduran’ resistance to prolonged desiccation, heat, ionizing, germicidal, and environmentally relevant UV radiation. Microb Ecol 61:715–722
Billi D (2009a) Subcellular integrities in Chroococcidiopsis sp. CCMEE 029 survivors after prolonged desiccation revealed by molecular probes and genome stability assays. Extremophiles 13:49–57
Billi D (2009b) Loss of topological relationships in a Pleurocapsalean cyanobacterium (Chroococcidiopsis sp.) with partially inactivated ftsZ. Ann Microbiol 59:1–4
Billi D (2012) Anhydrobiotic rock-inhabiting cyanobacteria: potential for astrobiology and biotechnology. In: Stan-Lotter H, Fendrihan F (eds) Adaptation of microbial life to environmental extremes: novel research results and application. Springer, Wien-New York, pp 119–132
Billi D, Grilli Caiola M, Paolozzi L, Ghelardini P (1998) A method for DNA extraction from the desert cyanobacterium Chroococcidiopsis and its application to identification of ftsZ. Appl Environ Microbiol 64:4053–4056
Billi D, Friedmann EI, Hofer KG, Grilli Caiola M, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66:1489–1492
Billi D, Viaggiu E, Cockell CS, Rabbow E, Horneck G, Onofri S (2011) Damage escape and repair in dried Chroococcidiopsis spp. from hot and cold deserts exposed to simulated space and Martian conditions. Astrobiology 11:65–73
Castenholz RW, Garcia-Pichel F (2012) Cyanobacterial responses to UV radiation. In: Whitton BA (ed) The ecology of cyanobacteria II: their diversity in space and time. Springer, The Netherlands, pp 481–499
Chan Y, Lacap DC, Lau MC, Ha KY, Warren-Rhodes KA, Cockell CS, Cowan DA, McKay CP, Pointing SB (2012) Hypolithic microbial communities: between a rock and a hard place. Environ Microbiol 14:2272–2282
Chen LZ, Wang GH, Hong S, Liu A, Li C, Liu YD (2009) UV-B-induced oxidative damage and protective role of exopolysaccharides in desert cyanobacterium Microcoleus vaginatus. J Integr Plant Biol 51:194–200
Cockell CS, Schuerger AC, Billi D, Friedmann EI, Panitz C (2005) Effects of a simulated Martian UV Flux on the cyanobacterium, Chroococcidiopsis sp. 029. Astrobiology 5:127–140
Cockell CS, McKay CP, Warren-Rhodes K, Horneck G (2008) Ultraviolet radiation-induced limitation to epilithic microbial growth in arid deserts—dosimetric experiments in the hyperarid core of the Atacama Desert. J Photochem Photobiol, B 90:79–87
Cox MM, Battista JR (2005) Deinococcus radiodurans—the consummate survivor. Nat Rev Microbiol 3:882–892
Daly MJ (2012) Death by protein damage in irradiated cells. DNA Repair (Amst) 11:12–21
Dillon JD, Castenholz RW (1999) Scytonemin, a cyanobacterial sheath pigment, protects against UVC radiation: implications for early photosynthetic life. J Phycol 35:673–681
Dillon JG, Tatsumi CM, Tandingan PG, Castenholz RW (2002) Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis sp.). Arch Microbiol 177:322–331
Domain F, Houot L, Chauvat F, Cassier-Chauvat C (2004) Function and regulation of the cyanobacterial genes lexA, recA and ruvB: LexA is critical to the survival of cells facing inorganic carbon starvation. Mol Microbiol 53:65–80
Fajardo-Cavazos P, Schuerger AC, Nicholson WL (2010) Exposure of DNA and Bacillus subtilis spores to simulated Martian environments: use of quantitative PCR (qPCR) to measure inactivation rates of DNA to function as a template molecule. Astrobiology 10:403–411
Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633
Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Microbiol 9:791–802
Garcia-Pichel F, Castenholz RW (1993) Occurrence of UV absorbing, mycosporine-like compounds among cyanobacterial isolates and an estimate of their screening capacity. Appl Environ Microbiol 59:163–169
Garcia-Pichel F, Wingard CE, Castenholz RW (1993) Evidence regarding the UV sunscreen role of a mycosporine-like compound in the cyanobacterium Gloeocapsa sp. Appl Environ Microbiol 59:170–176
Grilli Caiola M, Billi D (2007) Chroococcidiopsis from desert to Mars. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Series: Cellular origin, life in extreme habitats and astrobiology. Springer, Berlin, pp 553–568
Grilli Caiola M, Billi D, Friedmann EI (1996) Effect of desiccation on envelopes of the cyanobacterium Chroococcidiopsis sp. (Chroococcales). Eur J Phycol 31:97–105
Helm RH, Potts M (2012) Extracellular Matrix (ECM). In: Whitton BA (ed) Ecology of cyanobacteria II. Springer, Berlin, pp 461–480
Hu C, Gao K, Witthon BA (2012) Semi-arid regions and deserts. In: Witton BA (ed) Ecology of cyanobacteria II. Springer, Berlin, pp 345–369
Hunsucker SW, Tissue BM, Malcolm Potts, Helm RF (2001) Screening protocol for the ultraviolet-photoprotective pigment scytonemin. Anal Biochem 288:227–230
Kim M, Wolff E, Huang T, Garibyan L, Earl AM, Battista JR, Miller JH (2004) Developing a genetic system in Deinococcus radiodurans for analyzing mutations. Genetics 166:661–668
Kumar A, Tyagi MB, Jha PN (2004) Evidences showing ultraviolet-B radiation-induced damage of DNA in cyanobacteria and its detection by PCR assay. Biochem Biophys Res Commun 318:1025–1030
Levine E, Thiel T (1987) UV-inducible DNA repair in the cyanobacteria Anabaena spp. J Bacteriol 169:3988–3993
Moeller R, Setlow P, Reitz G, Nicholson WL (2009) Roles of small, acid-soluble spore proteins and core water content in survival of Bacillus subtilis spores exposed to environmental solar UV radiation. Appl Environ Microb 75:5202–5208
Ng WO, Pakrasi HB (2001) DNA photolyase homologs are the major UV resistance factors in the cyanobacterium Synechocystis sp. PCC 6803. Mol Gen Genet 264:924–930
Pattanaik B, Schmann R, Karsten U (2007) Effects of ultraviolet radiation on cyanobacteria and their protective mechanisms. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Series: Cellular origin life in extreme habitats and astrobiology. Springer, Berlin, pp 31–45
Pereira S, Zille A, Micheletti E, Moradas-Ferreira P, De Philippis R, Tamagnini P (2009) Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiol Rev 33:917–941
Qiu B, Zhang A, Liu Z (2003) Oxidative stress in Nostoc flagelliforme subjected to desiccation and effects of exogenous oxidants on its photosynthetic recovery. J Appl Phycol 15:445–450
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Roldán M, Thomas F, Castel S, Quesada A, Hernández-Mariné M (2009) Noninvasive pigment identification in single cells from living phototrophic biofilms by confocal imaging spectrofluorometry. Appl Environ Microbiol 70:3745–3750
Rossi F, Micheletti E, Bruno L, Adhikary SP, Albertano P, Philippis RD (2012) Characteristics and role of the exocellular polysaccharides produced by five cyanobacteria isolated from phototrophic biofilms growing on stone monuments. Biofouling 28:215–224
Rudi K, Hagen I, Johnsrud BC, Skjefstad G, Tryland I (2010) Different length (DL) qPCR for quantification of cell killing by UV-induced DNA damage. Int J Environ Res Public Health 7:3376–3381
Slade D, Radman M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75:133–191
Stivaletta N, Barbieri R, Billi D (2012) Microbial colonization of the salt deposits in the driest place of the Atacama Desert (Chile). Orig Life Evol Biosph 42:143–152
Tao Y, Zhang X, Au DW, Mao X, Yuan K (2010) The effects of sub-lethal UV-C irradiation on growth and cell integrity of cyanobacteria and green algae. Chemosphere 78:541–547
Tempest PR, Moseley BE (1982) Lack of ultraviolet mutagenesis in radiation-resistant bacteria. Mutat Res 104:275–280
Trombert A, Irazoqui H, Martín C, Zalazar F (2007) Evaluation of UV-C induced changes in Escherichia coli DNA using repetitive extragenic palindromic-polymerase chain reaction (REP-PCR). J Photochem Photobiol B 89:44–49
Vermaas WF, Timlin JA, Jones HD, Sinclair MB, Nieman LT, Hamad SW, Melgaard DK, Haaland DM (2008) In vivo hyperspectral confocal fluorescence imaging to determine pigment localization and distribution in cyanobacterial cells. Proc Natl Acad Sci USA 105:4050–4055
Wierzchos J, Ascaso C, McKay CP (2006) Endolithic cyanobacteria in halite rocks from the hyperarid core of the Atacama Desert. Astrobiology 6:415–422
Wolf E, Schüßler A (2005) Phycobiliprotein fluorescence of Nostoc punctiforme changes during the life cycle and chromatic adaptation: characterization by spectral confocal laser scanning microscopy and spectral unmixing. Plant Cell Environ 28:480–491
Acknowledgments
This research was funded by the Italian Ministry of Foreign Affairs and the Italian Space Agency. The authors thank Dr. Elena Romano and Palma Mattioli, Centre of Advanced Microscopy “P. B. Albertano”, University of Rome “Tor Vergata”, for skillful assistance in using the facility.
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Communicated by A. Oren.
This paper is in memoriam of Prof.ssa Patrizia B. Albertano, founder of the Centre of Advanced Microscopy and leader of the Laboratory of Biology of Algae at the University of Rome “Tor Vergata”. She died prematurely on March 14th, 2012.
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Baqué, M., Viaggiu, E., Scalzi, G. et al. Endurance of the endolithic desert cyanobacterium Chroococcidiopsis under UVC radiation. Extremophiles 17, 161–169 (2013). https://doi.org/10.1007/s00792-012-0505-5
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DOI: https://doi.org/10.1007/s00792-012-0505-5