Avoidance of protein oxidation correlates with the desiccation and radiation resistance of hot and cold desert strains of the cyanobacterium Chroococcidiopsis

Fagliarone, Claudia; Mosca, Claudia; Ubaldi, Ilaria; Verseux, Cyprien; Wilmotte, Annick; Billi, Daniela; Baqué, Mickael

doi:10.1007/s00792-017-0957-8

Article (Scientific journals)

Avoidance of protein oxidation correlates with the desiccation and radiation resistance of hot and cold desert strains of the cyanobacterium Chroococcidiopsis

Fagliarone, Claudia; Mosca, Claudia; Ubaldi, Ilaria et al.

2017 • In Extremophiles: Life Under Extreme Conditions, 21, p. 981-991

Peer Reviewed verified by ORBi

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https://hdl.handle.net/2268/213766

DOI
10.1007/s00792-017-0957-8

PubMed
28856526

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Keywords :

dessication; Chroococidiopsis; cyanobacteria; resistance; oxydative stress; radiation

Abstract :

[en] In order to investigate the relationship between desiccation and the extent of protein oxidation in desert strains of Chroococcidiopsis a selection of 10 isolates from hot and cold deserts and the terrestrial cyanobacterium Chroococcidiopsis thermalis sp. PCC 7203, were exposed to desiccation (air-drying) and analysed for survival. Strain CCMEE 029 from the Negev desert and the aquatic cyanobacterium Synechocystis sp. PCC 6803 were further investigated for protein oxidation after desiccation (drying over silica gel), treatment with H2O2 up to 1M and exposure to γ-rays up to 25 kGy. Then a selection of desert strains of Chroococcidiopsis with different survival rates after prolonged desiccation, as well as Synechocystis sp. PCC 6803 and Chroococcidiopsis thermalis sp. PCC 7203, were analysed for protein oxidation after treatment with 10 mM and 100 mM of H2O2. Results suggest that in the investigated strains a tight correlation occurs between desiccation and radiation tolerance and avoidance of protein oxidation

Research Center/Unit :

CIP - Centre d'Ingénierie des Protéines - ULiège

Disciplines :

Biochemistry, biophysics & molecular biology
Microbiology

Author, co-author :

Fagliarone, Claudia

Mosca, Claudia

Ubaldi, Ilaria

Verseux, Cyprien

Wilmotte, Annick ; Université de Liège > Département des sciences de la vie > Physiologie et génétique bactériennes

Billi, Daniela

Baqué, Mickael

Language :

English

Title :

Avoidance of protein oxidation correlates with the desiccation and radiation resistance of hot and cold desert strains of the cyanobacterium Chroococcidiopsis

Publication date :

November 2017

Journal title :

Extremophiles: Life Under Extreme Conditions

ISSN :

1431-0651

eISSN :

1433-4909

Publisher :

Springer Science & Business Media B.V., Tokyo, Japan

Volume :

Pages :

981-991

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

Italian Space Agency, National Antarctic Research Program (PNRA16/00101; PNRA2013/AZ1.17).

Available on ORBi :

since 23 August 2017

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Bibliography

Baqué M, Viaggiu E, Scalzi G, Billi D (2013a) Endurance of the endolithic desert cyanobacterium Chroococcidiopsis under UVC radiation. Extremophiles 17:161–169
Baqué M, Scalzi G, Rabbow E, Rettberg P, Billi D (2013b) Biofilm and planktonic lifestyles differently support the resistance of the desert cyanobacterium Chroococcidiopsis under space and Martian simulations. Orig Life Evol Biosph 43:377–389
Billi D (2009) 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 (2012) Anhydrobiotic rock-inhabiting cyanobacteria: potential for astrobiology and biotechnology. In: Stan-Lotter H, Fendrihan F (eds) Adaption of microbial life to environmental extremes. Novel research results and application. Springer-Verlag, Wien, 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, Caiola MG, 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
Billi D, Baqué M, Verseux C, Rothschild LJ, de Vera J-P (2017) Desert cyanobacteria—potential for space and earth applications. In: Stan-Lotter H, Fendrihan F (eds) Adaption of microbial life to environmental extremes. Novel research results and application, 2nd edn. Springer-Verlag, Wien, pp 133–146
Chong CW, Convey P, Pearce DA, Tan KP (2012) Assessment of soil bacterial communities on Alexander Island (in the maritime and continental Antarctic transitional zone). Polar Biol 35:387–399
Chuvochina MS, Alekhina IA, Normand P, Petit J-R, Bulat SA (2011) Three Saharan dust event depositions on Mont Blanc glacier associated with different snow-colonizing bacterial phylotype. Microbiology 80:125–131
Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal database project: data and tools for high throughput rRNA analysis Nucl. Acids Res 42(database issue):D633–D642
Daly MJ (2012) Death by protein damage in irradiated cells. DNA Repair 11:12–21
Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Venkateswaran A, Hess M, Omelchenko MV, Kostandarithes HM, Makarova KS, Wackett LP, Fredrickson JK, Ghosal D (2004) Accumulation of Mn(II) in Deinococcus radiodurans facilitates γ-radiation resistance. Science 306:1025–1028
Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Leapman RD, Lai B, Ravel B, Li SM, Kemner KM, Fredrickson JK (2007) Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol 5:e92
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
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Fredrickson JK, Li SMW, Gaidamakova EK, Matrosova VY, Zhai M, Sulloway HM, Scholten JC, Brown MG, Balkwill DL, Daly MJ (2008) Protein oxidation: key to bacterial desiccation resistance? ISME J 2:393–403
Friedmann EI (1980) Endolithic microbial life in hot and cold deserts. Orig Life 10:223–235
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Larsson J, Nylander JA, Bergman B (2011) Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits. BMC Evol Biol 11:187
Mattimore V, Battista JR (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178(3):633–637
Michaud AB, Šabacká M, Priscu JC (2012) Cyanobacterial diversity across landscape units in a polar desert: Taylor Valley, Antarctica. FEMS Microbiol Ecol 82:268–278
Munteanu A, Uivarosi V, Andries A (2015) Recent progress in understanding the molecular mechanisms of radioresistance in Deinococcus bacteria. Extremophiles 19:707–719
Murik O, Oren N, Shotland Y, Raanan H, Treves H, Kedem I, Keren N, Hagemann M, Pade N, Kaplan A (2017) What distinguishes cyanobacteria able to revive after desiccation from those that cannot: the genome aspect. Environ Microbiol 19:535–550
Paulino-Lima IG, Fujishima K, Navarrete JU, Galante D, Rodrigues F, Azua-Bustos A, Rothschild LJ (2017) Extremely high UV-C radiation resistant microorganisms from desert environments with different manganese concentrations. J Photochem Photobiol B 163:327–336
Pointing SB, Warren-Rhodes KA, Lacap DC, Rhodes KL, McKay CP (2007) Hypolithic community shifts occur as a result of liquid water availability along environmental gradients in China’s hot and cold hyperarid deserts. Environ Microbiol 9:414–424
Raanan H, Oren N, Treves H, Keren N, Ohad I, Berkowicz SM, Hagemann M, Koch M, Shotland Y, Kaplan A (2016) Towards clarifying what distinguishes cyanobacteria able to resurrect after desiccation from those that cannot: the photosynthetic aspect. Biochim Biophys Acta 1857:715–722
Rudi K, Skulberg OM, Larsen F, Jakobsen KS (1997) Strain characterization and classification of oxyphotobacteria in clone cultures on the basis of 16S rRNA sequences from the variable regions V6, V7, and V8. Appl Environ Microbiol 63:2593–2599
Sattin SR, Cleveland CC, Hood E, Reed SC, King AJ, Schmidt SK, Robeson MS, Ascarrunz N, Nemergut DR (2009) Functional shifts in unvegetated, perhumid, recently-deglaciated soils do not correlate with shifts in soil bacterial community composition. J Microbiol 47:673–681
Shirkey B, McMaster NJ, Smith SC, Wright DJ, Rodriguez H, Jaruga P, Birincioglu M, Helm RF, Potts M (2003) Genomic DNA of Nostoc commune (Cyanobacteria) becomes covalently modified during long-term (decades) desiccation but is protected from oxidative damage and degradation. Nucleic Acids Res 31:2995–3005
Slade D, Radman M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75:133–191
Smith HD, Baqué M, Duncan A, McKay CP, Billi D (2011) Comparative analysis of cyanobacteria inhabiting rocks with different light transmittance in the Mojave Desert: a Mars terrestrial analogue. Int J Astrobiol 13:271–277
Sun H, Xu G, Zhan H, Chen H, Sun Z, Tian B, Hua Y (2010) Identification and evaluation of the role of the manganese efflux protein in Deinococcus radiodurans. BMC Microbiol 10:319
Van de Peer Y, De Wachter R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Bioinformatics 10:569–570
Verseux C, Baqué M, Cifariello R, Fagliarone C, Raguse M, Moeller R, Billi D (2017) Evaluation of the resistance of Chroococcidiopsis spp. to sparsely and densely ionizing irradiation. Astrobiology 17:118–125
Warren-Rhodes KA, Rhodes KL, Pointing SB, Ewing SA, Lacap DC, Gómez-Silva B, Amundson R, Friedmann EI, McKay CP (2006) Hypolithic cyanobacteria, dry limit of photosynthesis, and microbial ecology in the hyperarid Atacama Desert. Microb Ecol 52:389–398