Survival of the Halophilic Archaeon Halovarius luteus after Desiccation, Simulated Martian UV Radiation and Vacuum in Comparison to Bacillus atrophaeus.
Bacillus atrophaeus
Desiccation
Halovarius luteus
Mars simulation chamber
Simulated Martian UV radiation
Vacuum
Journal
Origins of life and evolution of the biosphere : the journal of the International Society for the Study of the Origin of Life
ISSN: 1573-0875
Titre abrégé: Orig Life Evol Biosph
Pays: Netherlands
ID NLM: 8610391
Informations de publication
Date de publication:
Dec 2020
Dec 2020
Historique:
received:
07
02
2020
accepted:
20
05
2020
pubmed:
4
7
2020
medline:
10
4
2021
entrez:
4
7
2020
Statut:
ppublish
Résumé
Extraterrestrial environments influence the biochemistry of organisms through a variety of factors, including high levels of radiation and vacuum, temperature extremes and a lack of water and nutrients. A wide variety of terrestrial microorganisms, including those counted amongst the most ancient inhabitants of Earth, can cope with high levels of salinity, extreme temperatures, desiccation and high levels of radiation. Key among these are the haloarchaea, considered particularly relevant for astrobiological studies due to their ability to thrive in hypersaline environments. In this study, a novel haloarchaea isolated from Urmia Salt Lake, Iran, Halovarius luteus strain DA50
Identifiants
pubmed: 32617792
doi: 10.1007/s11084-020-09597-7
pii: 10.1007/s11084-020-09597-7
doi:
Types de publication
Comparative Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
157-173Commentaires et corrections
Type : ErratumIn
Références
Abrevaya XC, Paulino-Lima IG, Galante D, Rodrigues F, Mauas PJ, Cortón E, Lage CDAS (2011) Comparative survival analysis of Deinococcus radiodurans and the Haloarchaea Natrialba magadii and Haloferax volcanii exposed to vacuum ultraviolet irradiation. Astrobiology 11:1034–1040
pubmed: 22165956
Albers S-V, Meyer BH (2011) The archaeal cell envelope. Nat Rev Microbiol 9:414–426
pubmed: 21572458
Alipour S (2006) Hydrogeochemistry of seasonal variation of Urmia salt lake, Iran. Saline Systems 2:9
pubmed: 16834770
pmcid: 1533838
Alipour S, Mosavi Onlaghi K (2018) Mineralogy and geochemistry of major, trace and rare earth elements in sediments of the Hypersaline Urmia Salt Lake, Iran. Acta Geol Sin-Engl 92:1384–1395
Amiri V, Nakhaei M, Lak R, Kholghi M (2016) Geophysical, isotopic, and hydrogeochemical tools to identify potential impacts on coastal groundwater resources from Urmia hypersaline Lake, NW Iran. Environ Sci Pollut Res 23:16738–16760
Asem A, Eimanifar A, Djamali M, De Los Rios P, Wink M (2014) Biodiversity of the hypersaline Urmia Lake national park (NW Iran). Diversity 6:102–132
Awramik SM (2006) Respect for stromatolites. Nature 441:700–701
pubmed: 16760962
Baqué M, Viaggiu E, Scalzi G, Billi D (2013) Endurance of the endolithic desert cyanobacterium Chroococcidiopsis under UVC radiation. Extremophiles 17:161–169
pubmed: 23239185
Bibring J-P, Langevin Y, Gendrin A, Gondet B, Poulet F, Berthé M, Soufflot A, Arvidson R, Mangold N, Mustard J (2005) Mars surface diversity as revealed by the OMEGA/Mars express observations. Science 307:1576–1581
pubmed: 15718430
Blodgett, R. 2006. Appendix 2: most probable number from serial dilutions. Food And Drug Administration-Fda. Bacteriological Analytical Manual on line. Disponivelxem
Carrera M, Zandomeni R, Fitzgibbon J, Sagripanti JL (2007) Difference between the spore sizes of Bacillus anthracis and other Bacillus species. J Appl Microbiol 102:303–312
pubmed: 17241334
Cottin H, Kotler JM, Billi D, Cockell C, Demets R, Ehrenfreund P, Elsaesser A, D’hendecourt L, van Loon JJ, Martins Z (2017) Space as a tool for astrobiology: review and recommendations for experimentations in earth orbit and beyond. Space Sci Rev 209:83–181
Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599
pubmed: 1562184
Crowley DJ, Boubriak I, Berquist BR, Clark M, Richard E, Sullivan L, Dassarma S, McCready S (2006) The uvrA, uvrB and uvrC genes are required for repair of ultraviolet light induced DNA photoproducts in Halobacterium sp. NRC-1. Saline Systems 2:11
pubmed: 16970815
pmcid: 1590041
Csonka LN, Hanson AD (1991) Prokaryotic osmoregulation: genetics and physiology. Annu Rev Microbiol 45:569–606
pubmed: 1741624
Dassarma P, Capes MD, Dassarma S (2019) Comparative genomics of halobacterium strains from diverse locations. Microbial Diversity in the Genomic Era. Elsevier
De La Torre R, Sancho LG, Horneck G, De Los Ríos A, Wierzchos J, Olsson-Francis K, Cockell CS, Rettberg P, Berger T, De Vera J-PP (2010) Survival of lichens and bacteria exposed to outer space conditions–results of the Lithopanspermia experiments. Icarus 208:735–748
Diaz B, Schulze-Makuch D (2006) Microbial survival rates of Escherichia coli and Deinococcus radiodurans under low temperature, low pressure, and UV-irradiation conditions, and their relevance to possible martian life. Astrobiology 6:332–347
pubmed: 16689650
Dose K, Gill M (1995) DNA stability and survival of Bacillus subtilis spores in extreme dryness. Orig Life Evol Biosph 25:277–293
pubmed: 7708386
Dyall-Smith M (2008) The Halohandbook: protocols for haloarchaeal genetics. Haloarchaeal Genetics Laboratory, Melbourne, p 14
Fairén AG, Davila AF, Gago-Duport L, Amils R, McKay CP (2009) Stability against freezing of aqueous solutions on early Mars. Nature 459:401–404
pubmed: 19458717
Fendrihan S, Bérces A, Lammer H, Musso M, Rontó G, Polacsek TK, Holzinger A, Kolb C, Stan-Lotter H (2009) Investigating the effects of simulated Martian ultraviolet radiation on Halococcus dombrowskii and other extremely halophilic archaebacteria. Astrobiology 9:104–112
pubmed: 19215203
Gaidos, E. & Marion, G. 2003. Geological and geochemical legacy of a cold early Mars. J Geophys Res Planets: 108
Gooding JL (1992) Soil mineralogy and chemistry on Mars: possible clues from salts and clays in SNC meteorites. Icarus 99:28–41
Grant WD, Gemmell RT, McGenity TJ (1998) Halobacteria: the evidence for longevity. Extremophiles 2:279–287
pubmed: 9783175
Halfmann H, Denis B, Bibinov N, Wunderlich J, Awakowicz P (2007) Identification of the most efficient VUV/UV radiation for plasma based inactivation of Bacillus atrophaeus spores. J Phys D Appl Phys 40:5907–5911
Han S-B, Hou X-J, Wu C, Zhao Z, Ju Z, Zhang R, Cui H-L, Keen LJ, Xu L, Wu M (2019) Complete genome sequence of Salinigranum rubrum GX10T, an extremely halophilic archaeon isolated from a marine solar saltern. Mar Genomics 44:57–60
Henning KA, Li L, Iyer N, McDaniel LD, Reagan MS, Legerski R, Schultz RA, Stefanini M, Lehmann AR, Mayne LV (1995) The Cockayne syndrome group A gene encodes a WD repeat protein that interacts with CSB protein and a subunit of RNA polymerase II TFIIH. Cell 82:555–564
pubmed: 7664335
Hill DR, Keenan TW, Helm RF, Potts M, Crowe LM, Crowe JH (1997) Extracellular polysaccharide of Nostoc commune (cyanobacteria) inhibits fusion of membrane vesicles during desiccation. J Appl Phycol 9:237–248
Holland RD, Duffy CR, Rafii F, Sutherland JB, Heinze TM, Holder CL, Voorhees KJ, Lay JO Jr (1999) Identification of bacterial proteins observed in MALDI TOF mass spectra from whole cells. Anal Chem 71:3226–3230
pubmed: 10450164
Horneck G (1999) European activities in exobiology in earth orbit: results and perspectives. Adv Space Res 23:381–386
Huu NB, Denner EB, Ha DT, Wanner G, Stan-Lotter H (1999) Marinobacter aquaeolei sp. nov., a halophilic bacterium isolated from a Vietnamese oil-producing well. Int J Syst Evol Microbiol 49:367–375
Irie K, Scott A, Hasegawa N (2014) Investigation of the detection ability of an intrinsic fluorescence-based bioaerosol detection system for heat-stressed Bacteria. PDA J Pharm Sci Technol 68:478–493
pubmed: 25336419
Kish A, Kirkali G, Robinson C, Rosenblatt R, Jaruga P, Dizdaroglu M, Diruggiero J (2009) Salt shield: intracellular salts provide cellular protection against ionizing radiation in the halophilic archaeon, Halobacterium salinarum NRC-1. Environ Microbiol 11:1066–1078
pubmed: 19452594
Koike J, Oshima T, Koike K, Taguchi H, Tanaka R, Nishimura K, Miyaji M (1992) Survival rates of some terrestrial microorganisms under simulated space conditions. Adv Space Res 12:271–274
pubmed: 11538148
Kottemann M, Kish A, Iloanusi C, Bjork S, Diruggiero J (2005) Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation. Extremophiles 9:219–227
pubmed: 15844015
Kushner D (1968) Halophilic bacteria. Advances in applied microbiology, 10, 73–99
Landis GA (2001) Martian water: are there extant halobacteria on Mars? Astrobiology 1:161–164
pubmed: 12467119
Leuko S, Rothschild L, Burns B (2010) Halophilic archaea and the search for extinct and extant life on Mars. J Cosmol 5:940–950
Leuko S, Domingos C, Parpart A, Reitz G, Rettberg P (2015) The survival and resistance of Halobacterium salinarum NRC-1, Halococcus hamelinensis, and Halococcus morrhuae to simulated outer space solar radiation. Astrobiology 15:987–997
pubmed: 26539978
Li H (1976) Refractive index of alkali halides and its wavelength and temperature derivatives. J Phys Chem Ref Data 5:329–528
Lima T, Auchincloss AH, Coudert E, Keller G, Michoud K, Rivoire C, Bulliard V, De Castro E, Lachaize C, Baratin D (2009) HAMAP: a database of completely sequenced microbial proteome sets and manually curated microbial protein families in UniProtKB/Swiss-Prot. Nucleic Acids Res 37:D471–D478
pubmed: 18849571
Litchfield CD (1998) Survival strategies for microorganisms in hypersaline environments and their relevance to life on early Mars. Meteorit Planet Sci 33:813–819
pubmed: 11543079
Mancinelli R (2015) The affect of the space environment on the survival of Halorubrum chaoviator and Synechococcus (Nägeli): data from the space experiment OSMO on EXPOSE-R. Int J Astrobiol 14:123–128
Mancinelli R, White M, Rothschild L (1998) Biopan-survival I: exposure of the osmophiles Synechococcus sp.(Nageli) and Haloarcula sp. to the space environment. Adv Space Res 22:327–334
Mancinelli R, Fahlen T, Landheim R, Klovstad M (2004) Brines and evaporites: analogs for Martian life. Adv Space Res 33:1244–1246
Marion GM, Fritsen CH, Eicken H, Payne MC (2003) The search for life on Europa: limiting environmental factors, potential habitats, and Earth analogues. Astrobiology 3:785–811
pubmed: 14987483
Martins Z, Cottin H, Kotler JM, Carrasco N, Cockell CS, De La Torre Noetzel R, Demets R, De Vera J-P, D’hendecourt L, Ehrenfreund P (2017) Earth as a tool for astrobiology—a European perspective. Space Sci Rev 209:43–81
McCready S, Müller JA, Boubriak I, Berquist BR, Ng WL, Dassarma S (2005) UV irradiation induces homologous recombination genes in the model archaeon, Halobacterium sp. NRC-1. Saline Systems 1:3
pubmed: 16176594
pmcid: 1224876
McGenity TJ, Gemmell RT, Grant WD, Stan-Lotter H (2000) Origins of halophilic microorganisms in ancient salt deposits: Minireview. Environ Microbiol 2:243–250
pubmed: 11200425
Mehrshad M, Amoozegar MA, Makhdoumi A, Rasooli M, Asadi B, SCHUMANN P, Ventosa A (2015) Halovarius luteus gen. nov., sp. nov., an extremely halophilic archaeon from a salt lake. Int J Syst Evol Microbiol 65:2420–2425
pubmed: 25899505
Monk JD, Clavero MRS, Beuchat LR, Doyle MP, Brackett RE (1994) Irradiation inactivation of Listeria monocytogenes and Staphylococcus aureus in low-and high-fat, frozen and refrigerated ground beef. J Food Prot 57:969–974
pubmed: 31121723
Mustard J, Adler M, Allwood A, Bass D, Beaty D, Bell J, Brinckerhoff W, Carr M, Des Marais D, Brake B (2013) Report of the Mars 2020 science definition team. Mars Explor Progr Anal Gr:155–205
Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548–572
pubmed: 10974126
pmcid: 99004
Norton CF, Grant WD (1988) Survival of halobacteria within fluid inclusions in salt crystals. Microbiology 134:1365–1373
Oren A, Mana L (2002) Amino acid composition of bulk protein and salt relationships of selected enzymes of Salinibacter ruber, an extremely halophilic bacterium. Extremophiles 6:217–223
pubmed: 12072957
Peeters Z, Vos D, Ten Kate I, Selch F, van Sluis C, Sorokin DY, Muijzer G, Stan-Lotter H, van Loosdrecht M, Ehrenfreund P (2010) Survival and death of the haloarchaeon Natronorubrum strain HG-1 in a simulated martian environment. Adv Space Res 46:1149–1155
Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Mol Biol Rev 58:755–805
Rezvantalab, S. & Amrollahi, M. H. 2011. Investigation of recent changes in Urmia salt lake. International Journal of Chemical and Environmental Engineering, 2
Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline systems 1:5
Rothschild L, Lister A (2003) Evolution on planet earth: impact of the physical environment, Elsevier
Sawyer DJ, McGehee MD, Canepa J, Moore CB (2000) Water soluble ions in the Nakhla martian meteorite. Meteorit Planet Sci 35:743–747
Sella SRBR, Guizelini BP, Vandenberghe LPDS, Medeiros ABP, Soccol CR (2009) Lab-scale production of Bacillus atrophaeus' spores by solid state fermentation in fifferent types of bioreactors. Braz Arch Biol Technol 52:159–170
Sella SR, Vandenberghe LP, Soccol CR (2015) Bacillus atrophaeus: main characteristics and biotechnological applications–a review. Crit Rev Biotechnol 35:533–545
pubmed: 24963702
Shahmohammadi HR, Asgarani E, Terato H, Saito T, Ohyama Y, Gekko K, Yamamoto O, Ide H (1998) Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinarium against DNA-damaging agents. J Radiat Res 39:251–262
Siefermann-Harms D (1987) The light-harvesting and protective functions of carotenoids in photosynthetic membranes. Physiol Plant 69:561–568
Singh SP, Raval V, Purohit MK (2013) Strategies for the salt tolerance in Bacteria and Archeae and its implications in developing crops for adverse conditions. Plant Acclimation to Environmental Stress. Springer
Sonnenfeld, P. & Perthuisot, J.-P. 1984. Brines and evaporites, Wiley Online Library
Stan-Lotter H, Fendrihan S (2015) Halophilic archaea: life with desiccation, radiation and oligotrophy over geological times. Life 5:1487–1496
pubmed: 26226005
pmcid: 4598649
Sutton S (2010) The most probable number method and its uses in enumeration, qualification, and validation. J Valid Technol 16:35–38
Tebbe A, Schmidt A, Konstantinidis K, Falb M, Bisle B, Klein C, Aivaliotis M, Kellermann J, Siedler F, Pfeiffer F (2009) Life-style changes of a halophilic archaeon analyzed by quantitative proteomics. Proteomics 9:3843–3855
Tepfer D, Zalar A, Leach S (2012) Survival of plant seeds, their UV screens, and nptII DNA for 18 months outside the international Space Station. Astrobiology 12:517–528
pubmed: 22680697
Vago JL, Westall F, Coates AJ, Jaumann R, Korablev O, Ciarletti V, Mitrofanov I, Josset J-L, De Sanctis MC, Bibring J-P (2017) Habitability on early Mars and the search for biosignatures with the ExoMars Rover. Astrobiology 17:471–510
pubmed: 31067287
pmcid: 5685153
Vreeland RH, Rosenzweig WD, Powers DW (2000) Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal. Nature 407:897–900
pubmed: 11057666
Vreeland R, Jones J, Monson A, Rosenzweig W, Lowenstein T, Timofeeff M, Satterfield C, Cho B, Park J, Wallace A (2007) Isolation of live cretaceous (121–112 million years old) halophilic Archaea from primary salt crystals. Geomicrobiol J 24:275–282
Wall DB, Lubman DM, Flynn SJ (1999) Rapid profiling of induced proteins in bacteria using MALDI-TOF mass spectrometric detection of nonporous RP HPLC-separated whole cell lysates. Anal Chem 71:3894–3900
pubmed: 10489535
Wynn-Williams D, Newton E, Edwards H (2001) The role of habitat structure for biomolecule integrity and microbial survival under extreme environmental stress in Antarctica (and Mars?): ecology and technology. Exo−/astro-biology:225–237
Yang LF, Jiang JQ, Zhao BS, Zhang B, Feng DQ, Lu WD, Wang L, Yang SS (2006) A Na+/H+ antiporter gene of the moderately halophilic bacterium Halobacillus dabanensis D-8T: cloning and molecular characterization. FEMS Microbiol Lett 255:89–95
pubmed: 16436066
Zhou P, Wen J, Oren A, Chen M, Wu M (2007) Genomic survey of sequence features for ultraviolet tolerance in haloarchaea (family Halobacteriaceae). Genomics 90:103–109
pubmed: 17498923