Halophilic Archaea: Life with Desiccation, Radiation and Oligotrophy over Geological Times

Halophilic archaebacteria (Haloarchaea) can survive extreme desiccation, starvation and radiation, sometimes apparently for millions of years. Several of the strategies that are involved appear specific for Haloarchaea (for example, the formation of halomucin, survival in fluid inclusions of halite), and some are known from other prokaryotes (dwarfing of cells, reduction of ATP). Several newly-discovered haloarchaeal strategies that were inferred to possibly promote long-term survival—halomucin, polyploidy, usage of DNA as a phosphate storage polymer, production of spherical dormant stages—remain to be characterized in detail. More information on potential strategies is desirable, since evidence for the presence of halite on Mars and on several moons in the solar system increased interest in halophiles with respect to the search for extraterrestrial life. This review deals in particular with novel findings and hypotheses on haloarchaeal long-term survival.

[1]  D. Oesterhelt,et al.  Fluorescence microscopy visualization of halomucin, a secreted 927 kDa protein surrounding Haloquadratum walsbyi cells , 2015, Front. Microbiol..

[2]  J. Soppa Polyploidy in Archaea and Bacteria: About Desiccation Resistance, Giant Cell Size, Long-Term Survival, Enforcement by a Eukaryotic Host and Additional Aspects , 2015, Journal of Molecular Microbiology and Biotechnology.

[3]  Y. Liu,et al.  Halophilic Archaea Cultivated from Surface Sterilized Middle-Late Eocene Rock Salt Are Polyploid , 2014, PloS one.

[4]  J. Soppa,et al.  Polyploidy in haloarchaea: advantages for growth and survival , 2014, Front. Microbiol..

[5]  U. Gophna,et al.  DNA as a Phosphate Storage Polymer and the Alternative Advantages of Polyploidy for Growth or Survival , 2014, PloS one.

[6]  D. Loizeau,et al.  Habitability on Mars from a microbial point of view. , 2013, Astrobiology.

[7]  O. Prieto-Ballesteros,et al.  pH and salinity evolution of Europa's brines: Raman spectroscopy study of fractional precipitation at 1 and 300 bar. , 2013, Astrobiology.

[8]  A. I. Saralov,et al.  Haloferax chudinovii sp. nov., a halophilic archaeon from Permian potassium salt deposits , 2013, Extremophiles.

[9]  J. Soppa Evolutionary advantages of polyploidy in halophilic archaea. , 2013, Biochemical Society transactions.

[10]  J. DiRuggiero,et al.  Radiation Resistance in Extremophiles: Fending Off Multiple Attacks , 2013 .

[11]  P. Briza,et al.  Spherical particles of halophilic archaea correlate with exposure to low water activity – implications for microbial survival in fluid inclusions of ancient halite , 2012, Geobiology.

[12]  P. DasSarma,et al.  The core and unique proteins of haloarchaea , 2012, BMC Genomics.

[13]  Nicolas Thomas,et al.  Seasonal Flows on Warm Martian Slopes , 2011, Science.

[14]  G. C. Dı́az,et al.  Archaeal diversity along a subterranean salt core from the Salar Grande (Chile). , 2011, Environmental microbiology.

[15]  S. Schuster,et al.  Haloquadratum walsbyi : Limited Diversity in a Global Pond , 2011, PloS one.

[16]  S. Fendrihan,et al.  Responses of haloarchaea to simulated microgravity. , 2011, Astrobiology.

[17]  T. Lowenstein,et al.  Microbial communities in fluid inclusions and long-term survival in halite , 2011 .

[18]  T. Egli How to live at very low substrate concentration. , 2010, Water research.

[19]  T. Lowenstein,et al.  Halophilic Archaea cultured from ancient halite, Death Valley, California. , 2010, Environmental microbiology.

[20]  J. Polle,et al.  Dunaliella Cells in Fluid Inclusions in Halite: Significance for Long-term Survival of Prokaryotes , 2010 .

[21]  T. Lowenstein,et al.  Halophilic Archaea cultured from ancient halite, Death , 2010 .

[22]  M. Dyall-Smith,et al.  Diversity of Haloquadratum and other haloarchaea in three, geographically distant, Australian saltern crystallizer ponds , 2009, Extremophiles.

[23]  J. S. Park,et al.  Haloarchaeal diversity in 23, 121 and 419 MYA salts , 2009, Geobiology.

[24]  T. Lowenstein,et al.  Microscopic identification of prokaryotes in modern and ancient halite, Saline Valley and Death Valley, California. , 2009, Astrobiology.

[25]  F. Postberg,et al.  Sodium salts in E-ring ice grains from an ocean below the surface of Enceladus , 2009, Nature.

[26]  Michael J. Daly,et al.  A new perspective on radiation resistance based on Deinococcus radiodurans , 2009, Nature Reviews Microbiology.

[27]  Shiladitya DasSarma,et al.  Extremely Radiation-Resistant Mutants of a Halophilic Archaeon with Increased Single-Stranded DNA-Binding Protein (RPA) Gene Expression , 2007, Radiation research.

[28]  A. Monson,et al.  Isolation of Live Cretaceous (121–112 Million Years Old) Halophilic Archaea from Primary Salt Crystals , 2007 .

[29]  J. Lennon Diversity and Metabolism of Marine Bacteria Cultivated on Dissolved DNA , 2007, Applied and Environmental Microbiology.

[30]  T. Allers,et al.  Regulated Polyploidy in Halophilic Archaea , 2006, PloS one.

[31]  J. C. Adamski,et al.  Entrapment of bacteria in fluid inclusions in laboratory-grown halite. , 2006, Astrobiology.

[32]  S. Fendrihan,et al.  Extremely halophilic archaea and the issue of long-term microbial survival , 2006, Re/views in environmental science and bio/technology.

[33]  Friedhelm Pfeiffer,et al.  The genome of the square archaeon Haloquadratum walsbyi : life at the limits of water activity , 2006, BMC Genomics.

[34]  J. DiRuggiero,et al.  Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation , 2005, Extremophiles.

[35]  Henk Bolhuis Walsby’s Square Archaeon , 2005 .

[36]  N. Gunde-Cimerman,et al.  Adaptation to life at high salt concentrations in archaea, bacteria, and eukarya , 2005 .

[37]  J. Wiegel,et al.  Sporulation genes in members of the low G+C Gram-type-positive phylogenetic branch (Firmicutes) , 2004, Archives of Microbiology.

[38]  W. Grant Life at low water activity. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  H. Stan-Lotter,et al.  Halobacterium noricense sp. nov., an archaeal isolate from a bore core of an alpine Permian salt deposit, classification of Halobacterium sp. NRC-1 as a strain of H. salinarum and emended description of H. salinarum , 2004, Extremophiles.

[40]  S. Fendrihan,et al.  Survival of halobacteria in fluid inclusions as a model of possible biotic survival in Martian halite , 2004 .

[41]  T. Onstott,et al.  Isolation of Halobacterium salinarum retrieved directly from halite brine inclusions. , 2003, Environmental microbiology.

[42]  J. Bada,et al.  Radiation-Dependent Limit for the Viability of Bacterial Spores in Halite Fluid Inclusions and on Mars , 2003, Radiation research.

[43]  H. Stan-Lotter,et al.  Halococcus dombrowskii sp. nov., an archaeal isolate from a Permian alpine salt deposit. , 2002, International journal of systematic and evolutionary microbiology.

[44]  A. Oren Halophilic Microorganisms and their Environments , 2002, Cellular Origin, Life in Extreme Habitats and Astrobiology.

[45]  H. Stan-Lotter,et al.  Novel haloarchaeal 16S rRNA gene sequences from Alpine Permo-Triassic rock salt , 2001, Extremophiles.

[46]  A. Treiman,et al.  The SNC meteorites are from Mars , 2000 .

[47]  K. Stetter,et al.  Very similar strains of Halococcus salifodinae are found in geographically separated permo-triassic salt deposits. , 1999, Microbiology.

[48]  M. Zolensky,et al.  Asteroidal water within fluid inclusion-bearing halite in an H5 chondrite, Monahans (1998) , 1999, Science.

[49]  T. McGenity,et al.  Halobacteria: the evidence for longevity , 1998, Extremophiles.

[50]  G. Wanner,et al.  Halococcus salifodinae sp. nov., an Archaeal Isolate from an Austrian Salt Mine , 1994 .

[51]  T. McGenity,et al.  Archaeal halophiles (halobacteria) from two British salt mines , 1993 .

[52]  W. Grant,et al.  Survival of Halobacteria Within Fluid Inclusions in Salt Crystals , 1988 .

[53]  E. Roedder The fluids in salt , 1984 .

[54]  R. Y. Morita Starvation-Survival of Heterotrophs in the Marine Environment , 1982 .

[55]  A. Walsby,et al.  Ultrastructure of a Gas-vacuolate Square Bacterium , 1981 .

[56]  D. J. Barber Matrix phyllosilicates and associated minerals in C2M carbonaceous chondrites , 1981 .

[57]  Heinz Dombrowski,et al.  BACTERIA FROM PALEOZOIC SALT DEPOSITS , 1963, Annals of the New York Academy of Sciences.

[58]  P. Tasch,et al.  Investigation of the viability of osmophile bacteria of great geological age. , 1960, Transactions of the Kansas Academy of Science. Kansas Academy of Science.