Skip to main content
×
Home

Survival of halophilic Archaea in Earth's cold stratosphere

  • P. DasSarma (a1), V.J. Laye (a1), J. Harvey (a2), C. Reid (a2), J. Shultz (a2), A. Yarborough (a2), A. Lamb (a2), A. Koske-Phillips (a2), A. Herbst (a2), F. Molina (a2), O. Grah (a2), T. Phillips (a2) and S. DasSarma (a1)...
Abstract
Abstract

Halophilic Archaea are known to tolerate multiple extreme conditions on Earth and have been proposed as models for astrobiology. In order to assess the importance of cold-adaptation of these microorganisms in surviving stratospheric conditions, we launched live, liquid cultures of two species, the mesophilic model Halobacterium sp. NRC-1 and the cold-adapted Antarctic isolate Halorubrum lacusprofundi ATCC 49239, on helium balloons. After return to Earth, the cold-adapted species showed nearly complete survival while the mesophilic species exhibited slightly reduced viability. Parallel studies found that the cold-adapted species was also better able to survive freezing and thawing in the laboratory. Genome-wide transcriptomic analysis was used to compare the two haloarchaea at optimum growth temperatures versus low temperatures supporting growth. The cold-adapted species displayed perturbation of a majority of genes upon cold temperature exposure, divided evenly between up-regulated and down-regulated genes, while the mesophile exhibited perturbation of only a fifth of its genes, with nearly two-thirds being down-regulated. These results underscore the importance of genetic responses of H. lacusprofundi to cold temperature for enhanced survival in the stratosphere.

Copyright
Corresponding author
e-mail: pdassarma@som.umaryland.edu
References
Hide All
Anderson I.J., DasSarma P., Lucas S., Copeland A., Lapidus A., Del Rio T.G., Tice H., Dalin E., Bruce D.C., Goodwin L. et al. (2016). Complete genome sequence of the Antarctic Halorubrum lacusprofundi type strain ACAM 34. Stand. Genomic Sci. 11, 70.
Berquist B.R., Müller J.A. & DasSarma S. (2006). Genetic Systems for Halophilic Archaea. In Methods in Microbiology, ed. Oren A. & Rainey F., pp. 637668. Elsevier/Academic Press.
Boubriak I., Ng W.L., DasSarma P., DasSarma S., Crowley D.J. & McCready S.J. (2008). Transcriptional responses to biologically relevant doses of UV-B radiation in the model archaeon, Halobacterium sp. NRC-1. Saline Syst. 4, 13.
Calcott P.H. & MacLeod R.A. (1975). The survival of Escherichia coli from freeze-thaw damage: permeability barrier damage and viability. Can. J. Microbiol. 21, 17241732.
Capes M.D., Coker J.A., Gessler R., Grinblat-Huse V., DasSarma S.L., Jacob C.G., Kim J.M., DasSarma P. & DasSarma S. (2011). The information transfer system of halophilic archaea. Plasmid 65, 77101.
Capes M.D., DasSarma P. & DasSarma S. (2012). The core and unique proteins of haloarchaea. BMC Genomics 13, 39.
Chudobova D., Cihalova K., Jelinkova P., Zitka J., Nejdl L., Guran R., Klimanek M., Adam V. & Kizek R. (2015). Effects of stratospheric conditions on the viability, metabolism and proteome of prokaryotic cells. Atmosphere 6, 12901306.
Coker J.A. & DasSarma S. (2007). Genetic and transcriptomic analysis of transcription factor genes in the model halophilic Archaeon: coordinate action of TbpD and TfbA. BMC Genet.. 8, 61.
Coker J.A., DasSarma P., Kumar J., Müller J.A. & DasSarma S. (2007). Transcriptional profiling of the model Archaeon Halobacterium sp. NRC-1: responses to changes in salinity and temperature. Saline Syst. 3, 6.
Crowley D.J., Boubriak I., Berquist B.R., 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 Syst. 2, 11.
DasSarma S. (2006). Extreme halophiles are models for astrobiology. Microbe 1, 120127.
DasSarma S. & DasSarma P. (2012). Halophiles. In eLS, John Wiley & Sons, Ltd, DOI: 10.1002/9780470015902.a0000394.pub3.
DasSarma S. & DasSarma P. (2015). Halophiles and their enzymes: negativity put to good use. Curr. Op. Microbiol. 25, 120126.
DasSarma S.L., Capes M.D., DasSarma P. & DasSarma S. (2010). HaloWeb: the haloarchaeal genomes database. Saline Syst. 6, 12.
DasSarma S., Berquist B.R., Coker J.A., DasSarma P. & Müller J.A. (2006). Post-genomics of the model haloarchaeon Halobacterium sp. NRC-1. Saline Syst. 2, 3.
DasSarma P., Zamora R.C., Müller J.A. & DasSarma S. (2012). Genome-wide responses of the model archaeon Halobacterium sp. strain NRC-1 to oxygen limitation. J. Bacteriol. 194, 55205537.
DasSarma S., Capes M.D., Karan R. & DasSarma P. (2013). Amino acid substitutions in cold-adapted proteins from Halorubrum lacusprofundi, an extremely halophilic microbe from Antarctica. PLoS ONE 8, e58587.
DeVeaux L.C., Müller J.A., Smith J., Petrisko J., Wells D.P. & DasSarma S. (2007). Extremely radiation-resistant mutants of a halophilic archaeon with increased single-stranded DNA binding protein (RPA) gene expression. Radiation Res. 168, 507514.
Franzmann P.D., Stackebrandt E., Sanderson K., Volkman J.K., Cameron D.E., Stevenson P.L., McMeekin T.A. & Burton H.R. (1988). Halobacterium lacusprofundi sp. nov., a halophilic bacterium isolated from Deep Lake, Antarctica. Syst. Appl. Microbiol. 11, 2027.
Goh F., Jeon Y.J., Barrow K., Neilan B.A. & Burns B.P. (2011). Osmoadaptive strategies of the archaeon Halococcus hamelinensis isolated from a hypersaline stromatolite environment. Astrobiology 11, 529536.
Horneck G., Klaus D.M. & Mancinelli R.L. (2010). Space microbiology. Microbiol Mol. Biol. Rev. 74, 121156.
Jacob D.J. (1999). Introduction to Atmospheric Chemistry. Princeton University Press, USA.
Karan R., Capes M.D. & DasSarma S. (2012). Function and biotechnology of extremophilic enzymes in low water activity. Aquatic Biosyst. 8, 4.
Karan R., Capes M.D. & DasSarma S. (2013). Cloning, overexpression, purification, and characterization of a polyextremophilic β-galactosidase from the Antarctic haloarchaeon Halorubrum lacusprofundi . BMC Biotechnol. 13, 3.
Karan R., DasSarma P., Balcer-Kubiczek E., Weng R.R., Liao C.C., Goodlett D.R., Ng W.V. & DasSarma S. (2014). Bioengineering radioresistance by overproduction of RPA, a mammalian-type single-stranded DNA-binding protein, in a halophilic archaeon. Appl. Microbiol. Biotechnol. 98, 17371747.
Kounaves S.P., Chaniotakis N.A., Chevrier V.F., Carrier B.L., Folds K.E., Hansen V.M., McElhoney K.M., O'Neil G.D. & Weber A.W. (2014). Identification of the perchlorate parent salts at the Phoenix Mars landing site and possible implications. Icarus 232, 226231.
Leuko S., Rettberg P., Pontifex A.L. & Burns B.P. (2014). On the response of halophilic archaea to space conditions. Life (Basel) 4, 6676.
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, 327334.
Mancinelli R.L., Fahlen T.F., Landheim R. & Klovstad M.R. (2004). Brines and evaporites: analogs for Martian life. Adv. Space Res. 33, 12441246.
McCready S., Müller J.A., Boubriak I., Berquist B.R., Ng W.L. & DasSarma S. (2005). UV irradiation induces homologous recombination genes in the model archaeon, Halobacterium sp. NRC-1. Saline Syst. 1, 3.
McEwen A.S., Ojha L., Dundas C.M., Mattson S.S., Byrne S., Wray J.J., Cull S.C., Murchie S.L., Thomas N. & Gulick V.C. (2011). Seasonal flows on warm Martian slopes. Science 333, 740743.
Müller J.A. & DasSarma S. (2005). Functional genomic analysis of anaerobic respiration of the archaeon Halobacterium sp. NRC-1: dimethyl sulfoxide (DMSO) and trimethylamine N-oxide (TMAO) as terminal electron acceptors. J. Bacteriol. 187, 16591667.
Nicholson W.L., Moeller R. & Horneck G. (2012). Transcriptomic responses of germinating Bacillus subtilis spores exposed to 1.5 years of space and simulated martian conditions on the EXPOSE-E experiment PROTECT. Astrobiology 12, 469486.
Ojha L., Wilhelm M.B., Murchie S.L., McEwen A.S. & Wray J.J. (2015). Spectral evidence for hydrated salts in recurring slope lineae on Mars. Nat. Geosci. 8, 829832.
Reid I.N., Sparks W.B., Lubow S., McGrath M., Livio M., Valenti J., Sowers K.R., Shukla H.D., MacAuley S., Miller T. et al. (2006). Terrestrial models for extraterrestrial life: methanogens and halophiles at Martian temperatures. Int. J. Astrobiol. 5, 8997.
Rummel J.D., Beaty D.W., Jones M.A., Bakermans C., Barlow N.G., Boston P.J., Chevrier V.F., Clark B.C., de Vera J.-P.P., Gough R.V. et al. (2014). A New analysis of mars ‘‘Special Regions’’: findings of the second MEPAG special regions science analysis group (SR-SAG2). Astrobiology 14, 887968.
Schuerger A.C., Ulrich R., Berry B.J. & Nicholson W.L. (2013). Growth of Serratia liquefaciens under 7 mbar, 0 °C, and CO2-enriched anoxic atmospheres. Astrobiology 13, 115131.
Smith D.J. (2013). Microbes in the upper atmosphere and unique opportunities for astrobiology research. Astrobiology 13, 981990.
Smith D.L., Griffin D.W., McPeters R.D., Ward P.D. & Schuerger A.C. (2011). Microbial survival in the stratosphere and implications for global dispersal. Aerobiologia 27, 319332.
Stoker C.R., Zent A., Catling D.C., Douglas S., Marshall J.R., Archer D. Jr., Clark B., Kounaves S.P., Lemmon M.T., Quinn R. et al. (2010). Habitability of the Phoenix landing site. J. Geophys. Res. 115, E00E20.
Toner J.D., Catling D.C. & Light B. (2014). Soluble salts at the Phoenix lander site, Mars: a reanalysis of the wet chemistry laboratory data. Geochim. Cosmochim. Acta 136, 142168.
Vaishampayan P.A., Rabbow E., Horneck G. & Venkateswaran K.J. (2012). Survival of Bacillus pumilus spores for a prolonged period of time in real space conditions. Astrobiology 12, 487497.
Wassmann M., Moeller R., Rabbow E., Panitz C., Horneck G., Reitz G., Douki T., Cadet J., Stan-Lotter H., Cockell C.S et al. (2012). Survival of spores of the UV-resistant Bacillus subtilis strain MW01 after exposure to low-earth orbit and simulated martian conditions: data from the space experiment ADAPT on EXPOSE-E. Astrobiology 12, 498507.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

International Journal of Astrobiology
  • ISSN: 1473-5504
  • EISSN: 1475-3006
  • URL: /core/journals/international-journal-of-astrobiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 46
Total number of PDF views: 176 *
Loading metrics...

Abstract views

Total abstract views: 909 *
Loading metrics...

* Views captured on Cambridge Core between 27th October 2016 - 14th December 2017. This data will be updated every 24 hours.