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Experimental Evolution to Explore Adaptation of Terrestrial Bacteria to the Martian Environment

  • Wayne L. Nicholson
Chapter
Part of the Grand Challenges in Biology and Biotechnology book series (GCBB)

Abstract

Since their origin some 3.8 billion years ago, microorganisms have diversified such that they now inhabit practically every conceivable niche on planet Earth. Many of these earthly niches are at physical and/or chemical conditions considered to be at the extreme margins of habitability. But what are the true extremes at which life can exist? Recent robotic explorations of our solar system have led to the discovery of potentially habitable environments on other celestial bodies such as the planet Mars or in subsurface oceans under the icy moons of Jupiter and Saturn. In order to investigate whether life could exist in such extraterrestrial environments, laboratory evolution experiments have been undertaken to probe the physical limits at which life can be forced to adapt. Results from these experiments are informing us about the molecular mechanisms microbes utilize to perform critical life functions at environmental extremes both on and off Earth.

Notes

Acknowledgments

The author thanks Andrew Schuerger and Patricia Fajardo-Cavazos for helpful discussions and Hoang Nguyen for communication of data before publication. This work has been supported over the years by grants from the NASA Exobiology (NNA04CI35A, NNX08AO15G) and Planetary Protection (NNA05CS68G, NNA06CB58G) programs.

References

  1. Bergqvist S, Williams MA, O’Brien R, Ladbury JE (2003) Halophilic adaptation of protein-DNA interactions. Biochem Soc Trans 31:677–680.  https://doi.org/10.1042/bst0310677 CrossRefPubMedGoogle Scholar
  2. Berry BJ, Jenkins DG, Schuerger AC (2010) Effects of simulated Mars conditions on the survival and growth of Escherichia coli and Serratia liquefaciens. Appl Environ Microbiol 76(8):2377–2386.  https://doi.org/10.1128/AEM.02147-09 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Casanueva A, Tuffin M, Cary C, Cowan DA (2010) Molecular adaptations to psychrophily: the impact of ‘omic’ technologies. Trends Microbiol 18(8):374–381.  https://doi.org/10.1016/j.tim.2010.05.002 CrossRefPubMedGoogle Scholar
  4. Cho KH (2017) The structure and function of the Gram-positive bacterial RNA degradosome. Front Microbiol 8:154.  https://doi.org/10.3389/fmicb.2017.00154 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Coates JD, Michaelidou U, Bruce RA, O'Connor SM, Crespi JN, Achenbach LA (1999) Ubiquity and diversity of dissimilatory (per)chlorate-reducing bacteria. Appl Environ Microbiol 65(12):5234–5241PubMedPubMedCentralGoogle Scholar
  6. Cockell CS, Catling DC, Davis WL, Snook K, Kepner RL, Lee P, McKay CP (2000) The ultraviolet environment of Mars: biological implications past, present, and future. Icarus 146(2):343–359CrossRefGoogle Scholar
  7. Cockell CS, Bush T, Bryce C, Direito S, Fox-Powell M, Harrison JP, Lammer H, Landenmark H, Martin-Torres J, Nicholson N, Noack L, O’Malley-James J, Payler SJ, Rushby A, Samuels T, Schwendner P, Wadsworth J, Zorzano MP (2016) Habitability: a review. Astrobiology 16(1):89–117.  https://doi.org/10.1089/ast.2015.1295 CrossRefPubMedGoogle Scholar
  8. Collins MA, Buick RK (1989) Effect of temperature on the spoilage of stored peas by Rhodotorula glutinis. Food Microbiol 6:135–142CrossRefGoogle Scholar
  9. Crawford RL (2005) Microbial diversity and its relationship to planetary protection. Appl Environ Microbiol 71(8):4163–4168.  https://doi.org/10.1128/AEM.71.8.4163-4168.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  10. D’Amico S, Collins T, Marx JC, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7(4):385–389.  https://doi.org/10.1038/sj.embor.7400662 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Detkova EN, Boltyanskaya YV (2007) Osmoadaptation of haloalkaliphilic bacteria: role of osmoregulators and their possible practical application. Microbiology 76(5):511–522.  https://doi.org/10.1134/s0026261707050013 CrossRefGoogle Scholar
  12. Eigenbrode JL, Summons RE, Steele A, Freissinet C, Millan M, Navarro-González R, Sutter B, McAdam AC, Franz HB, Glavin DP, Archer PD, Mahaffy PR, Conrad PG, Hurowitz JA, Grotzinger JP, Gupta S, Ming DW, Sumner DY, Szopa C, Malespin C, Buch A, Coll P (2018) Organic matter preserved in 3-billion-year-old mudstones at Gale crater, Mars. Science 360(6393):1096–1101CrossRefGoogle Scholar
  13. Egli T (2010) How to live at very low substrate concentration. Water Res 44(17):4826–4837.  https://doi.org/10.1016/j.watres.2010.07.023 CrossRefPubMedGoogle Scholar
  14. Ehlmann BL, Mustard JF, Murchie SL (2010) Geologic setting of serpentine deposits on Mars. Geophys Res Lett 37:5.  https://doi.org/10.1029/2010gl042596 CrossRefGoogle Scholar
  15. Fajardo-Cavazos P, Schuerger A, Nicholson W (2007) Testing interplanetary transfer of bacteria between Earth and Mars as a result of natural impact phenomena and human spaceflight activities. Acta Astronaut 60(4-7):534–540CrossRefGoogle Scholar
  16. Ferrer M, Chernikova TN, Yakimov MM, Golyshin PN, Timmis KN (2003) Chaperonins govern growth of Escherichia coli at low temperatures Chaperonins govern growth of Escherichia coli at low temperatures. Nat Biotechnol 21(11):1266–1267.  https://doi.org/10.1038/nbt1103-1266 CrossRefPubMedGoogle Scholar
  17. Freissinet C, Glavin DP, Mahaffy PR, Miller KE, Eigenbrode JL, Summons RE, Brunner AE, Buch A, Szopa C, Archer PD, Franz HB, Atreya SK, Brinckerhoff WB, Cabane M, Coll P, Conrad PG, Des Marais DJ, Dworkin JP, Fairen AG, Francois P, Grotzinger JP, Kashyap S, ten Kate IL, Leshin LA, Malespin CA, Martin MG, Martin-Torres FJ, McAdam AC, Ming DW, Navarro-Gonzalez R, Pavlov AA, Prats BD, Squyres SW, Steele A, Stern JC, Sumner DY, Sutter B, Zorzano MP, Team MSLS (2015) Organic molecules in the Sheepbed Mudstone, Gale Crater, Mars. J Geophys Res Planets 120(3):495–514.  https://doi.org/10.1002/2014je004737 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2006) DNA repair and mutagenesis, 2nd edn. ASM Press, Washington, DCGoogle Scholar
  19. Gaillard F, Michalski J, Berger G, McLennan SM, Scaillet B (2013) Geochemical reservoirs and timing of sulfur cycling on Mars. Space Sci Rev 174(1–4):251–300.  https://doi.org/10.1007/s11214-012-9947-4 CrossRefGoogle Scholar
  20. Glavin DP, Freissinet C, Miller KE, Eigenbrode JL, Brunner AE, Buch A, Sutter B, Archer PD, Atreya SK, Brinckerhoff WB, Cabane M, Coll P, Conrad PG, Coscia D, Dworkin JP, Franz HB, Grotzinger JP, Leshin LA, Martin MG, McKay C, Ming DW, Navarro-Gonzalez R, Pavlov A, Steele A, Summons RE, Szopa C, Teinturier S, Mahaffy PR (2013) Evidence for perchlorates and the origin of chlorinated hydrocarbons detected by SAM at the Rocknest aeolian deposit in Gale Crater. J Geophys Res Planets 118(10):1955–1973.  https://doi.org/10.1002/jgre.20144 CrossRefGoogle Scholar
  21. Guildford SJ, Hecky RE (2000) Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: is there a common relationship? Limnol Oceanogr 45(6):1213–1223CrossRefGoogle Scholar
  22. Hassler DM, Zeitlin C, Wimmer-Schweingruber RF, Ehresmann B, Rafkin S, Eigenbrode JL, Brinza DE, Weigle G, Böttcher S, Böhm E, Burmeister S, Guo J, Köhler J, Martin C, Reitz G, Cucinotta FA, Kim MH, Grinspoon D, Bullock MA, Posner A, Gómez-Elvira J, Vasavada A, Grotzinger JP, Team MS (2014) Mars’ surface radiation environment measured with the Mars Science Laboratory’s Curiosity rover. Science 343(6169):1244797.  https://doi.org/10.1126/science.1244797 CrossRefPubMedGoogle Scholar
  23. Hecht MH, Kounaves SP, Quinn RC, West SJ, Young SM, Ming DW, Catling DC, Clark BC, Boynton WV, Hoffman J, Deflores LP, Gospodinova K, Kapit J, Smith PH (2009) Detection of perchlorate and the soluble chemistry of martian soil at the Phoenix lander site. Science 325(5936):64–67.  https://doi.org/10.1126/science.1172466 CrossRefPubMedGoogle Scholar
  24. Heller R, Armstrong J (2014) Superhabitable worlds. Astrobiology 14(1):50–66.  https://doi.org/10.1089/ast.2013.1088 CrossRefPubMedGoogle Scholar
  25. Hoffmann T, Bremer E (2017) Guardians in a stressful world: the Opu family of compatible solute transporters from Bacillus subtilis. Biol Chem 398(2):193–214.  https://doi.org/10.1515/hsz-2016-0265 CrossRefPubMedGoogle Scholar
  26. Horikoshi K, Antranikian G, Bull AT, Robb FT, Stetter KO (eds) (2011) Extremophiles handbook. Springer, BerlinGoogle Scholar
  27. Horneck G (1993) Responses of Bacillus subtilis spores to the space environment: results from experiments in space. Orig Life Evol Biosph 23(1):37–52CrossRefGoogle Scholar
  28. Kempf M, Chen F, Kern R, Venkateswaran K (2005) Recurrent isolation of hydrogen peroxide-resistant spores of Bacillus pumilus from a spacecraft assembly facility. Astrobiology 5(3):391–405CrossRefGoogle Scholar
  29. Kral TA, Altheide TS, Lueders AE, Schuerger AC (2011) Low pressure and desiccation effects on methanogens: implications for life on Mars. Planet Space Sci 59:264–270CrossRefGoogle Scholar
  30. La Duc M, Nicholson W, Kern R, Venkateswaran K (2003) Microbial characterization of the Mars Odyssey spacecraft and its encapsulation facility. Environ Microbiol 5(10):977–985CrossRefGoogle Scholar
  31. La Duc M, Kern R, Venkateswaran K (2004) Microbial monitoring of spacecraft and associated environments. Microb Ecol 47(2):150–158.  https://doi.org/10.1007/s00248-003-1012-0 CrossRefPubMedGoogle Scholar
  32. La Duc M, Dekas A, Osman S, Moissl C, Newcombe D, Venkateswaran K (2007) Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments. Appl Environ Microbiol 73(8):2600–2611.  https://doi.org/10.1128/AEM.03007-06 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Link L, Sawyer J, Venkateswaran K, Nicholson W (2004) Extreme spore UV resistance of Bacillus pumilus isolates obtained from an ultraclean spacecraft assembly facility. Microb Ecol 47(2):159–163CrossRefGoogle Scholar
  34. Melosh H (1984) Impact ejection, spallation, and the origin of meteorites. Icarus 59(2):234–260CrossRefGoogle Scholar
  35. Melosh HJ (1989) Impact cratering: a geologic process. Oxford University Press, New YorkGoogle Scholar
  36. Mileikowsky C, Cucinotta F, Wilson J, Gladman B, Horneck G, Lindegren L, Melosh J, Rickman H, Valtonen M, Zheng J (2000) Natural transfer of viable microbes in space – 1. From Mars to Earth and Earth to Mars. Icarus 145(2):391–427CrossRefGoogle Scholar
  37. Mileikowsky C, Cucinotta FA, Wilson JW, Gladman B, Horneck G, Lindegren L, Melosh HJ, Rickman H, Valtonen M, Zheng JQ (2002) Natural transfer of viable microbes in space. Part 1: From Mars to Earth and Earth to Mars. Icarus 145:391–427CrossRefGoogle Scholar
  38. Millan M, Szopa C, Buch A, Coll P, Glavin DP, Freissinet C, Navarro-Gonzalez R, Francois P, Coscia D, Bonnet JY, Teinturier S, Cabane M, Mahaffy PR (2016) In situ analysis of martian regolith with the SAM experiment during the first mars year of the MSL mission: identification of organic molecules by gas chromatography from laboratory measurements. Planet Space Sci 129:88–102.  https://doi.org/10.1016/j.pss.2016.06.007 CrossRefGoogle Scholar
  39. Mumma MJ, Villanueva GL, Novak RE, Hewagama T, Bonev BP, Disanti MA, Mandell AM, Smith MD (2009) Strong release of methane on Mars in northern summer 2003. Science 323(5917):1041–1045.  https://doi.org/10.1126/science.1165243 CrossRefPubMedGoogle Scholar
  40. Munteanu A, Uivarosi V, Andries A (2015) Recent progress in understanding the molecular mechanisms of radioresistance in Deinococcus bacteria. Extremophiles 19(4):707–719.  https://doi.org/10.1007/s00792-015-0759-9 CrossRefPubMedGoogle Scholar
  41. Newcombe DA, Schuerger AC, Benardini JN, Dickinson D, Tanner R, Venkateswaran K (2005) Survival of spacecraft-associated microorganisms under simulated martian UV irradiation. Appl Environ Microbiol 71(12):8147–8156.  https://doi.org/10.1128/aem.71.12.8147-8156.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Nicholson WL (2009) Ancient micronauts: interplanetary transport of microbes by cosmic impacts. Trends Microbiol 17(6):243–250.  https://doi.org/10.1016/j.tim.2009.03.004 CrossRefPubMedGoogle Scholar
  43. 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(3):548–572.  https://doi.org/10.1128/mmbr.64.3.548-572.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nicholson WL, Schuerger AC, Setlow P (2005) The solar UV environment and bacterial spore UV resistance: considerations for Earth-to-Mars transport by natural processes and human spaceflight. Mutat Res 571(1–2):249–264.  https://doi.org/10.1016/j.mrfmmm.2004.10.012 CrossRefPubMedGoogle Scholar
  45. Nicholson W, Schuerger A, Race M (2009) Migrating microbes and planetary protection. Trends Microbiol 17(9):389–392.  https://doi.org/10.1016/j.tim.2009.07.001 CrossRefPubMedGoogle Scholar
  46. Nicholson WL, Fajardo-Cavazos P, Fedenko J, Ortiz-Lugo JL, Rivas-Castillo A, Waters SM, Schuerger AC (2010) Exploring the low-pressure growth limit: evolution of Bacillus subtilis in the laboratory to enhanced growth at 5 kilopascals. Appl Environ Microbiol 76(22):7559–7565.  https://doi.org/10.1128/aem.01126-10 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Nicholson WL, McCoy L, Kerney K, Ming DW, Golden DC, Schuerger AC (2012) An aqueous extract of Mars analogue soil from the Phoenix landing site does not inhibit spore germination or growth of model spacecraft contaminants Bacillus subtilis 168 and B. pumilus SAFR-032. Icarus 220:904–910CrossRefGoogle Scholar
  48. Nicholson WL, Krivushin K, Gilichinsky D, Schuerger AC (2013) Growth of Carnobacterium spp. from permafrost under low pressure, temperature, and anoxic atmosphere has implications for Earth microbes on Mars. Proc Natl Acad Sci USA 110(2):666–671.  https://doi.org/10.1073/pnas.1209793110 CrossRefPubMedGoogle Scholar
  49. O’Leary M (2008) Anaxagoras and the origin of panspermia theory. iUniverse Press, BloomingtonGoogle Scholar
  50. Parry BR, Shain DH (2011) Manipulations of AMP metabolic genes increase growth rate and cold tolerance in Escherichia coli: implications for psychrophilic evolution. Mol Biol Evol 28(7):2139–2145.  https://doi.org/10.1093/molbev/msr038 CrossRefPubMedGoogle Scholar
  51. Rainey FA, Ray K, Ferreira M, Gatz BZ, Nobre F, Bagaley D, Rash BA, Park MJ, Earl AA, Shank NC, Small AM, Henk MC, Battista JR, Kampfer P, da Costa MS (2005) Extensive diversity of ionizing-radiation-resistant bacteria recovered from Sonoran desert soil and description of nine new species of the genus Deinococcus obtained from a single soil sample. Appl Environ Microbiol 71(11):7630.  https://doi.org/10.1128/aem.71.11.7630.2005 CrossRefPubMedCentralGoogle Scholar
  52. Raven JA, Andrews M, Quigg A (2005) The evolution of oligotrophy: implications for the breeding of crop plants for low input agricultural systems. Ann Appl Biol 146(3):261–280.  https://doi.org/10.1111/j.1744-7348.2005.040138.x CrossRefGoogle Scholar
  53. Reed CJ, Lewis H, Trejo E, Winston V, Evilia C (2013) Protein adaptations in archaeal extremophiles. Archaea Int Microbiol J 2013:14.  https://doi.org/10.1155/2013/373275 CrossRefGoogle Scholar
  54. Rettberg P, Anesio A, Baker V, Baross J, Cady SL, Foreman CM, Hauber E, Gabriele-Ori G, Pearce D, Rennó N, Ruvkun G, Sattler B, Saunders MP, Wagner D, Westall F (2015) Review of the MEPAG report on Mars special regions. National Academies Press, Washington, DCGoogle Scholar
  55. Rummel J (2001) Planetary exploration in the time of astrobiology: protecting against biological contamination. Proc Natl Acad Sci USA 98(8):2128–2131CrossRefGoogle Scholar
  56. Rummel JD, Beaty DW, Jones MA, Bakermans C, Barlow NG, Boston PJ, Chevrier VF, Clark BC, de Vera JP, Gough RV, Hallsworth JE, Head JW, Hipkin VJ, Kieft TL, McEwen AS, Mellon MT, Mikucki JA, Nicholson WL, Omelon CR, Peterson R, Roden EE, Sherwood Lollar B, Tanaka KL, Viola D, Wray JJ (2014) A new analysis of Mars “Special Regions”: findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology 14(11):887–968.  https://doi.org/10.1089/ast.2014.1227 CrossRefPubMedGoogle Scholar
  57. Schuerger AC (2004) Microbial ecology of the surface exploration of Mars with human-operated vehicles. In: Cockell CS (ed) Martian expedition planning. Univelt Publishers, Santa Barbra, CA, pp 363–386Google Scholar
  58. Schuerger AC, Nicholson WL (2006) Interactive effects of hypobaria, low temperature, and CO2 atmospheres inhibit the growth of mesophilic Bacillus spp. under simulated martian conditions. Icarus 185(1):143–152.  https://doi.org/10.1016/j.icarus.2006.06.014 CrossRefGoogle Scholar
  59. Schuerger AC, Nicholson WL (2016) Twenty species of hypobarophilic bacteria recovered from diverse soils exhibit growth under simulated martian conditions at 0.7 kPa. Astrobiology 16(12):964–976.  https://doi.org/10.1089/ast.2016.1587 CrossRefPubMedGoogle Scholar
  60. Schuerger A, Richards J, Hintze P, Kern R (2005) Surface characteristics of spacecraft components affect the aggregation of microorganisms and may lead to different survival rates of bacteria on Mars landers. Astrobiology 5(4):545–559CrossRefGoogle Scholar
  61. Schuerger A, Richards J, Newcombe D, Venkateswaran K (2006) Rapid inactivation of seven Bacillus spp. under simulated Mars UV irradiation. Icarus 181(1):52–62.  https://doi.org/10.1016/j.icarus.2005.10.008 CrossRefGoogle Scholar
  62. Schuerger AC, Golden DC, Ming DW (2012) Biotoxicity of Mars soils: 1. Dry deposition of analog soils on microbial colonies and survival under martian conditions. Planet Space Sci 72(1):91–101CrossRefGoogle Scholar
  63. Schuerger AC, Ulrich R, Berry BJ, Nicholson WL (2013) Growth of Serratia liquefaciens under 7 mbar, 0 °C, and CO2-enriched anoxic atmospheres. Astrobiology 13(2):115–131.  https://doi.org/10.1089/ast.2011.0811 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sephton MA, Lewis JMT, Watson JS, Montgomery W, Garnier C (2014) Perchlorate-induced combustion of organic matter with variable molecular weights: implications for Mars missions. Geophys Res Lett 41(21):7453–7460.  https://doi.org/10.1002/2014gl062109 CrossRefGoogle Scholar
  65. Shcherbakova V, Oshurkova V, Yoshimura Y (2015) The effects of perchlorates on the permafrost methanogens: implication for autotrophic life on Mars. Microorganisms 3(3):518–534.  https://doi.org/10.3390/microorganisms3030518 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Smith DJ, Schuerger AC, Davidson MM, Pacala SW, Bakermans C, Onstott TC (2009) Survivability of Psychrobacter cryohalolentis K5 under simulated martian surface conditions. Astrobiology 9(2):221–228.  https://doi.org/10.1089/ast.2007.0231 CrossRefPubMedGoogle Scholar
  67. Stern JC, Sutter B, Freissinet C, Navarro-Gonzalez R, McKay CP, Archer PD, Buch A, Brunner AE, Coll P, Eigenbrode JL, Fairen AG, Franz HB, Glavin DP, Kashyap S, McAdam AC, Ming DW, Steele A, Szopa C, Wray JJ, Martin-Torres FJ, Zorzano MP, Conrad PG, Mahaffy PR, Team MSLS (2015) Evidence for indigenous nitrogen in sedimentary and aeolian deposits from the Curiosity rover investigations at Gale crater, Mars. Proc Natl Acad Sci USA 112(14):4245–4250.  https://doi.org/10.1073/pnas.1420932112 CrossRefPubMedGoogle Scholar
  68. Stillman DE, Grimm RE (2011) Dielectric signatures of adsorbed and salty liquid water at the Phoenix landing site, Mars. J Geophys Res Planets 116:11.  https://doi.org/10.1029/2011je003838 CrossRefGoogle Scholar
  69. Stolper DA, Revsbech NP, Canfield DE (2010) Aerobic growth at nanomolar oxygen concentrations. Proc Natl Acad Sci USA 107(44):18755–18760.  https://doi.org/10.1073/pnas.1013435107 CrossRefPubMedGoogle Scholar
  70. Toner JD, Catling DC (2016) Water activities of NaClO4, Ca(ClO4)(2), and Mg(ClO4)(2) brines from experimental heat capacities: water activity > 0.6 below 200 K. Geochim Cosmochim Acta 181:164–174.  https://doi.org/10.1016/j.gca.2016.03.005 CrossRefGoogle Scholar
  71. Toner JD, Catling DC, Light B (2014) The formation of supercooled brines, viscous liquids, and low-temperature perchlorate glasses in aqueous solutions relevant to Mars. Icarus 233:36–47.  https://doi.org/10.1016/j.icarus.2014.01.018 CrossRefGoogle Scholar
  72. Van der Zee FR, Cervantes FJ (2009) Impact and application of electron shuttles on the redox (bio)transformation of contaminants: a review. Biotechnol Adv 27(3):256–277.  https://doi.org/10.1016/j.biotechadv.2009.01.004 CrossRefPubMedGoogle Scholar
  73. Venkateswaran K, Satomi M, Chung S, Kern R, Koukol R, Basic C, White D (2001) Molecular microbial diversity of a spacecraft assembly facility. Syst Appl Microbiol 24(2):311–320CrossRefGoogle Scholar
  74. Waite JH, Combi MR, Ip WH, Cravens TE, McNutt RL, Kasprzak W, Yelle R, Luhmann J, Niemann H, Gell D, Magee B, Fletcher G, Lunine J, Tseng WL (2006) Cassini ion and neutral mass spectrometer: enceladus plume composition and structure. Science 311(5766):1419–1422.  https://doi.org/10.1126/science.1121290 CrossRefPubMedGoogle Scholar
  75. Wassmann M, Moeller R, Reitz G, Rettberg P (2010) Adaptation of Bacillus subtilis cells to Archean-like UV climate: relevant hints of microbial evolution to remarkably increased radiation resistance. Astrobiology 10(6):605–615.  https://doi.org/10.1089/ast.2009.0455 CrossRefPubMedGoogle Scholar
  76. Waters SM, Robles-Martínez JA, Nicholson WL (2014) Exposure of Bacillus subtilis to low pressure (5 kPa) induces several global regulons including the sigB-mediated General Stress Response. Appl Environ Microbiol 80(16):4788–4794.  https://doi.org/10.1128/AEM.00885-14 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Waters SM, Zeigler DR, Nicholson WL (2015) Experimental evolution of enhanced growth by Bacillus subtilis at low atmospheric pressure: genomic changes revealed by whole-genome sequencing. Appl Environ Microbiol 81(21):7525–7532.  https://doi.org/10.1128/AEM.01690-15 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Webster CR, Mahaffy PR, Atreya SK, Flesch GJ, Mischna MA, Meslin PY, Farley KA, Conrad PG, Christensen LE, Pavlov AA, Martín-Torres J, Zorzano MP, McConnochie TH, Owen T, Eigenbrode JL, Glavin DP, Steele A, Malespin CA, Archer PD, Sutter B, Coll P, Freissinet C, McKay CP, Moores JE, Schwenzer SP, Bridges JC, Navarro-Gonzalez R, Gellert R, Lemmon MT, Team MS (2015) Mars atmosphere. Mars methane detection and variability at Gale crater. Science 347(6220):415–417.  https://doi.org/10.1126/science.1261713 CrossRefPubMedGoogle Scholar
  79. Webster CR, Mahaffy PR, Atreya SK, Moores JE, Flesch GJ, Malespin C, McKay CP, Martinez G, Smith CL, Martin-Torres J, Gomez-Elvira J, Zorzano M-P, Wong MH, Trainer MG, Steele A, Archer D Jr, Sutter B, Coll PJ, Freissinet C, Meslin P-Y, Gough RV, House CH, Pavlov A, Eigenbrode JL, Glavin DP, Pearson JC, Keymeulen D, Christensen LE, Schwenzer SP, Navarro-Gonzalez R, Pla-García J, Rafkin SCR, Vicente-Retortillo Á, Kahanpää H, Viudez-Moreiras D, Smith MD, Harri A-M, Genzer M, Hassler DM, Lemmon M, Crisp J, Sander SP, Zurek RW, Vasavada AR (2018) Background levels of methane in Mars’ atmosphere show strong seasonal variations. Science 360:1093–1096.  https://doi.org/10.1126/science.aaq0131 CrossRefPubMedGoogle Scholar
  80. Wood AP, Aurikko JP, Kelly DP (2004) A challenge for 21st century molecular biology and biochemistry: what are the causes of obligate autotrophy and methanotrophy? FEMS Microbiol Rev 28(3):335–352.  https://doi.org/10.1016/j.femsre.2003.12.001 CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Microbiology and Cell ScienceUniversity of FloridaMerritt IslandUSA

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