Skip to main content
PMC home page
Frontiers in Microbiology logoLink to Frontiers in Microbiology
. 2019 Aug 13;10:1785. doi: 10.3389/fmicb.2019.01785

Corrigendum: Living at the Extremes: Extremophiles and the Limits of Life in a Planetary Context

Nancy Merino 1,2,3, Heidi S Aronson 4, Diana P Bojanova 1, Jayme Feyhl-Buska 1, Michael L Wong 5,6, Shu Zhang 7, Donato Giovannelli 2,8,9,10,*
PMCID: PMC6700686  PMID: 31456760

In the original article, there was a mistake in the legend for Table 4 as published. The legend in Table 4 is missing two parentheses around “Poly.” The correct legend appears below.

“Table 4. Examples of notable (Poly)extremophiles and their physiological requirements.”

Additionally, there was a mistake in Table 3 and Table 5 as published. In Table 3, the lowest temperature listed for Planococcus halocryophilus Or1 is “−18°C.” It should be “−15°C” instead. In addition, the pH range is “nr” but should be “6–11” instead. In the temperature column, 37 is bold type, but this should be regular type.

Table 3.

Limits of life as identified by (poly)extremophilic organisms in pure cultures.

Strain Domain Extremophile Type Isolation ecosystem Temperature (°C) pH Pressure (Mpa) Salinity (%) Water activity (aw) References
Picrophilus oshimae KAW 2/2 Archaea Hypercidophile Hot springs, Solfataras 47–65 (60)a −0.06–1.8 (0.7) nr 0–20 nr Schleper et al., 1995, 1996
Serpentinomonas sp. B1 Bacteria Alkaliphile Serpentinizing system (water) 18–37 (30) 9–12.5 (11) nr 0–0.5 (0) nr Suzuki et al., 2014
Methanopyrus kandleri 116 Archaea Hyperthemophile Deep-sea hydrothermal vent 90–122 (105) (6.3–6.6) 0.4–40 0.5–4.5 (3.0) nr Takai et al., 2008
Planococcus halocryophilus Or1 Bacteria Halopsychrophile Sea ice core −15–37 (25) 6–11 (7–8) nr 0–19 (2) nr Mykytczuk et al., 2012, 2013
Halarsenatibacter silvermanii SLAS-1 Bacteria Haloalkaliphile Soda lake 28–55 (44) 8.7–9.8 (9.4) nr 20–35 (35) nr Oremland et al., 2005
Thermococcus piezophilus CDGS Archaea Piezothermophile Deep-sea hydrothermal vent 60–95 (75) 5.5–9 (6) 0.1–125 (50) 2–6 (3) nr Dalmasso et al., 2016
Haloarchaeal strains GN-2 and GN-5 Archaea Xerophile Solar salterns (brine) nr nr nr nr 0.635 Javor, 1984
Open in a new tab
a

Data presented as range (optimum) for each parameter. nr, not reported in the original publication. Current limits are highlighted in bold.

Table 5.

Boundary conditions for different planetary bodies of astrobiological interest (compared to Earth), split into atmosphere, surface, and subsurface layers.

Planetary body Type Layer Temperature (°C) pH Pressure (MPa) Salinity (% NaCl) Geochemistry References
Earth Planet Atmosphere −100 – 40 Neutral, local acidic conditions possible due to volcanism and human activities 0.0001 – 0.1 0 78% N2, 21% O2, 9340 ppm Ar, 400 ppm CO2 18.2 ppm Ne, 5.2 ppm He, 1.7 ppm CH4, 1.1 ppm Kr, 0.6 ppm H2, variable H2 Hans Wedepohl, 1995; McDonough and Sun, 1995; Wayne, 2000
Surface −98.6 – 464 −3.6 – 13.3 0.003 – 112 0 – saturation Soils and sediments of varying lithologies, siliceous crust, ranging from mafic to felsic composition. Extensive ocean (70% planet surface), with 4,000 m average depth, 4°C and 3.5% average temperature and salinity respectively
Subsurface 3.25 – <400 ~1 – 12.8 <800 0.05 – saturation Soils and sediments of varying lithologies, siliceous crust, ranging from mafic to felsic composition, ultramafic mantle
Venus Planet Atmosphere −40 – 482a 0b 0.1 – 9.3c nr 96.5% CO2, 3.5% N2; small quantities of CO, SO2, HCl, HF, HDO, and H2O; H2SO4 condensates Cockell, 1999; Basilevsky and Head, 2003; Schulze-Makuch et al., 2004; Lang and Hansen, 2006; Bertaux et al., 2007; Airey et al., 2017
Surface 377 – 482 nr 4.5 – 9.3c nr Rocks are similar to tholeiitic and alkaline basalts; no liquid water
Subsurface nr nr nr nr Fluid channels; volcanism
Mars Planet Atmosphere −138 – 35d nr 0.0001–0.0009 nr 95.3% CO2, 2.7% N2, 1.6% Ar, 0.13% O2, 0.08% CO; trace amounts of H2O, NO, Ne, Kr, Xe Varnes et al., 2003; Fairén et al., 2004; Nicholson and Schuerger, 2005; Hecht et al., 2009; Smith et al., 2009; Johnson et al., 2011; Jones et al., 2011; Michalski et al., 2013; Longstaff, 2014; Wordsworth, 2016; Sinha et al., 2017; NASA, 2018
Surface −138 – 30 7.7e 0.0004–0.0009 5.2–5.8 Basaltic, Fe-/Mg-rich phyllosilicates, perchlorate salts, Al-rich clays, sulfates, chlorides, calcite, and silicas; potential cryosphere
Subsurface 55g 4.96–9.13h 10–303g Cl-rich brines Potential groundwater; basalt crust; possible serpentinization
Enceladus Icy moon Plume jets 0 ~8.5 – 9 High velocity jets > 0.5 90–99% H2O, ≤ 0.61–4.27% N2, 0.3–5.3% CO2, 0.1–1.68% CH4, 0.4–0.9% NH3, 0.4–39% H2, trace amounts of hydrocarbons; high mass organic cations, silicates, sodium, potassium, carbonates Gioia et al., 2007; Postberg et al., 2009, 2018; Waite et al., 2009; Zolotov et al., 2011; Glein et al., 2015; Holm et al., 2015; Hsu et al., 2015; Taubner et al., 2018
Icy shell (~10 km thick) −233 – −23 nr nr May have ammonia brine pockets May have tectonics
Subsurface global ocean (~0–170 km depth) <90 8.5 – 12.2k 1 – 8 0.45 – <4 Possible serpentinization
Titan Icy moon Atmosphere −183 – −73j nr > 0.01 – 0.15 nr 98.4% N2, 1.4% CH4, 0.2% H2, trace hydrocarbons and organics; 95% N2, 5% CH4, 0.1% H2; ~50 ppmv CO and ~15 ppbv CO2; C2H3CN; clouds Fulchignoni et al., 2005; de Kok et al., 2007; Norman, 2011; Baland et al., 2014; Mastrogiuseppe et al., 2014; Mitri et al., 2014; Sohl et al., 2014; Jennings et al., 2016; McKay, 2016; Mitchell and Lora, 2016; Brassé et al., 2017; Cordier et al., 2017
Surface −183 – −179 nr 0.15–0.35i nr Lakes and sea have CH4, C2H4, and dissolved nitrogen; dunes of solid organic material; low-latitude deserts and high-latitude moist climates
Subsurface −18 11.8l 50–300m Likely dense subsurface ocean (≤ 1,350 kg m−3) suggesting high salinity CH4 and C2H6
Ceres Dwarf planet Atmosphere nr nr nr nr Transient atmosphere with possible water vapo Fanale and Salvail, 1989; Zolotov, 2009, 2017; Küppers et al., 2014; Hayne and Aharonson, 2015; Neveu and Desch, 2015; Hendrix et al., 2016; Villarreal et al., 2017; Vu et al., 2017; Castillo-Rogez et al., 2018; McCord and Castillo-Rogez, 2018; McCord and Zambon, 2019
Surface (−157– −30)n 9.7–11.3n nr <10n Surface clays; (Mg, Ca)-carbonates; (Mg, NH4)-phyllosilicates; Fe-rich clays; salt deposits; chloride salts; water-rock interactions; brucite and magnetite; sulfur species and graphitized carbon; localized Na-carbonates (e.g.,Na2CO3), NH4Cl, NH4HCO3
Subsurface −143 – −93°o Likely alkaline <140 – 200p Potentially has briny or NH3-rich subsurface liquid Active water/ice-driven subsurface processes
Europa Icy moon Atmosphere (tenuous) nr nr 0.1−12 – 1−12 nr Ion sputtering of the surface; potential water plumes; O2; trace amounts of sodium and potassium Spencer et al., 1999; Chyba and Phillips, 2001; Marion et al., 2005; McGrath et al., 2009; Zolotov and Kargel, 2009; Travis et al., 2012; Cassidy et al., 2013; Muñoz-Iglesias et al., 2013; Kattenhorn and Prockter, 2014; Soderlund et al., 2014; Hand and Carlson, 2015; Kimura and Kitadai, 2015; Noell et al., 2015; Vance et al., 2016; Teolis et al., 2017; Zhu et al., 2017; Jones et al., 2018; Martin and McMinn, 2018; Pavlov et al., 2018
Surface (icy shell) −187 - −141 nr 0.1−12 May be saline, as delivered to the surface from a salty ocean, may have brine or salt inclusions H2O2, H2SO4, CO2; salts concentrated in cracks; oxidants and simple organics; potentially MgSO4, Na2SO4, Na2CO3, may have gas inclusions; may have tectonics
Subsurface ocean Daily inundation of seawater at T = −4 – 0 Potential for wide rangeq 0.1 – 30r <3.5 Likely contains Mg2+, SO42-, Na+, Cl−; oxidants and simple organics
Open in a new tab

The observed or putative geochemistry as well as other potential influences are also listed.

a

Thermosphere can be as cold as −173°C (Bertaux et al., 2007); the upper-to-middle cloud layers are between −40 and 60°C (Cockell, 1999).

b

Acid concentration in upper cloud layer is 81%, in lower layers up to 98% (Cockell, 1999).

c

Up to 11 MPa in a deep depression (Basilevsky and Head, 2003).

d

Summer air temperatures on Mars near the equator can reach a maximum of 35°C (Longstaff, 2014).

e

Measured by the Phoenix Mars Lander Wet Chemistry Laboratory at the northern plains of the Vastitas Borealis (Hecht et al., 2009).

f Liquid water may have had water activity > 0.95 (Fairén et al., 2009).

g

Calculated temperature at a depth of 1–30 km (Jones et al., 2011; Sinha et al., 2017); at a depth ~310 km, the calculated temperature is <427°C (Jones et al., 2011); the Martian core has temperature 1527°C (Longstaff, 2014).

h

Calculated groundwater pH (Varnes et al., 2003).

i

Calculated pressure at Titan's large sea, Ligeia Mare, is 0.20–0.35 MPa (Cordier et al., 2017).

j

Tropospheric temperature can be −193°C; 80% of incident sunlight is absorbed by Titan's atmosphere, suggesting that there are greenhouse and antigreenhouse effects (Mitchell and Lora, 2016).

k

The subsurface ocean on Enceladus could also have pH range 10.8–13.5 (Glein et al., 2015).

l

Calculated ocean pH with 5 wt% NH3 (Brassé et al., 2017).

m

Calculated pressure for the subsurface ocean with thickness 100 km and outer shell thickness 40–170 km (Baland et al., 2014); 800 MPa at the mantle ice shell-core boundary (Sohl et al., 2014).

n

Calculated surface temperatures, illuminated surfaces can have temperature < -173°C (Hayne and Aharonson, 2015); calculated pH and salinity for bright deposits in Occator crater (Zolotov, 2017); temperature for bright deposits in Occator crater might reach < -0.2°C (Zolotov, 2017).

o

Internal temperature might reach 77°C (McCord and Sotin, 2005).

p

Ceres' center pressure (Zolotov, 2009).

q

Acid brine may result from hydrothermal systems and be enriched with sulfuric acid (Kargel et al., 2000); neutral brine may occur as leachate from chondritic material and be enriched with magnesium sulfate (Kargel et al., 2000; Pasek and Greenberg, 2012); alkaline brine may occur in areas with natron (Na2CO3.10H2O), produced from the venting of CO2 from aqueous reservoirs (Langmuir, 1971; Millero and Rabindra, 1997).

r

At the base of a 100 km Europan ocean, the pressure is calculated to be 146 MPa (Marion et al., 2005).

In Table 5, the atmosphere entry for Earth > Atmosphere > Geochemistry is listed as “8.1% N2,” but the actual composition of Earth's atmosphere is “78% N2.”

The corrected Table 3 and Table 5 appear below.

Lastly, there is a grammatical error in the original article.

A correction has therefore been made to the section Can Life Originate, Evolve, or Survive on Other Planetary Bodies?, paragraph five:

“Solar and galactic cosmic rays (high-energy particles with energies from 10 MeV to >10 GeV) present challenges to life on the surface and near-surface of Mars and other planetary bodies. However, any subsurface aquifer deeper than a few meters would be protected from damaging radiation. Dartnell et al. (2007) calculated the galactic cosmic ray dosage rates and the corresponding survival times (which they defined as a million-fold decrease in cell number) of characteristic microbes at different depths in Mars's subsurface. At the surface, E. coli has a survival time of 1,200 years, while at 20-m depth, that survival time jumps to 1.5 × 108 years. Compared to E. coli, D. radiodurans has survival times an order of magnitude longer. These survival times are, in fact, lower limits in light of recent measurements by the Radiation Assessment Detector onboard the Mars Science Laboratory (Hassler et al., 2014), which found that the actual dose rate at Gale Crater (76 mGy year−1) is a factor of 2 lower than that modeled by Dartnell et al. (2007).”

The authors apologize for these errors and state that they do not change the scientific conclusions of the article in any way. The original article has been updated.

References

  1. Airey M. W., Mather T. A., Pyle D. M., Ghail R. C. (2017). The distribution of volcanism in the Beta-Atla-Themis region of Venus: its relationship to rifting and implications for global tectonic regimes. J. Geophys. Res. Planets 122, 1626–1649. 10.1002/2016JE005205 [DOI] [Google Scholar]
  2. Baland R. M., Tobie G., Lefèvre A., Van Hoolst T. (2014). Titan's internal structure inferred from its gravity field, shape, and rotation state. Icarus 237, 29–41. 10.1016/j.icarus.2014.04.007 [DOI] [Google Scholar]
  3. Basilevsky A. T., Head J. W. (2003). The surface of Venus. Rep. Prog. Phys. 66, 1699–1734. 10.1088/0034-4885/66/10/R04 [DOI] [Google Scholar]
  4. Bertaux J.-L., Vandaele A.-C., Korablev O., Villard E., Fedorova A., Fussen D., et al. (2007). A warm layer in Venus' cryosphere and high-altitude measurements of HF, HCl, H2O and HDO. Nature 450, 646–649. 10.1038/nature05974 [DOI] [PubMed] [Google Scholar]
  5. Brassé C., Buch A., Coll P., Raulin F. (2017). Low-temperature alkaline pH hydrolysis of oxygen-free Titan Tholins: carbonates' Impact. Astrobiology 17, 8–26. 10.1089/ast.2016.1524 [DOI] [PubMed] [Google Scholar]
  6. Cassidy T. A., Paranicas C. P., Shirley J. H., Dalton J. B., Teolis B. D., Johnson R. E., et al. (2013). Magnetospheric ion sputtering and water ice grain size at Europa. Planet. Space Sci. 77, 64–73. 10.1016/j.pss.2012.07.008 [DOI] [Google Scholar]
  7. Castillo-Rogez J., Neveu M., McSween H. Y., Fu R. R., Toplis M. J., Prettyman T. (2018). Insights into Ceres's evolution from surface composition. Meteorit. Planet. Sci. 53, 1820–1843. 10.1111/maps.13181 [DOI] [Google Scholar]
  8. Chyba C., Phillips C. (2001). Possible ecosystems and the search for life on Europa. Proc. Natl. Acad. Sci. U.S.A. 98, 801–804. 10.1073/pnas.98.3.801 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cockell C. S. (1999). Life on Venus. Planet. Space Sci. 47, 1487–1501. 10.1016/S0032-0633(99)00036-7 [DOI] [Google Scholar]
  10. Cordier D., Garciá-Sánchez F., Justo-Garciá D. N., Liger-Belair G. (2017). Bubble streams in Titan's seas as a product of liquid N2 + CH4 + C2H6 cryogenic mixture. Nat. Astron. 1:0102 10.1038/s41550-017-0102 [DOI] [Google Scholar]
  11. Dalmasso C., Oger P., Selva G., Courtine D., L'Haridon S., Garlaschelli A., et al. (2016). Thermococcus piezophilus sp. nov., a novel hyperthermophilic and piezophilic archaeon with a broad pressure range for growth, isolated from a deepest hydrothermal vent at the Mid-Cayman Rise. Syst. Appl. Microbiol. 39, 440–444. 10.1016/j.syapm.2016.08.003 [DOI] [PubMed] [Google Scholar]
  12. Dartnell L. R., Desorgher L., Ward J. M., Coates A. J. (2007). Modelling the surface and subsurface Martian radiation environment: implications for astrobiology. Geophys. Res. Lett. 34, 4–9. 10.1029/2006GL027494 [DOI] [Google Scholar]
  13. de Kok R., Irwin P. G. J., Teanby N. A., Lellouch E., Bézard B., Vinatier S., et al. (2007). Oxygen compounds in Titan's stratosphere as observed by Cassini CIRS. Icarus 186, 354–363. 10.1016/J.ICARUS.2006.09.016 [DOI] [Google Scholar]
  14. Fairén A. G., Davila A. F., Gago-Duport L., Amils R., McKay C. P. (2009). Stability against freezing of aqueous solutions on early Mars. Nature 459, 401–404. 10.1038/nature07978 [DOI] [PubMed] [Google Scholar]
  15. Fairén A. G., Fern?ndez-Remolar D., Dohm J. M., Baker V. R., Amils R. (2004). Inhibition of carbonate synthesis in acidic oceans on early Mars. Nature 431, 423–426. 10.1038/nature02911 [DOI] [PubMed] [Google Scholar]
  16. Fanale F. P., Salvail J. R. (1989). The water regime of asteroid (1) Ceres. Icarus 82, 97–110. 10.1016/0019-1035(89)90026-2 [DOI] [Google Scholar]
  17. Fulchignoni M., Ferri F., Angrilli F., Ball A. J., Bar-Nun A., Barucci M. A., et al. (2005). In situ measurements of the physical characteristics of Titan's environment. Nature 438, 785–791. 10.1038/nature04314 [DOI] [PubMed] [Google Scholar]
  18. Gioia G., Chakraborty P., Marshak S., Kieffer S. W. (2007). Unified model of tectonics and heat transport in a frigid Enceladus. Proc. Natl. Acad. Sci. U.S.A. 104, 13578–13581. 10.1073/pnas.0706018104 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Glein C. R., Baross J. A., Waite J. H. (2015). The pH of Enceladus' ocean. Geochim. Cosmochim. Acta 162, 202–219. 10.1016/j.gca.2015.04.017 [DOI] [Google Scholar]
  20. Hand K. P., Carlson R. W. (2015). Europa's surface color suggests an ocean rich with sodium chloride. Geophys. Res. Lett. 42, 3174–3178. 10.1002/2015GL063559 [DOI] [Google Scholar]
  21. Hans Wedepohl K. (1995). The composition of the continental crust. Geochim. Cosmochim. Acta 59, 1217–1232. 10.1016/0016-7037(95)00038-2 [DOI] [Google Scholar]
  22. Hassler D. M., Zeitlin C., Wimmer-schweingruber R. F., Ehresmann B., Rafkin S., Eigenbrode J. L., et al. (2014). Mars' surface radiation environment. Science 343:1244797. 10.1126/science.1244797 [DOI] [PubMed] [Google Scholar]
  23. Hayne P. O., Aharonson O. (2015). Thermal stability of ice on Ceres with rough topography. J. Geophys. Res. E Planets 120, 1567–1584. 10.1002/2015JE004887 [DOI] [Google Scholar]
  24. Hecht M. H., Kounaves S. P., Quinn R. C., West S. J., Young S. M. M., Ming D. W., et al. (2009). Detection of perchlorate and the soluble chemistry of Martian soil at the phoenix lander site. Science 325, 64–67. 10.1126/science.1172466 [DOI] [PubMed] [Google Scholar]
  25. Hendrix A. R., Vilas F., Li J. Y. (2016). Ceres: sulfur deposits and graphitized carbon. Geophys. Res. Lett. 43, 8920–8927. 10.1002/2016GL070240 [DOI] [Google Scholar]
  26. Holm N. G., Oze C., Mousis O., Waite J. H., Guilbert-Lepoutre A. (2015). Serpentinization and the Formation of H2 and CH4 on Celestial Bodies (Planets, Moons, Comets). Astrobiology 15, 587–600. 10.1089/ast.2014.1188 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hsu H. W., Postberg F., Sekine Y., Shibuya T., Kempf S., Horányi M., et al. (2015). Ongoing hydrothermal activities within Enceladus. Nature 519, 207–210. 10.1038/nature14262 [DOI] [PubMed] [Google Scholar]
  28. Javor B. (1984). Growth potential of halophilic bacteria isolated from solar salt environments: carbon sources and salt requirements. Appl. Environ. Microbiol. 48, 352–360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Jennings D. E., Cottini V., Nixon C. A., Achterberg R. K., Flasar F. M., Kunde V. G., et al. (2016). Surface temperatures on Titan during northern winter and spring. Astrophys. J. 816:L17 10.3847/2041-8205/816/1/L17 [DOI] [Google Scholar]
  30. Johnson A. P., Pratt L. M., Vishnivetskaya T., Pfiffner S., Bryan R. A., Dadachova E., et al. (2011). Extended survival of several organisms and amino acids under simulated martian surface conditions. Icarus 211, 1162–1178. 10.1016/j.icarus.2010.11.011 [DOI] [Google Scholar]
  31. Jones E. G., Lineweaver C. H., Clarke J. D. (2011). An extensive phase space for the potential martian biosphere. Astrobiology 11, 1017–1033. 10.1089/ast.2011.0660 [DOI] [PubMed] [Google Scholar]
  32. Jones R. M., Goordial J. M., Orcutt B. N. (2018). Low energy subsurface environments as extraterrestrial analogs. Front. Microbiol. 9:1605. 10.3389/fmicb.2018.01605 [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kargel J. S., Kaye J. Z., Head J. W., Marion G. M., Sassen R., Crowley J. K., et al. (2000). Europa?s crust and ocean: origin, composition, and the prospects for life. Icarus 148, 226–265. 10.1006/ICAR.2000.6471 [DOI] [Google Scholar]
  34. Kattenhorn S. A., Prockter L. M. (2014). Evidence for subduction in the ice shell of Europa. Nat. Geosci. 7, 762–767. 10.1038/ngeo2245 [DOI] [Google Scholar]
  35. Kimura J., Kitadai N. (2015). Polymerization of building blocks of life on Europa and other icy moons. Astrobiology 15, 430–441. 10.1089/ast.2015.1306 [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Küppers M., O'Rourke L., Bockelée-Morvan D., Zakharov V., Lee S., Von Allmen P., et al. (2014). Localized sources of water vapour on the dwarf planet (1) Ceres. Nature 505, 525–527. 10.1038/nature12918 [DOI] [PubMed] [Google Scholar]
  37. Lang N. P., Hansen V. L. (2006). Venusian channel formation as a subsurface process. J. Geophys. Res. E Planets 111:E04001 10.1029/2005JE002629 [DOI] [Google Scholar]
  38. Langmuir D. (1971). The geochemistry of some carbonate ground waters in central Pennsylvania. Geochim. Cosmochim. Acta 35, 1023–1045. 10.1016/0016-7037(71)90019-6 [DOI] [Google Scholar]
  39. Longstaff A. (2014). Astrobiology: An Introduction. Boca Raton, FL: CRC Press; 10.1201/b17880 [DOI] [Google Scholar]
  40. Marion G. M., Kargel J. S., Catling D. C., Jakubowski S. D. (2005). Effects of pressure on aqueous chemical equilibria at subzero temperatures with applications to Europa. Geochim. Cosmochim. Acta 69, 259–274. 10.1016/j.gca.2004.06.024 [DOI] [Google Scholar]
  41. Martin A., McMinn A. (2018). Sea ice, extremophiles and life on extra-terrestrial ocean worlds. Int. J. Astrobiol. 17, 1–16. 10.1017/S1473550416000483 [DOI] [Google Scholar]
  42. Mastrogiuseppe M., Poggiali V., Hayes A., Lorenz R., Lunine J., Picardi G., et al. (2014). The bathymetry of a Titan sea. Geophys. Res. Lett. 41, 1432–1437. 10.1002/2013GL058618 [DOI] [Google Scholar]
  43. McCord T. B., Castillo-Rogez J. C. (2018). Ceres's internal evolution: The view after Dawn. Meteorit. Planet. Sci. 53, 1778–1792. 10.1111/maps.13135 [DOI] [Google Scholar]
  44. McCord T. B., Sotin C. (2005). Ceres: evolution and current state. J. Geophys. Res. E Planets 110:E5 10.1029/2004JE002244 [DOI] [Google Scholar]
  45. McCord T. B., Zambon F. (2019). The surface composition of Ceres from the Dawn mission. Icarus 318, 2–13. 10.1016/j.icarus.2018.03.004 [DOI] [Google Scholar]
  46. McDonough W. F., Sun S. S. (1995). The composition of the Earth. Chem. Geol. 120, 223–253. 10.1016/0009-2541(94)00140-4 [DOI] [Google Scholar]
  47. McGrath M. A., Hansen C. J., Hendrix A. R. (2009). “Observations of Europa's Tenuous Atmosphere,” in Europa, Pappalardo R. T., McKinnon W. B., Khurana K. K. (Tucson, AZ: University of Arizona Press, 485–506. [Google Scholar]
  48. McKay C. P. (2016). Titan as the Abode of Life. Life 6:8. 10.3390/life6010008 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Michalski J. R., Cuadros J., Niles P. B., Parnell J., Deanne Rogers A., Wright S. P. (2013). Groundwater activity on Mars and implications for a deep biosphere. Nat. Geosci. 6, 133–138. 10.1038/ngeo1706 [DOI] [Google Scholar]
  50. Millero F. J., Rabindra N. R. (1997). A chemical equilibrium model for the carbonate system in natural waters. Croat. Chem. Acta 70, 1–38. [Google Scholar]
  51. Mitchell J. L., Lora J. M. (2016). The climate of titan. Annu. Rev. Earth Planet. Sci. 44, 353–380. 10.1146/annurev-earth-060115-012428 [DOI] [Google Scholar]
  52. Mitri G., Meriggiola R., Hayes A., Lefevre A., Tobie G., Genova A., et al. (2014). Shape, topography, gravity anomalies and tidal deformation of Titan. Icarus 236, 169–177. 10.1016/j.icarus.2014.03.018 [DOI] [Google Scholar]
  53. Muñoz-Iglesias V., Bonales L. J., Prieto-Ballesteros O. (2013). pH and Salinity Evolution of Europa's Brines: Raman Spectroscopy Study of Fractional Precipitation at 1 and 300 Bar. Astrobiology 13, 693–702. 10.1089/ast.2012.0900 [DOI] [PubMed] [Google Scholar]
  54. Mykytczuk N. C. S., Foote S. J., Omelon C. R., Southam G., Greer C. W., Whyte L. G. (2013). Bacterial growth at−15°C; molecular insights from the permafrost bacterium Planococcus halocryophilus Or1. ISME J. 7, 1211–1226. 10.1038/ismej.2013.8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Mykytczuk N. C. S., Wilhelm R. C., Whyte L. G. (2012). Planococcus halocryophilus sp. nov., an extreme sub-zero species from high arctic permafrost. Int. J. Syst. Evol. Microbiol. 62, 1937–1944. 10.1099/ijs.0.035782-0 [DOI] [PubMed] [Google Scholar]
  56. NASA (2018). Mars Fact Sheet. Greenbelt, MD: NASA; Available at: https://nssdc.gsfc.nasa.gov/planetary/factsheet/marsfact.html (accessed September 27, 2018). [Google Scholar]
  57. Neveu M., Desch S. J. (2015). Geochemistry, thermal evolution, and cryovolcanism on Ceres with a muddy ice mantle. Geophys. Res. Lett. 42, 10197–10206. 10.1002/2015GL066375 [DOI] [Google Scholar]
  58. Nicholson W. L., Schuerger A. C. (2005). Bacillus subtilis spore survival and expression of germination-induced bioluminescence after prolonged incubation under simulated mars atmospheric pressure and composition: implications for planetary protection and Lithopanspermia. Astrobiology 5, 536–544. 10.1089/ast.2005.5.536 [DOI] [PubMed] [Google Scholar]
  59. Noell A. C., Ely T., Bolser D. K., Darrach H., Hodyss R., Johnson P. V., et al. (2015). Spectroscopy and Viability of Bacillus subtilis Spores after Ultraviolet Irradiation: Implications for the Detection of Potential Bacterial Life on Europa. Astrobiology 15, 20–31. 10.1089/ast.2014.1169 [DOI] [PubMed] [Google Scholar]
  60. Norman L. H. (2011). Is there life on … Titan? Astron. Geophys. 52, 39–31. 10.1111/j.1468-4004.2011.52139.x [DOI] [Google Scholar]
  61. Oremland R., Kulp T., Blum J., Hoeft S., Baesman S., Miller L., et al. (2005). A microbial arsenic cycle in a salt-saturated, extreme environment. Science 308, 1305–1308. 10.1126/science.1110832 [DOI] [PubMed] [Google Scholar]
  62. Pasek M. A., Greenberg R. (2012). Acidification of Europa's Subsurface Ocean as a Consequence of Oxidant Delivery. Astrobiology 12, 151–159. 10.1089/ast.2011.0666 [DOI] [PubMed] [Google Scholar]
  63. Pavlov A., Cheptsov V., Tsurkov D., Lomasov V., Frolov D., Vasiliev G., et al. (2018). Survival of Radioresistant Bacteria on Europa's Surface after Pulse Ejection of Subsurface Ocean Water. Geosciences 9:9 10.3390/geosciences9010009 [DOI] [Google Scholar]
  64. Postberg F., Kempf S., Schmidt J., Brilliantov N., Beinsen A., Abel B., et al. (2009). Sodium salts in E-ring ice grains from an ocean below the surface of Enceladus. Nature 459, 1098–1101. 10.1038/nature08046 [DOI] [PubMed] [Google Scholar]
  65. Postberg F., Khawaja N., Abel B., Choblet G., Glein C. R., Gudipati M. S., et al. (2018). Macromolecular organic compounds from the depths of Enceladus. Nature 558, 564–568. 10.1038/s41586-018-0246-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Schleper C., Puehler G., Holz I., Gambacorta A., Janekovic D., Santarius U., et al. (1995). Picrophilus gen. nov., fam. nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J. Bacteriol. 177, 7050–7059. 10.1128/jb.177.24.7050-7059.1995 [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Schleper C., Puhler G., Klenk H.-P., Zillig W. (1996). Picrophilus oshimae and Picrophilus torridus fam. nov., gen. nov., sp. nov., two species of hyperacidophilic, thermophilic, heterotrophic, aerobic archaea. Int. J. 46, 814–816. 10.1099/00207713-46-3-814 [DOI] [Google Scholar]
  68. Schulze-Makuch D., Grinspoon D. H., Abbas O., Irwin L. N., Bullock M. A. (2004). A sulfur-based survival strategy for putative phototrophic life in the venusian atmosphere. Astrobiology 4, 11–18. 10.1089/153110704773600203 [DOI] [PubMed] [Google Scholar]
  69. Sinha N., Nepal S., Kral T., Kumar P. (2017). Survivability and growth kinetics of methanogenic archaea at various pHs and pressures: implications for deep subsurface life on Mars. Planet. Space Sci. 136, 15–24. 10.1016/j.pss.2016.11.012 [DOI] [Google Scholar]
  70. Smith D. J., Schuerger A. C., Davidson M. M., Pacala S. W., Bakermans C., Onstott T. C. (2009). Survivability of Psychrobacter cryohalolentis K5 under simulated martian surface conditions. Astrobiology 9, 221–228. 10.1089/ast.2007.0231 [DOI] [PubMed] [Google Scholar]
  71. Soderlund K. M., Schmidt B. E., Wicht J., Blankenship D. D. (2014). Ocean-driven heating of Europa's icy shell at low latitudes. Nat. Geosci. 7, 16–19. 10.1038/ngeo2021 [DOI] [Google Scholar]
  72. Sohl F., Solomonidou A., Wagner F. W., Coustenis A., Hussmann H., Schulze-Makuch D. (2014). Structural and tidal models of Titan and inferences on cryovolcanism. J. Geophys. Res. Planets 119, 1013–1036. 10.1002/2013JE004512 [DOI] [Google Scholar]
  73. Spencer J. R., Tamppari L. K., Martin T. Z., Travis L. D. (1999). Temperatures on Europa from Galileo photopolarimeter-radiometer: nighttime thermal anomalies. Science 284, 1514–1516. 10.1126/science.284.5419.1514 [DOI] [PubMed] [Google Scholar]
  74. Suzuki S., Kuenen J. G., Schipper K., Van Der Velde S., Ishii S., Wu A., et al. (2014). Physiological and genomic features of highly alkaliphilic hydrogen-utilizing Betaproteobacteria from a continental serpentinizing site. Nat. Commun. 5:3900. 10.1038/ncomms4900 [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Takai K., Nakamura K., Toki T., Tsunogai U., Miyazaki M., Miyazaki J., et al. (2008). Cell proliferation at 122 C and isotopically heavy CH4 production by a hyperthermophilic methanogen under high-pressure cultivation. Proc. Natl. Acad. Sci. U.S.A. 105, 10949–10954. 10.1073/pnas.0712334105 [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Taubner R. S., Pappenreiter P., Zwicker J., Smrzka D., Pruckner C., Kolar P., et al. (2018). Biological methane production under putative Enceladus-like conditions. Nat. Commun. 9:748. 10.1038/s41467-018-02876-y [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Teolis B. D., Wyrick D. Y., Bouquet A., Magee B. A., Waite J. H. (2017). Plume and surface feature structure and compositional effects on Europa's global exosphere: preliminary Europa mission predictions. Icarus 284, 18–29. 10.1016/j.icarus.2016.10.027 [DOI] [Google Scholar]
  78. Travis B. J., Palguta J., Schubert G. (2012). A whole-moon thermal history model of Europa: impact of hydrothermal circulation and salt transport. Icarus 218, 1006–1019. 10.1016/j.icarus.2012.02.008 [DOI] [Google Scholar]
  79. Vance S. D., Hand K. P., Pappalardo R. T. (2016). Geophysical controls of chemical disequilibria in Europa. Geophys. Res. Lett. 43, 4871–4879. 10.1002/2016GL068547.Received [DOI] [Google Scholar]
  80. Varnes E. S., Jakosky B. M., McCollom T. M. (2003). Biological potential of Martian hydrothermal systems. Astrobiology 3, 407–414. 10.1089/153110703769016479 [DOI] [PubMed] [Google Scholar]
  81. Villarreal M. N., Russell C. T., Luhmann J. G., Thompson W. T., Prettyman T. H., A'Hearn M. F., et al. (2017). The dependence of the cerean exosphere on solar energetic particle events. Astrophys. J. 838:L8 10.3847/2041-8213/aa66cd [DOI] [Google Scholar]
  82. Vu T. H., Hodyss R., Johnson P. V., Choukroun M. (2017). Preferential formation of sodium salts from frozen sodium-ammonium-chloride-carbonate brines – Implications for Ceres' bright spots. Planet. Space Sci. 141, 73–77. 10.1016/j.pss.2017.04.014 [DOI] [Google Scholar]
  83. Waite J. H., Lewis W. S., Magee B. A., Lunine J. I., McKinnon W. B., Glein C. R., et al. (2009). Liquid water on Enceladus from observations of ammonia and40Ar in the plume. Nature 460, 487–490. 10.1038/nature08153 [DOI] [Google Scholar]
  84. Wayne R. P. (2000). Chemistry of Atmospheres, 3rd Edn. Oxford: Clarendon Press. [Google Scholar]
  85. Wordsworth R. (2016). The climate of early mars. Annu. Rev. Earth Planet. Sci. 44, 381–408. 10.1146/annurev-earth-060115-012355 [DOI] [Google Scholar]
  86. Zhu P., Manucharyan G. E., Thompson A. F., Goodman J. C., Vance S. D. (2017). The influence of meridional ice transport on Europa's ocean stratification and heat content. Geophys. Res. Lett. 44, 5969–5977. 10.1002/2017GL072996 [DOI] [Google Scholar]
  87. Zolotov M. Y. (2009). On the composition and differentiation of Ceres. Icarus 204, 183–193. 10.1016/j.icarus.2009.06.011 [DOI] [Google Scholar]
  88. Zolotov M. Y. (2017). Aqueous origins of bright salt deposits on Ceres. Icarus 296, 289–304. 10.1016/j.icarus.2017.06.018 [DOI] [Google Scholar]
  89. Zolotov M. Y., Kargel J. S. (2009). “On the chemical composition of Europa's icy shell, ocean, and underlying rocks,” in Europa, eds Pappalardo R. T., McKinnon W. B., Khurana K. (Tucson, AZ: University of Arizona Press; ), 431. [Google Scholar]
  90. Zolotov M. Y., Tobie G., Postberg F., Magee B., Waite J. H., Esposito L. (2011). Chemical and phase composition of Enceladus: insights from Cassini data. EPSC Abstracts 6:EPSC-DPS2011-1330 10.1029/2011GL047415 [DOI] [Google Scholar]

Articles from Frontiers in Microbiology are provided here courtesy of Frontiers Media SA

RESOURCES