ASTROBIOLOGY

Volume 16, Number 2, 2016

Mary Ann Liebert, Inc.
DOI: 10.1089/ast.2015.1380

The Last Possible Outposts for Life on Mars

Alfonso F. Davila1,2 and Dirk Schulze-Makuch3,4

Abstract

The evolution of habitable conditions on Mars is often tied to the existence of aquatic habitats and largely
constrained to the first billion years of the planet. Here, we propose an alternate, lasting evolutionary trajectory
that assumes the colonization of land habitats before the end of the Hesperian period (ca. 3 billion years ago) at a
pace similar to life on Earth. Based on the ecological adaptations to increasing dryness observed in dryland
ecosystems on Earth, we reconstruct the most likely sequence of events leading to a late extinction of land
communities on Mars. We propose a trend of ecological change with increasing dryness from widespread edaphic
communities to localized lithic communities and finally to communities exclusively found in hygroscopic sub-
strates, reflecting the need for organisms to maximize access to atmospheric sources of water. If our thought
process is correct, it implies the possibility of life on Mars until relatively recent times, perhaps even the present.
Key Words: Life—Mars—Evolution—Desert—Land ecosystems—Deliquescence. Astrobiology 16, 159–168.

1. Introduction sources of water. The possibility of life in the deep sub-

surface is not discussed.
H abitability models of Mars often tie the potential for
life to the existence of aquatic habitats such as lakes or
oceans (e.g., McKay and Davis, 1991). Along these lines,
2. The Colonization of Land
current and planned robotic missions mainly focus on the The three domains of life on Earth contain both aquatic
study of sedimentary deposits formed in aquatic environ- and terrestrial groups, but among the prokaryotes there
ments billions of years ago. The discovery of ancient lake appears to be a major evolutionary group with a common
sediments deposited in a geochemical environment compat- ancestor on land, the so-called Terrabacteria, which in-
ible with life (Grotzinger et al., 2014), together with the cludes members of the cyanobacteria, the Gram-positive
certainty that such environments were widespread during the phyla, and the Chloroflexi and Deinococcus-Thermus
Noachian and Hesperian periods (e.g., Bibring et al., 2006; (Battistuzzi and Hedges, 2009). Representatives of this
Mustard et al., 2008; Ehlmann and Edwards, 2014), has so far group possess specific adaptations to land environments
validated this strategy. such as resistance to desiccation, high salinity, and high
However, this vision of habitability is incomplete, and UV radiation. Phylogenetic, cytological, and environmen-
the above paradigm ought to be reconsidered because the tal data suggest that the Terrabacteria and Hydrobacteria
fate of an early martian biosphere was not necessarily tied could have diverged as early as 3.54 Ga (Battistuzzi and
to the duration of aquatic habitats. An alternative evolu- Hedges, 2009), relatively fast after the origin of life. To
tionary trajectory would have opened with the colonization date, possible evidence of land ecosystems have been
of land, at which point a portion of the martian biosphere found in late Mesoproterozoic to early Neoproterozoic
would have become dependent solely on atmospheric paleosols (ca. 1.2–1 billion years ago) (Prave, 2002) in
sources of water. In this synthesis paper, we consider this 2.9–2.7 billion-year-old ephemeral ponds (Rye and Hol-
second trajectory by addressing two aspects of the prob- land, 2000) and alluvial sequences, some of which bear
lem: (1) the probability that early life on Mars would have microfossils (Hallbauer and van Warmelo, 1974; Mossman
colonized land and (2) land ecosystems’ response to in- et al., 2008), and in paleosols that formed between 2.7 and
creasing dryness. We focus our analysis on forms of life 2.6 billion years ago (Watanabe et al., 2000). Considering
on, or near, the surface that ultimately rely on atmospheric that the geological record of land environments is sparse,
1
Carl Sagan Center at the SETI Institute, Mountain View, California, USA.
2
NASA Ames Research Center, Moffett Field, California, USA.
3
School of the Environment, Washington State University, Pullman, Washington, USA.
4
Center of Astronomy and Astrophysics, Technical University Berlin, Berlin, Germany.
ª Alfonso F. Davila and Dirk Schulze-Makuch, 2016; Published by Mary Ann Liebert, Inc. This Open Access article is distributed under
the terms of the Creative Commons Attribution Noncommercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits
any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

159
160 DAVILA AND SCHULZE-MAKUCH

the colonization of land might have occurred earlier than need of organisms to maximize exposure to liquid water
what the fossil record suggests. during sporadic wet events.
Resistance to desiccation, high salinity, and UV radiation, Many desert organisms are capable of desiccation toler-
the trademarks of the Terrabacteria, are also survival ad- ance, the ability to dry up without dying (Potts, 1994; Al-
aptations of aquatic microorganisms in coastal areas, such as pert, 2005) and to resume metabolic activity quickly after
those that inhabit benthic mats periodically exposed to air- rehydration, even after years of complete desiccation (e.g.,
drying and UV radiation during cycles of evaporation and Potts, 1994; Proctor et al., 2007). In arid regions, these
flooding (e.g., Garcia-Pichel, 1998; Pattanaik et al., 2007; poikilohydric microorganisms colonize the top few centi-
Beraldi-Campesi, 2013). Perhaps not surprisingly, the cya- meters of soil and rock substrates between a patchy vege-
nobacteria, a deeply rooted taxonomic group often found in tation cover (Belnap and Lange, 2003; Pointing and Belnap,
aquatic environments, include some of the most desiccation- 2012), and relatively complex microbial communities lar-
resistant organisms known, which are adapted to survive in gely sustained by phototrophic organisms can develop as
the driest regions on Earth (Friedmann, 1980; Friedmann biological soil crusts (BSC) (Fig. 1A). In arid deserts, BSC
and Ocampo-Friedmann, 1995; Warren-Rhodes et al., 2006; can cover up to 70% of the total soil surface (Belnap and
Pointing and Belnap, 2012; Wierzchos et al., 2012b). The Lange, 2003), leading to relatively high concentrations of
above suggests that the colonization of land could be a rela- organic carbon (OC) that is recycled relatively fast, within
tively straightforward evolutionary step once aquatic habitats decades to several centuries (Amundson, 2001).
are established. However, a significant ecological collapse occurs in soils
On Mars, the established existence of aquatic habitats at the transition from arid to hyperarid conditions (Fig. 2).
during the late Noachian about 3.8 billion years ago (Grot- This transition signals a dramatic reduction in vegetation
zinger et al., 2014) and the inferred existence of aquatic en- cover, which becomes almost entirely confined to ephemeral
vironments at the end of the Hesperian ca. 3 billion years ago runoff channels (washes) and episodic and transient blooms
(McKay and Davis, 1991), together with the cumulative ev- that follow rare rainfall events. Biological soil crusts in
idence of episodic aquatic environments during the Early hyperarid soils become increasingly fragmented or patchy,
Amazonian (Fairén et al., 2009; Rodrı́guez et al., 2014, 2015), and there is a significant decline of both cell abundance and
suggest that an early martian biosphere could have had suf- species richness (Pointing et al., 2007; Pointing and Belnap,
ficient time to colonize land, assuming a similar pace of 2012; Crits-Christoph et al., 2013). Soil microbial commu-
colonization as life on Earth. But contrary to Earth, most of nities and BSC in both temperate and cold hyperarid envi-
the surface of Mars was emerged land even when liquid water ronments become discontinuous and are gradually replaced
was abundant (Carr and Head, 2015). The inferred existence by regolith and desert pavements (Pointing and Belnap,
of tens of thousands of crater lakes in the martian southern 2012; Colesie et al., 2013). This is reflected in the distri-
highlands, and possibly a large northern ocean, implies a bution of soil OC and biomass (Fig. 2B), which fall to the
potentially large net shoreline area with shallow aquatic en- lowest levels found anywhere on Earth (ca. 103 to 105 cells
vironments that could have propelled the emergence of land g-1 soil), concurrent with an increase in mean residence time
microorganisms. The absence of a magnetic field since the of soil OC to tens of thousands of years (Ewing et al., 2008).
late Noachian (Acuna et al., 1998; Carr and Head, 2010) In these hyperarid environments, soil communities are
along with the continued decline in atmospheric pressure in largely replaced by rock-inhabiting (lithobiontic) commu-
the first 2 billion years (Lammer et al., 2013) would have nities (e.g., Friedmann, 1980; Pointing and Belnap, 2012;
exerted strong selective pressures on martian organisms to Wierzchos et al., 2012b). Lithobiontic communities com-
adapt to desiccation, UV radiation, and high salinity, thus prise epilithic microorganisms that colonize the surface of
paving the way for the colonization of land. After the colo- rocks, hypolithic microorganisms that colonize the under-
nization of land, long-term habitability on Mars would no side of translucent substrates such as quartz rocks and
longer have been tied to the existence of aquatic environments gypsum crusts (Fig. 1C), and endolithic microorganisms that
but to atmospheric sources of water. This could have signif- colonize the interior of porous substrates such as sandstone
icantly expanded the martian habitability window beyond the rocks and salt crusts (Fig. 1D). The colonization of lithic
Hesperian period. substrates is a direct response to water deficit. Hypolithic
and endolithic habitats extend the range of conditions under
which liquid water can occur, and at the same time, surface
3. Ecological Transitions in Dryland Ecosystems
tensions in the rock matrix slow the evaporation of water
Important lessons regarding the possible adaptations of and thus prolong access to moisture after a wetting event.
land ecosystems to increasing dryness can be learned from This is critical for microbial communities whose long-term
the study of life in dryland environments on Earth. Drylands survival hinges on their capacity to sustain a net positive
are one of the largest terrestrial biomes, and more than 35% of carbon balance in the course of repeated cycles of wetting
Earth’s land mass is permanently or seasonally arid (Pointing and drying (Alpert and Oechel, 1985; Friedmann et al.,
and Belnap, 2012). Dryland ecosystems encompass a broad 1993; Coe et al., 2012). In temperate deserts, this is not
hydrological range, typically measured as the Aridity Index trivial, because liquid water often occurs during the night,
(AI), defined as the ratio of mean annual precipitation to when respiration, but not photosynthesis, can occur. The net
potential evapotranspiration. Based on the AI scale, drylands flux of CO2 is negative in these first hours of dark metabolic
are categorized as semiarid (0.20 < AI <0.50), arid (0.05 < AI activity and can only be balanced via photosynthesis if water
<0.20), and hyperarid (AI <0.05). Research conducted over still persists in the early morning (Noy-Meir, 1973; Alpert
the past 40 years suggests that there is a predictable pathway and Oechel, 1985; Alpert, 2005). Due to their water reten-
of ecological change with increasing dryness, driven by the tion, lithic substrates expand the window for photosynthesis
THE LAST OUTPOSTS FOR LIFE ON MARS 161

FIG. 1. Successions of dryland ecosystems with increasing dryness. (A) Vegetated arid site in the Mojave Desert, with a
continuous cover of BSC. (B) Nonvegetated hyperarid site in the Atacama Desert devoid of BSC. (C) Hypolithic microbial
community under a translucent quartz stone in the hyperarid Namib Desert. (D) Microbial community inside a hygroscopic
salt crust in the hyperarid core of the Atacama Desert. Black arrows in A and B point to features of similar size, for scale.
(Color graphics available at www.liebertonline.com/ast)

in the morning and enable the communities to balance res- the coldest and driest valleys the endolithic colonies are lar-
piration with carbon fixation. The protected lithic microen- gely fossilized (Friedmann et al., 1994; Wierzchos et al.,
vironment also provides shelter against erosion and wind, 2004, 2005; Sun, 2013). A similar trend of extinction is ob-
amelioration of extreme temperature changes, and shielding served in hypolithic habitats with decreasing rainfall in hy-
against UV radiation (Friedmann, 1980). Colonized lithic perarid deserts. Hypolithic colonization of translucent rocks
habitats are found in all deserts, including regions once is typically 100% (i.e., all suitable rocks are colonized) in
considered to be too dry for life (Friedmann, 1982; Warren- semiarid regions, dropping to <50% in arid areas and to <1%
Rhodes et al., 2006; Wierzchos et al., 2006, 2012b; Pointing in hyperarid regions, where the hypolithic habitat becomes
et al., 2009; Cary et al., 2010; Khan et al., 2011; Pointing practically nonexistent (Warren-Rhodes et al., 2006, 2007)
and Belnap, 2012). Despite the diversity of lithic habitats (Fig. 2A) except in local areas of recurrent fog (Azúa-Bustos
and the broad range of dryland environments where they are et al., 2011). The disappearance of hypolithic colonies with
found, community structure in hypolithic and endolithic diminishing rainfall is mirrored by epilithic lichens (Wierz-
habitats is remarkably similar, although the composition of chos et al., 2011), despite the fact that some can supplement
the community might be very different (Pointing et al., liquid water with water vapor and restore photosynthesis with
2007). A key concept with regard to lithic habitats is that the high (>75%) humidity only (Lange, 1993).
physical properties of the substrate generate local habitable At the driest end of hyperaridity, where soils and most
conditions in environments that might otherwise be too lithic substrates can no longer sustain active biology (e.g.,
harsh for life (Friedmann and Ocampo-Friedmann, 1984). Warren-Rhodes et al., 2006; Ewing et al., 2008; Crits-
Yet there are also trends of extinction within lithic habitats Christoph et al., 2013), relatively complex and abundant
with increasing dryness. For example, in the Dry Valleys of communities of autotrophic and heterotrophic bacteria and
Antarctica endolithic microbial communities are found pri- archaea (de los Rı́os et al., 2010; Robinson et al., 2015) are
marily in the interior of south-facing sandstone rocks and still found inside porous, hygroscopic salt crusts (Wierzchos
cliffs, where microorganisms take advantage of meager et al., 2006) (Fig. 1D). The communities inside the salt
snowmelt that percolates into the rock during warm summer nodules use liquid brines that form in the interior of the salt
days (Friedmann, 1982; McKay and Friedmann, 1985). substrate from the vapor phase via deliquescence and cap-
However, the sandstone endolithic community in the Dry illary condensation (Davila et al., 2008, 2013; Wierzchos
Valleys appears to be at the brink of extinction, and in some of et al., 2012a). Because the salt substrate retains water
162 DAVILA AND SCHULZE-MAKUCH

FIG. 2. (A) Percent vegetation cover (dots) and percent hypolithic colonization (squares) as a function of aridity (ex-
pressed as AI). Blue dots are actual field observations (data from Delgado-Baquerizo et al., 2013). Orange dots are from
satellite data. Percent hypolithic colonization data was obtained from Allen (1997), Warren-Rhodes et al. (2006, 2007,
2013), Khan et al. (2011), Al-Thani (2014) and references therein. (B) Soil OC concentration as a function of aridity (data
from Delgado-Baquerizo et al., 2013).

efficiently, cyanobacteria inside the salt nodules can fix CO2 First, relatively diverse microbial communities would
for days after a wetting event (Davila et al., 2015), and the have been widespread in the top centimeters of the regolith,
community is capable of carbon cycling rates in timescales with metabolic cycles tuned to episodes of rainfall, dew,
of decades (Ziolkowski et al., 2013) even in the absence fog, snow, or glacier melt. Pigmentation and community
of atmospheric precipitation. Such deliquescent substrates structure could be adequate solutions for UV protection, and
provide a minimalistic habitat for survival under extremely proximity to the surface would have granted access to
dry conditions, and in the driest place on Earth they likely sunlight and an abundant carbon source in the atmosphere.
represent the last available habitat for life. These communities would likely be comprised of poikilo-
hydric organisms capable of desiccation tolerance, analo-
gous to BSC and soil bacteria found in terrestrial arid deserts
4. The Late-Stage Evolution of Land
and in permafrost in polar regions. Other possible early land
Ecosystems on Mars
habitats could have been seasonal or perennial snow banks,
The transition from widespread edaphic communities to debris-rich glacier ice, ice-bearing permafrost ( Jakosky
localized lithic communities and finally to communities ex- et al., 2003; Córdoba-Jabonero et al., 2005; McKay et al.,
clusively found in hygroscopic substrates reflects the need for 2013), or protected habitats near the surface such as caves
land organisms to maximize access to atmospheric sources (Boston et al., 2011; Northup et al., 2011).
of water. We propose that, if life colonized martian land, a With increasing dryness, regolith communities would have
similar sequence of ecological transitions would have oc- become discontinuous and gradually replaced by desert
curred as the planet became increasingly dry (Fig. 3). pavements. Wind erosion or dust deposition would have
THE LAST OUTPOSTS FOR LIFE ON MARS 163

FIG. 3. Proposed sequence of ecological transitions on Mars with increasing dryness, assuming an early colonization of
land. After the disappearance of aquatic environments, land habitats (edaphic, lithic, and lastly hygroscopic) would still be
available, based on different sources of atmospheric water. (Color graphics available online at www.liebertonline.com/ast)

slowly erased any surface expression of such communities pressure to colonize lithic habitats ought to be independent of
through dispersal or burial, although transient climate ex- sources of energy and nutrients and instead should apply to
cursions toward wetter conditions, driven for example by forms of life that rely on atmospheric sources of water.
orbital fluctuations, could have reactivated the regolith Finally, the last habitat for life near the surface would have
communities for relatively short periods. At this point, long- been the interior of hygroscopic salt crusts, which could
term active metabolism would have been largely constrained trigger the condensation of liquid water via deliquescence at
to lithobiontic communities, both in hypolithic and endolithic relative humidity (RH) conditions well below the atmo-
habitats selected based upon certain physical properties of spheric condensation point. At the same time, the deliques-
the rock substrate, such as color, opacity, size, and porosity cent brines would have acted as antifreeze, depressing the
(e.g., Friedmann and Koriem, 1989; McKay et al., 1992). If freezing point of water, and the interior of the salt substrate
members of these lithic communities were light-dependent, would have provided shelter against UV radiation. Analogues
relatively translucent rocks such as sandstone, calcite, ig- of such salt communities would be the endolithic communi-
nimbrite, gypsum, quartz, or dolomite would have been ties found in fossil salars in the hyperarid core of the Atacama
suitable for colonization, such as is observed in practically all Desert (Wierzchos et al., 2006; Davila et al., 2010).
deserts on Earth (Friedmann, 1982; Friedmann and Ocampo- The proposed sequence of ecological transitions with in-
Friedmann, 1984; Wierzchos et al., 2011, 2013; Pointing and creasing dryness is based on global trends observed in both
Belnap, 2012; DiRuggiero et al., 2013). In the case of light- hot and cold deserts on Earth. Our analysis does not pre-
independent communities, other lithic substrates might have clude the existence today, or in the recent past, of special-
been available, such as opaque rocks. Yet the strong selective ized habitats typical of polar desert environments, such as
164 DAVILA AND SCHULZE-MAKUCH

debris-rich ice ( Jakosky et al., 2003; Córdoba-Jabonero et al., 1995), and there could be >1000 pr-lm of atmospheric
2005; McKay et al., 2013), but such habitats would require water at midlatitudes and low latitudes during recent high-
local sources of water and are constrained to high latitudes, obliquity (i.e., 45) periods ( Jakosky and Carr, 1985). In
which are permanently cold, an additional constraint to life. comparison, the median column of PWV above the Andean
plateau in the Atacama Desert is approximately 1200 pr-lm
at an elevation of 5000 m (Giovanelli et al., 2001; Tremblin
5. Implications for Recent Martian Habitability
et al., 2012), equivalent to the PWV in the hyperarid core of
If hygroscopic habitats such as those found in the Ata- the desert where deliquescence-driven microbial ecosystems
cama Desert represent the last possible outposts for life are found. For completeness, we note that the lowest PWV
under extremely dry conditions, then we can use them to reported so far on our planet is near the South Pole and
approximate the last time when Mars might have been a ranges between 100 and 800 pr-lm, with minimum annual
habitable planet. values as low as 30 pr-lm (Buravo et al., 1986; Chamber-
The habitability of hygroscopic salt crusts depends criti- lain et al., 2000). Hence, as a first approximation the water
cally on the abundance of water in the atmosphere and in the abundance in the present-day martian atmosphere is lower
nature of the salt substrate, which determines its deliques- than in the driest regions on Earth by a factor of 10–100, but
cence properties and the eutectic temperature and water during high obliquity it is comparable to levels measured
activity of the deliquescence solution (Davila et al., 2010). in the hyperarid core of the Atacama Desert. Assuming—
Water activity is the relevant parameter that links liquid rather arbitrarily—that a PWV of 1000 pr-lm represents the
water and habitability. Assuming long-term equilibrium minimum atmospheric water abundance that can sustain
conditions and the average temperature and RH on the deliquescence-driven microbial ecosystems, the abundance
martian surface, the water activity of an aqueous solution of water on a comparison of the martian surface to the driest
on present-day Mars should fall well below the conditions deserts on Earth suggests that the habitability window in
for habitability for any terrestrial organisms (e.g., Kminek this type of substrate might have closed relatively recently,
et al., 2010; Rummel et al., 2014). However, for a more perhaps during the late Amazonian, or it may possibly still
precise assessment of habitability we must consider that the be open.
planet is not in equilibrium and determinations of water
activity need to be done at the scale of the environment 6. Conclusions
experienced by microorganisms, where environmental con-
ditions can depart significantly from the average (McKay Currently, the search for ancient aqueous environments as
and Friedmann, 1985; Nienow et al., 1988a, 1988b; Davila repositories of possible evidence of life is the primary focus
et al., 2008; Wierzchos et al., 2012a; Meckenstock et al., of robotic missions to Mars. However, the colonization of
2014). Temperature and RH fluctuations on Mars could land by putative martian microorganisms could have opened
promote transient deliquescence inside salt crusts with low a lasting evolutionary trajectory for life independent of
eutectic points (Chevrier et al., 2009; Davila et al., 2010; aquatic habitats. The ecological transitions that occur in
Martı́n-Torres et al., 2015). For salt with very low eutectic Earth’s deserts with increasing dryness can inform us as to
points such as perchlorate, the water activity of the resulting where the last martian near-surface ecosystems may have
transient solution—in addition to its temperature—would existed or still exist. In analogy with terrestrial dryland
still fall below the known threshold for growth, but other ecosystems, the physical properties of habitats with regard
salts such as NaCl would produce more benign deliquescent to water retention, rather than the physiological adaptations
brines. These examples serve to illustrate the limitations that of microorganisms, could have directed the late-stage evo-
arise when assessing habitability assuming only large-scale lution of life on Mars. As is the case for Earth’s driest
equilibrium conditions. regions, the last possible sources of water for life on Mars
A comparison of the abundance of atmospheric water on would have been the deliquescence of hygroscopic salt
Mars and in the driest regions on Earth might give an idea of crusts, and this window of habitability might have closed
how prevalent and intense deliquescent events might be on relatively recently or may still be open. As such, and in
the planet. Most of the martian water inventory is seques- retrospect, dry regolith samples analyzed by the Viking
tered in the polar layered terrains and in the near-surface landers might not have been the best substrates to search for
regolith at latitudes above 30–40 (e.g., Head et al., 2003; active (or extinct) biology. Future robotic missions would be
Feldman, 2004; Byrne et al., 2009; Carr and Head, 2010; advised to prioritize the study of lithic substrates.
Kadish and Head, 2011). The median column of precipitable
water vapor (PWV) is between <3 and 100 precipitable Acknowledgments
micrometers (pr-lm) planetwide ( Jakosky and Farmer, A.F.D. acknowledges funding from the NASA Exobiol-
1982; Haberle et al., 2001). Climate simulations predict that ogy Program (Grant NNX12AD61G) and the NASA As-
increased polar summer insolation during high obliquity trobiology Institute (NAI Grant NNX15BB01A to the SETI
leads to a water cycle that is much more intense than to- Institute). D.S.M. acknowledges funding for this work from
day’s, with a column water abundance up to 3000 pr-lm ERC Advanced Grant 339231. We thank Kim Warren-
above the northern polar cap around summer solstice and Rhodes, Chris McKay, and Henry Sun for helpful discus-
about 50 pr-lm in the summer tropics ( Jakosky and Carr, sions and for providing some of the images in Fig. 1.
1985; Forget et al., 2006). Assuming an average obliquity of
40 during the last 3 billion years, the long-term water
Author Disclosure Statement
content of the lower atmosphere could be 2 orders of
magnitude higher than it is at present (Mellon and Jakosky, No competing financial interests exist.
THE LAST OUTPOSTS FOR LIFE ON MARS 165

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endolithic life in the hyperarid core of the Atacama Desert. BSC ¼ biological soil crusts
Biogeosciences 9:3071–3098. OC ¼ organic carbon
Wierzchos, J., de los Rı́os, A., and Ascaso, C. (2012b) Micro- PWV ¼ precipitable water vapor
organisms in desert rocks: the edge of life on Earth. Int Mi- RH ¼ relative humidity
crobiol 15:173–183.