A New Analysis of Mars “Special Regions”: Findings of the Second MEPAG Special Regions Science Analysis Group (SR-SAG2)

Rummel, John D.; Beaty, D. W.; Jones, Melissa A.; Bakermans, Corien; Barlow, N. G.; Boston, Penelope J.; Chevrier, V. F.; Clark, B. C.; Vera, Jean Pierre Paul de; Gough, R. V.; Hallsworth, John E.; Head, J. W.; Hipkin, V.; Kieft, Thomas L.; McEwen, A. S.; Mellon, M. T.; Mikucki, Jill A.; Nicholson, Wayne L.; Omelon, Christopher R.; Peterson, Ronald C.; Roden, Eric E.; Lollar, Barbara Sherwood; Tanaka, Kenneth L.; Viola, D.; Wray, J. J.

doi:10.1089/ast.2014.1227

Cited by 337 publications

(258 citation statements)

References 565 publications

(586 reference statements)

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“…The physicochemical boundaries beyond which multiplication of all microorganisms is prevented are imposed by low water activity, extremes of temperature (approximately Ϫ20 to 120°C), and other situations, including high pH (Ͼ12), chaotropicity, and oxidative damage (e.g., due to UV radiation) (8)(9)(10). The stress mechanism for a number of these parameters involves changes in the entropic status of lipid bilayers and other macromolecular systems (see reference 9 and citations therein).…”

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confidence: 99%

Reduction of the Temperature Sensitivity of Halomonas hydrothermalis by Iron Starvation Combined with Microaerobic Conditions

Harrison

Hallsworth

Cockell

2015

Appl Environ Microbiol

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bThe limits to biological processes on Earth are determined by physicochemical parameters, such as extremes of temperature and low water availability. Research into microbial extremophiles has enhanced our understanding of the biophysical boundaries which define the biosphere. However, there remains a paucity of information on the degree to which rates of microbial multiplication within extreme environments are determined by the availability of specific chemical elements. Here, we show that iron availability and the composition of the gaseous phase (aerobic versus microaerobic) determine the susceptibility of a marine bacterium, Halomonas hydrothermalis, to suboptimal and elevated temperature and salinity by impacting rates of cell division (but not viability). In particular, iron starvation combined with microaerobic conditions (5% [vol/vol] O 2 , 10% [vol/vol] CO 2 , reduced pH) reduced sensitivity to temperature across the 13°C range tested. These data demonstrate that nutrient limitation interacts with physicochemical parameters to determine biological permissiveness for extreme environments. The interplay between resource availability and stress tolerance, therefore, may shape the distribution and ecology of microorganisms within Earth's biosphere. Knowledge of the physical and/or chemical parameters that can limit cell division and metabolic activity is of critical importance in fields such as ecology, agriculture, food preservation, biotechnology, and astrobiology (1-7). The physicochemical boundaries beyond which multiplication of all microorganisms is prevented are imposed by low water activity, extremes of temperature (approximately Ϫ20 to 120°C), and other situations, including high pH (Ͼ12), chaotropicity, and oxidative damage (e.g., due to UV radiation) (8-10). The stress mechanism for a number of these parameters involves changes in the entropic status of lipid bilayers and other macromolecular systems (see reference 9 and citations therein). Others, including the reactive oxygen species generated by UV radiation, act by inducing alterations in the primary structure of cellular macromolecules (11). One of the primary effects of extreme pH is the breakdown of electrochemical (and other) gradients across the plasma membrane (12).An increasing body of evidence suggests that it is frequently the net effect of diverse stress parameters that defines the boundary space for life (8,(13)(14)(15)(16)(17)(18). The sea ice bacterium Shewanella gelidimarina, for example, has been shown to exhibit an increased temperature range for cell division when cultured at high (NaCl) salinity, with increases in membrane lipid packing and fatty acid content conferring tolerance of both conditions (13). Other solutes (including MgCl 2 ) have also been found to influence the temperature limits for microbial multiplication (15, 17). Moreover, adaptation to high hydrostatic pressure has been proposed as a mechanism that enables bacterial multiplication within hypersaline deep-sea environments (14). Such interactions between st...

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confidence: 99%

Reduction of the Temperature Sensitivity of Halomonas hydrothermalis by Iron Starvation Combined with Microaerobic Conditions

Harrison

Hallsworth

Cockell

2015

Appl Environ Microbiol

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“…Second, man-made LP environments (e.g., hypobaric chambers at pressures of ϳ2 kPa) have proven useful for the long-term storage of high-value agricultural commodities, partly due to LP inhibition of the growth of spoilage microorganisms (6). Third, considerable effort is currently being devoted to the study of the biology of the extraterrestrial environment of Mars, which features an LP atmosphere ranging from ϳ0.1 kPa to ϳ1 kPa; in this context, LP microbiology is important both for life detection and for planetary protection purposes (7).…”

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confidence: 99%

Experimental Evolution of Enhanced Growth by Bacillus subtilis at Low Atmospheric Pressure: Genomic Changes Revealed by Whole-Genome Sequencing

Waters

Zeigler

Nicholson

2015

Appl Environ Microbiol

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Knowledge of how microorganisms respond and adapt to low-pressure (LP) environments is limited. Previously, Bacillus subtilis strain WN624 was grown at the near-inhibitory LP of 5 kPa for 1,000 generations and strain WN1106, which exhibited increased relative fitness at 5 kPa, was isolated. Genomic sequence differences between ancestral strain WN624 and LP-evolved strain WN1106 were identified using whole-genome sequencing. LP-evolved strain WN1106 carried amino acid-altering mutations in the coding sequences of only seven genes (fliI, parC, ytoI, bacD, resD, walK, and yvlD) and a single 9-nucleotide in-frame deletion in the rnjB gene that encodes RNase J2, a component of the RNA degradosome. By using a collection of frozen stocks of the LP-evolved culture taken at 50-generation intervals, it was determined that (i) the fitness increase at LP occurred rapidly, while (ii) mutation acquisition exhibited complex kinetics. A knockout mutant of rnjB was shown to increase the competitive fitness of B. subtilis at both LP and standard atmospheric pressure. Microorganisms exhibit an ability to survive and even thrive in a wide range of harsh environments on Earth, which feature extremes of fundamental physical parameters such as temperature and pressure (1). Organisms able to grow at extremely high temperatures (i.e., thermophiles) or low temperatures (i.e., psychrophiles) have been studied extensively (1), as well as organisms capable of growth at high pressure (HP) (i.e., piezophiles) (1, 2). In sharp contrast, our understanding is extremely limited concerning microbial survival, adaptation, and growth in low-pressure (LP) environments. In part, this reflects a relative scarcity of LP environments on the Earth's surface; the atmospheric pressure at sea level averages ϳ101.3 kPa, and the lowest average terrestrial barometric pressure is ϳ34 kPa, atop Mount Everest. However, there has been a recent upsurge of interest in studying the response of microbes to LP exposure. First, Earth's upper atmosphere is a global LP environment that poses unique challenges to microbial survival and growth; for example, 5 kPa of pressure corresponds to an altitude of ϳ19 km, in the lower stratosphere (3-5). Second, man-made LP environments (e.g., hypobaric chambers at pressures of ϳ2 kPa) have proven useful for the long-term storage of high-value agricultural commodities, partly due to LP inhibition of the growth of spoilage microorganisms (6). Third, considerable effort is currently being devoted to the study of the biology of the extraterrestrial environment of Mars, which features an LP atmosphere ranging from ϳ0.1 kPa to ϳ1 kPa; in this context, LP microbiology is important both for life detection and for planetary protection purposes (7).To understand how microbes respond and adapt to LP, we previously reported an evolution experiment in which Bacillus subtilis ancestral strain WN624 was propagated in liquid LB medium for 1,000 generations at an LP of 5 kPa; during this experiment, an enhanced growth capability evolved in the cultur...

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“…Mars has been considered in much earlier times (Herschel 1784) and one of the co-founders of the theory of evolution (Wallace 1907) declared that Mars would be devoid of life. This issue has been discussed in depth in a recent review (Rummel et al 2014). The main conclusion concerning the potential for life on Mars stated in that review was that it was "..… determined by locations where both of the parameters (without margins added) of temperature (above 255°K) and water activity (relative humidity > 60%) are attained.…”

Section: Introductionmentioning

confidence: 99%

The fate of proteins in outer space

Seddon

Bywater

2015

International Journal of Astrobiology

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It is well established that any properly conducted biophysical studies of proteins must take appropriate account of solvent. For water-soluble proteins it has been an article of faith that water is largely responsible for stabilizing the fold, a notion that has recently come under increasing scrutiny. Further, there are some instances when proteins are studied experimentally in the absence of solvent, as in matrix-assisted laser desorption/ionization or electrospray mass spectrometry, for example, or in organic solvents for protein engineering purposes. Apart from these considerations, there is considerable speculation as to whether there is life on planets other than Earth, where conditions including the presence of water (both in liquid or vapor form and indeed ice), temperature and pressure may be vastly different from those prevailing on Earth. Mars, for example, has only 0.6% of Earth's mean atmospheric pressure which presents profound problems to protein structures, as this paper and a large corpus of experimental work demonstrate. Similar objections will most likely apply in the case of most exoplanets and other bodies such as comets whose chemistry and climate are still largely unknown.This poses the question, how do proteins survive in these different environments? In order to cast some light on these issues we have conducted a series of molecular dynamics simulations on protein dehydration under a variety of conditions. We find that, while proteins undergoing dehydration can retain their integrity for a short duration they ultimately become disordered, and we further show that the disordering can be retarded if superficial water is kept in place on the surface. These findings are compared with other published results on protein solvation in an astrobiological and astrochemical setting. Inter alia, our results suggest that there are limits as to what to expect in terms of the existence of possible extraterrestrial forms as well to what can be achieved in experimental investigations on living systems despatched from Earth. This finding may appear to undermine currently held hopes that life will be found on nearby planets, but it is important to be aware that the presence of ice and water are by themselves not sufficient; there has to be an atmosphere which includes water vapor at a sufficiently high partial pressure for proteins to be active. A possible scenario in which there has been a history of adequate water vapor pressure which allowed organisms to prepare for a future dessicated state by forming suitable protective capsules cannot of course be ruled out.

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A New Analysis of Mars “Special Regions”: Findings of the Second MEPAG Special Regions Science Analysis Group (SR-SAG2)

Cited by 337 publications

References 565 publications

Reduction of the Temperature Sensitivity of Halomonas hydrothermalis by Iron Starvation Combined with Microaerobic Conditions

Reduction of the Temperature Sensitivity of Halomonas hydrothermalis by Iron Starvation Combined with Microaerobic Conditions

Experimental Evolution of Enhanced Growth by Bacillus subtilis at Low Atmospheric Pressure: Genomic Changes Revealed by Whole-Genome Sequencing

The fate of proteins in outer space

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