Bacterial Growth in Chloride and Perchlorate Brines: Halotolerances and Salt Stress Responses of<i>Planococcus halocryophilus</i>

Heinz, Jacob; Waajen, Annemiek C.; Airo, Alessandro; Alibrandi, Armando; Schirmack, Janosch; Schulze‐Makuch, Dirk

doi:10.1089/ast.2019.2069

Cited by 38 publications

(51 citation statements)

References 53 publications

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“…In addition, there appears to be no correlation with specific groupings of cations or anions. Each combination of cation and ion (salt) dictates its own growth limit, although there are some general trends, such as perchlorate being more detrimental to growth than the other anions, which agrees with other studies (Heinz et al, 2019).…”

Section: Discussionsupporting

confidence: 91%

A Systematic Study of the Limits of Life in Mixed Ion Solutions: Physicochemical Parameters Do Not Predict Habitability

Stevens

Cockell

2020

Front. Microbiol.

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This study investigated what defines the limits of life in mixed ion solutions. Better understanding these limits should allow us to better predict the habitability of extreme environments on the Earth and extraterrestrial environments. We systematically examined the response of Bacillus subtilis, a well characterized non-halophile model organism, to a range of solutions made from single and mixed salts up to their solubility limits and measured at what concentration growth was arrested, specifically exploring Na, Mg, and Ca cations and Cl, SO 4 , and ClO 4 anions. We measured the physicochemical properties of the solutions to identify which properties correlated with the limits of growth. Individual salts imposed a growth limit specific to the combination of cation and anion, although we generally observe that chloride salts allow growth at lower water activity than sulfate salts, with perchlorate restricting growth even at the highest measured water activity. Growth was limited at a wide range of ionic strength, with no apparently correlation. Despite the theoretically counteracting disordering effects (chaotropic) of perchlorates and ordering effects (kosmotropic) effects of sulfates, when these salts were combined they instead additively narrowed the window for growth in both the Na and Mg cation systems, in the same manner as the combined effects of two chaotropic Ca salts. Our results imply that away from hard limits that might be imposed by physicochemical properties such as water activity, ionic strength or chaotropicity in highly concentrated brines, these properties do not set the limits of life. Instead these limits are highly specific to the salts and organisms in question. This specificity means that the habitability of extreme environments cannot be predicted, even with accurate measurements of the physicochemical conditions present.

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Section: Discussionsupporting

confidence: 91%

A Systematic Study of the Limits of Life in Mixed Ion Solutions: Physicochemical Parameters Do Not Predict Habitability

Stevens

Cockell

2020

Front. Microbiol.

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“…Indeed, dried biofilms of Sphingomonas desiccabilis exposed to brines showed an enhanced resistance compared to hydrated biofilms, suggesting that drying before brining helps protect against brine exposure [50]. On the other hand, both strains CCMEE 171 and CCMEE 029 were killed by the exposure in pure water at 258 K, 233 K and 203 K. This was in line with the observation that freeze-thawing of Planococcus halocryophilus was less lethal in eutectic brines than in salt-free water [42].…”

Section: Discussionsupporting

confidence: 73%

“…Indeed, when exposed to eutectic NaCl solution Planococcus halocryophilus died within two weeks at room temperature; however, it survived at 277 K, an increased survival occurring at 258 K [41]. In addition, the maximum CaCl 2 concentration suitable for its growth increased when the temperature was lowered from 298 K to 277 K [42].…”

Section: Discussionmentioning

confidence: 99%

Survivability of Anhydrobiotic Cyanobacteria in Salty Ice: Implications for the Habitability of Icy Worlds

Cosciotti

Balbi

Ceccarelli

et al. 2019

Life

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Two anhydrobiotic strains of the cyanobacterium Chroococcidiopsis, namely CCMEE 029 and CCMEE 171, isolated from the Negev Desert in Israel and from the Dry Valleys in Antarctica, were exposed to salty-ice simulations. The aim of the experiment was to investigate the cyanobacterial capability to survive under sub-freezing temperatures in samples simulating the environment of icy worlds. The two strains were mixed with liquid solutions having sub-eutectic concentration of Na2SO4, MgSO4 and NaCl, then frozen down to different final temperatures (258 K, 233 K and 203 K) in various experimental runs. Both strains survived the exposure to 258 K in NaCl solution, probably as they migrated in the liquid veins between ice grain boundaries. However, they also survived at 258 K in Na2SO4 and MgSO4-salty-ice samples—that is, a temperature well below the eutectic temperature of the solutions, where liquid veins should not exist anymore. Moreover, both strains survived the exposure at 233 K in each salty-ice sample, with CCMEE 171 showing an enhanced survivability, whereas there were no survivors at 203 K. The survival limit at low temperature was further extended when both strains were exposed to 193 K as air-dried cells. The results suggest that vitrification might be a strategy for microbial life forms to survive in potentially habitable icy moons, for example in Europa’s icy crust. By entering a dried, frozen state, they could be transported from niches, which became non-habitable to new habitable ones, and possibly return to metabolic activity.

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“…It remains unknown which physicochemical parameters of a salt solution have the greatest influence on the survival of P. halocryophilus and whether additional chemical reactivity or biochemical toxicity plays a role. A recent study by Heinz et al (2019) suggests for chloride and perchlorate salt solutions that ion-specific factors of salts have a larger influence on the growth limitation of P. halocryophilus than general physicochemical parameters of the solution, such as water activity or ionic strength. In order to determine whether this applies to other salts, and to establish the relevance of other physicochemical salt parameters, we investigated the influence of a wide range of physicochemical parameters on the survival of P. halocryophilus.…”

Section: Introductionmentioning

confidence: 99%

Physicochemical Salt Solution Parameters Limit the Survival of Planococcus halocryophilus in Martian Cryobrines

et al. 2020

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Microorganisms living in sub-zero environments can benefit from the presence of dissolved salts, as they significantly increase the temperature range of liquid water by lowering the freezing point. However, high concentrations of salts can reduce microbial growth and survival, and can evoke a physiological stress response. It remains poorly understood how the physicochemical parameters of brines (e.g. water activity, ionic strength, solubility and hydration shell strength between the ions and the surrounding water molecules) influence the survival of microorganisms. We used the cryo− and halotolerant bacterial strain Planococcus halocryophilus as a model organism to evaluate the degree of stress different salts assert. Cells were incubated in liquid media at −15 • C containing single salts at eutectic concentrations (CaCl 2 , LiCl, LiI, MgBr 2 , MgCl 2 , NaBr, NaCl, NaClO 4 and NaI). Four of these salts (LiCl, LiI, MgBr 2 and NaClO 4) were also investigated at concentrations with a low water activity (0.635) and, separately, with a high ionic strength (8 mol/L). Water activity of all solutions was measured at −15 • C. This is the first time that water activity has been measured for such a large number of liquid salt solutions at constant sub-zero temperatures (−15 • C). Colony-Forming Unit (CFU) counts show that the survival of P. halocryophilus has a negative correlation with the salt concentration, molecular weight of the anion and anion radius; and a positive correlation with the water activity and anions' hydration shell strength. The survival of P. halocryophilus did not show a significant correlation with the ionic strength, the molecular weight of the cation, the hydrated and unhydrated cation and hydrated anion radius, and the cations' hydration bond length. Thus, the water activity, salt concentration and anion parameters play the largest role in the survival of P. halocryophilus in concentrated brines. These findings improve our understanding of the limitations of microbial life in saline environments, which provides a basis for better evaluation of the habitability of extraterrestrial environments such as Martian cryobrines.

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Bacterial Growth in Chloride and Perchlorate Brines: Halotolerances and Salt Stress Responses ofPlanococcus halocryophilus

Cited by 38 publications

References 53 publications

A Systematic Study of the Limits of Life in Mixed Ion Solutions: Physicochemical Parameters Do Not Predict Habitability

A Systematic Study of the Limits of Life in Mixed Ion Solutions: Physicochemical Parameters Do Not Predict Habitability

Survivability of Anhydrobiotic Cyanobacteria in Salty Ice: Implications for the Habitability of Icy Worlds

Physicochemical Salt Solution Parameters Limit the Survival of Planococcus halocryophilus in Martian Cryobrines

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