NaCl-saturated brines are thermodynamically moderate, rather than extreme, microbial habitats

Callum J D Lee, Phillip E McMullan, Callum J O'Kane, Andrew Stevenson, Inês C Santos, Chayan Roy, Wriddhiman Ghosh, Rocco L Mancinelli, Melanie R Mormile, Geoffrey McMullan, Horia L Banciu, Mario A Fares, Kathleen C Benison, Aharon Oren, Mike L Dyall-Smith, John E Hallsworth

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

NaCl-saturated brines such as saltern crystallizer ponds, inland salt-lakes, deep-sea brines, and liquids-of-deliquescence on halite are commonly regarded as a paradigm for the limit-of-life on Earth. There are, however, other habitats that are thermodynamically more extreme. Typically, NaCl-saturated environments contain all domains-of-life and perform complete biogeochemical cycling. Despite their reduced water activity, ∼0.755 at 5 M NaCl, some halophiles belonging to the Archaea and Bacteria exhibit optimum growth/metabolism in these brines. Furthermore, the recognized water-activity limit for microbial function, ∼0.585 for some strains of fungi, lies far below 0.755. Other biophysical constraints on the microbial biosphere (temperatures of >121°C; pH >12; and high chaotropicity; e.g. ethanol at >18.9% w/v (24% v/v) and MgCl2 at >3.03 M) can prevent all ecosystem function and cellular metabolism. By contrast, NaCl-saturated environments contain biomass-dense, metabolically-diverse, highly-active, and complex microbial ecosystems which underscores their moderate character. Here, we survey the evidence that NaCl-saturated brines are biologically permissive, fertile habitats that are thermodynamically mid-range rather than extreme. Indeed, were NaCl sufficiently soluble, some halophiles might grow at 8 M. The finite solubility of NaCl may have stabilized the genetic composition of halophile populations and limited the action of natural selection in driving the halophile evolution towards greater xerophilicity. Implications are also considered for the origin(s)-of-life and other aspects of astrobiology.

LanguageEnglish
JournalFEMS microbiology reviews
Early online date11 Jun 2018
DOIs
Publication statusEarly online date - 11 Jun 2018
Externally publishedYes

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Ecosystem
Exobiology
Magnesium Chloride
Water
Genetic Selection
Archaea
Lakes
Oceans and Seas
Biomass
Solubility
Fungi
Ethanol
Salts
Bacteria
Temperature
Growth
Population

Cite this

Lee, Callum J D ; McMullan, Phillip E ; O'Kane, Callum J ; Stevenson, Andrew ; Santos, Inês C ; Roy, Chayan ; Ghosh, Wriddhiman ; Mancinelli, Rocco L ; Mormile, Melanie R ; McMullan, Geoffrey ; Banciu, Horia L ; Fares, Mario A ; Benison, Kathleen C ; Oren, Aharon ; Dyall-Smith, Mike L ; Hallsworth, John E. / NaCl-saturated brines are thermodynamically moderate, rather than extreme, microbial habitats. In: FEMS microbiology reviews. 2018.
@article{2432036960394451a4aab3a06cf896de,
title = "NaCl-saturated brines are thermodynamically moderate, rather than extreme, microbial habitats",
abstract = "NaCl-saturated brines such as saltern crystallizer ponds, inland salt-lakes, deep-sea brines, and liquids-of-deliquescence on halite are commonly regarded as a paradigm for the limit-of-life on Earth. There are, however, other habitats that are thermodynamically more extreme. Typically, NaCl-saturated environments contain all domains-of-life and perform complete biogeochemical cycling. Despite their reduced water activity, ∼0.755 at 5 M NaCl, some halophiles belonging to the Archaea and Bacteria exhibit optimum growth/metabolism in these brines. Furthermore, the recognized water-activity limit for microbial function, ∼0.585 for some strains of fungi, lies far below 0.755. Other biophysical constraints on the microbial biosphere (temperatures of >121°C; pH >12; and high chaotropicity; e.g. ethanol at >18.9{\%} w/v (24{\%} v/v) and MgCl2 at >3.03 M) can prevent all ecosystem function and cellular metabolism. By contrast, NaCl-saturated environments contain biomass-dense, metabolically-diverse, highly-active, and complex microbial ecosystems which underscores their moderate character. Here, we survey the evidence that NaCl-saturated brines are biologically permissive, fertile habitats that are thermodynamically mid-range rather than extreme. Indeed, were NaCl sufficiently soluble, some halophiles might grow at 8 M. The finite solubility of NaCl may have stabilized the genetic composition of halophile populations and limited the action of natural selection in driving the halophile evolution towards greater xerophilicity. Implications are also considered for the origin(s)-of-life and other aspects of astrobiology.",
author = "Lee, {Callum J D} and McMullan, {Phillip E} and O'Kane, {Callum J} and Andrew Stevenson and Santos, {In{\^e}s C} and Chayan Roy and Wriddhiman Ghosh and Mancinelli, {Rocco L} and Mormile, {Melanie R} and Geoffrey McMullan and Banciu, {Horia L} and Fares, {Mario A} and Benison, {Kathleen C} and Aharon Oren and Dyall-Smith, {Mike L} and Hallsworth, {John E}",
year = "2018",
month = "6",
day = "11",
doi = "10.1093/femsre/fuy026",
language = "English",
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Lee, CJD, McMullan, PE, O'Kane, CJ, Stevenson, A, Santos, IC, Roy, C, Ghosh, W, Mancinelli, RL, Mormile, MR, McMullan, G, Banciu, HL, Fares, MA, Benison, KC, Oren, A, Dyall-Smith, ML & Hallsworth, JE 2018, 'NaCl-saturated brines are thermodynamically moderate, rather than extreme, microbial habitats', FEMS microbiology reviews. https://doi.org/10.1093/femsre/fuy026

NaCl-saturated brines are thermodynamically moderate, rather than extreme, microbial habitats. / Lee, Callum J D; McMullan, Phillip E; O'Kane, Callum J; Stevenson, Andrew; Santos, Inês C; Roy, Chayan; Ghosh, Wriddhiman; Mancinelli, Rocco L; Mormile, Melanie R; McMullan, Geoffrey; Banciu, Horia L; Fares, Mario A; Benison, Kathleen C; Oren, Aharon; Dyall-Smith, Mike L; Hallsworth, John E.

In: FEMS microbiology reviews, 11.06.2018.

Research output: Contribution to journalArticle

TY - JOUR

T1 - NaCl-saturated brines are thermodynamically moderate, rather than extreme, microbial habitats

AU - Lee, Callum J D

AU - McMullan, Phillip E

AU - O'Kane, Callum J

AU - Stevenson, Andrew

AU - Santos, Inês C

AU - Roy, Chayan

AU - Ghosh, Wriddhiman

AU - Mancinelli, Rocco L

AU - Mormile, Melanie R

AU - McMullan, Geoffrey

AU - Banciu, Horia L

AU - Fares, Mario A

AU - Benison, Kathleen C

AU - Oren, Aharon

AU - Dyall-Smith, Mike L

AU - Hallsworth, John E

PY - 2018/6/11

Y1 - 2018/6/11

N2 - NaCl-saturated brines such as saltern crystallizer ponds, inland salt-lakes, deep-sea brines, and liquids-of-deliquescence on halite are commonly regarded as a paradigm for the limit-of-life on Earth. There are, however, other habitats that are thermodynamically more extreme. Typically, NaCl-saturated environments contain all domains-of-life and perform complete biogeochemical cycling. Despite their reduced water activity, ∼0.755 at 5 M NaCl, some halophiles belonging to the Archaea and Bacteria exhibit optimum growth/metabolism in these brines. Furthermore, the recognized water-activity limit for microbial function, ∼0.585 for some strains of fungi, lies far below 0.755. Other biophysical constraints on the microbial biosphere (temperatures of >121°C; pH >12; and high chaotropicity; e.g. ethanol at >18.9% w/v (24% v/v) and MgCl2 at >3.03 M) can prevent all ecosystem function and cellular metabolism. By contrast, NaCl-saturated environments contain biomass-dense, metabolically-diverse, highly-active, and complex microbial ecosystems which underscores their moderate character. Here, we survey the evidence that NaCl-saturated brines are biologically permissive, fertile habitats that are thermodynamically mid-range rather than extreme. Indeed, were NaCl sufficiently soluble, some halophiles might grow at 8 M. The finite solubility of NaCl may have stabilized the genetic composition of halophile populations and limited the action of natural selection in driving the halophile evolution towards greater xerophilicity. Implications are also considered for the origin(s)-of-life and other aspects of astrobiology.

AB - NaCl-saturated brines such as saltern crystallizer ponds, inland salt-lakes, deep-sea brines, and liquids-of-deliquescence on halite are commonly regarded as a paradigm for the limit-of-life on Earth. There are, however, other habitats that are thermodynamically more extreme. Typically, NaCl-saturated environments contain all domains-of-life and perform complete biogeochemical cycling. Despite their reduced water activity, ∼0.755 at 5 M NaCl, some halophiles belonging to the Archaea and Bacteria exhibit optimum growth/metabolism in these brines. Furthermore, the recognized water-activity limit for microbial function, ∼0.585 for some strains of fungi, lies far below 0.755. Other biophysical constraints on the microbial biosphere (temperatures of >121°C; pH >12; and high chaotropicity; e.g. ethanol at >18.9% w/v (24% v/v) and MgCl2 at >3.03 M) can prevent all ecosystem function and cellular metabolism. By contrast, NaCl-saturated environments contain biomass-dense, metabolically-diverse, highly-active, and complex microbial ecosystems which underscores their moderate character. Here, we survey the evidence that NaCl-saturated brines are biologically permissive, fertile habitats that are thermodynamically mid-range rather than extreme. Indeed, were NaCl sufficiently soluble, some halophiles might grow at 8 M. The finite solubility of NaCl may have stabilized the genetic composition of halophile populations and limited the action of natural selection in driving the halophile evolution towards greater xerophilicity. Implications are also considered for the origin(s)-of-life and other aspects of astrobiology.

U2 - 10.1093/femsre/fuy026

DO - 10.1093/femsre/fuy026

M3 - Article

JO - FEMS microbiology reviews

T2 - FEMS microbiology reviews

JF - FEMS microbiology reviews

SN - 0168-6445

ER -