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Single-cell analysis in hypersaline brines predicts a water-activity limit of microbial anabolic activity.

ABSTRACT: Hypersaline brines provide excellent opportunities to study extreme microbial life. Here, we investigated anabolic activity in nearly 6000 individual cells from solar saltern sites with water activities (a_w) ranging from 0.982 to 0.409 (seawater to extreme brine). Average anabolic activity decreased exponentially with a_w, with nuanced trends evident at the single-cell level: The proportion of active cells remained high (>50%) even after NaCl saturation, and subsets of cells spiked in activity as a_w decreased. Intracommunity heterogeneity in activity increased as seawater transitioned to brine, suggesting increased phenotypic heterogeneity with increased physiological stress. No microbial activity was detected in the 0.409-a_w brine (an MgCl₂-dominated site) despite the presence of cell-like structures. Extrapolating our data, we predict an a_w limit for detectable anabolic activity of 0.540, which is beyond the currently accepted limit of life based on cell division. This work demonstrates the utility of single-cell, metabolism-based techniques for detecting active life and expands the potential habitable space on Earth and beyond.

SUBMITTER: Paris ER

PROVIDER: S-EPMC10745694 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Single-cell analysis in hypersaline brines predicts a water-activity limit of microbial anabolic activity.

Paris Emily R ER Arandia-Gorostidi Nestor N Klempay Benjamin B Bowman Jeff S JS Pontefract Alexandra A Elbon Claire E CE Glass Jennifer B JB Ingall Ellery D ED Doran Peter T PT Som Sanjoy M SM Schmidt Britney E BE Dekas Anne E AE

Science advances 20231222 51

Hypersaline brines provide excellent opportunities to study extreme microbial life. Here, we investigated anabolic activity in nearly 6000 individual cells from solar saltern sites with water activities (aw) ranging from 0.982 to 0.409 (seawater to extreme brine). Average anabolic activity decreased exponentially with aw, with nuanced trends evident at the single-cell level: The proportion of active cells remained high (>50%) even after NaCl saturation, and su ...[more]

PMID: 38134283

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Project description:Soda lakes are salt lakes with a naturally alkaline pH due to evaporative concentration of sodium carbonates in the absence of major divalent cations. Hypersaline soda brines harbor microbial communities with a high species- and strain-level archaeal diversity and a large proportion of still uncultured poly-extremophiles compared to neutral brines of similar salinities. We present the first "metagenomic snapshots" of microbial communities thriving in the brines of four shallow soda lakes from the Kulunda Steppe (Altai, Russia) covering a salinity range from 170 to 400 g/L. Both amplicon sequencing of 16S rRNA fragments and direct metagenomic sequencing showed that the top-level taxa abundance was linked to the ambient salinity: Bacteroidetes, Alpha-, and Gamma-proteobacteria were dominant below a salinity of 250 g/L, Euryarchaeota at higher salinities. Within these taxa, amplicon sequences related to Halorubrum, Natrinema, Gracilimonas, purple non-sulfur bacteria (Rhizobiales, Rhodobacter, and Rhodobaca) and chemolithotrophic sulfur oxidizers (Thioalkalivibrio) were highly abundant. Twenty-four draft population genomes from novel members and ecotypes within the Nanohaloarchaea, Halobacteria, and Bacteroidetes were reconstructed to explore their metabolic features, environmental abundance and strategies for osmotic adaptation. The Halobacteria- and Bacteroidetes-related draft genomes belong to putative aerobic heterotrophs, likely with the capacity to ferment sugars in the absence of oxygen. Members from both taxonomic groups are likely involved in primary organic carbon degradation, since some of the reconstructed genomes encode the ability to hydrolyze recalcitrant substrates, such as cellulose and chitin. Putative sodium-pumping rhodopsins were found in both a Flavobacteriaceae- and a Chitinophagaceae-related draft genome. The predicted proteomes of both the latter and a Rhodothermaceae-related draft genome were indicative of a "salt-in" strategy of osmotic adaptation. The primary catabolic and respiratory pathways shared among all available reference genomes of Nanohaloarchaea and our novel genome reconstructions remain incomplete, but point to a primarily fermentative lifestyle. Encoded xenorhodopsins found in most drafts suggest that light plays an important role in the ecology of Nanohaloarchaea. Putative encoded halolysins and laccase-like oxidases might indicate the potential for extracellular degradation of proteins and peptides, and phenolic or aromatic compounds.

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Single-cell analysis in hypersaline brines predicts a water-activity limit of microbial anabolic activity.

Publications

Single-cell analysis in hypersaline brines predicts a water-activity limit of microbial anabolic activity.

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