Journal Article

Covariation of hot spring geochemistry with microbial genomic diversity, function, and evolution

Andrade-Barahona, Eva, Boyd, Eric S., Arteaga-Pozo, Emilia, Colman, Daniel R., Cox, Alysia, Keller, Lisa M., Shoemaker, Anna, St. Clair, Brian

2024

Overview

The geosphere and the microbial biosphere have co-evolved for ~3.8 Ga, with many lines of evidence suggesting a hydrothermal habitat for life’s origin. However, the extent that contemporary thermophiles and their hydrothermal habitats reflect those that likely existed on early Earth remains unknown. To address this knowledge gap, 64 geochemical analytes were measured and 1022 metagenome-assembled-genomes (MAGs) were generated from 34 chemosynthetic high-temperature springs in Yellowstone National Park and analysed alongside 444 MAGs from 35 published metagenomes. We used these data to evaluate co-variation in MAG taxonomy, metabolism, and phylogeny as a function of hot spring geochemistry. We found that cohorts of MAGs and their functions are discretely distributed across pH gradients that reflect different geochemical provinces. Acidic or circumneutral/alkaline springs harbor MAGs that branched later and are enriched in sulfur- and arsenic-based O 2 -dependent metabolic pathways that are inconsistent with early Earth conditions. In contrast, moderately acidic springs sourced by volcanic gas harbor earlier-branching MAGs that are enriched in anaerobic, gas-dependent metabolisms (e.g. H 2 , CO 2 , CH 4 metabolism) that have been hypothesized to support early microbial life. Our results provide insight into the influence of redox state in the eco-evolutionary feedbacks between thermophiles and their habitats and suggest moderately acidic springs as early Earth analogs. Life may have originated in a hydrothermal habitat, but the extent that contemporary thermophilic microbes and their environments reflect those on early Earth is unclear. Here, Colman et al. evaluate covariation in microbial taxonomy, metabolism and phylogeny as a function of hot spring geochemistry, suggesting moderately acidic springs as early Earth analogs.

• Publisher: Nature Publishing Group UK,Nature Publishing Group,Nature Portfolio
• Subject: 45/22 / 45/23 / 631/326/171 / 631/326/2565/2142 / 631/326/2565/855 / 631/326/47/4112 / 704/445/209 / Anaerobic conditions / Anaerobic microorganisms / Analogs / Archaea - classification / Archaea - genetics / Archaea - metabolism / Arsenic / Bacteria - classification / Bacteria - genetics / Bacteria - metabolism / Biosphere / Carbon dioxide / Earth / Earth analogs / Ecosystem / Evolution / Genome, Microbial / Geochemistry / Geosphere / Habitats / High temperature / Hot springs / Hot Springs - chemistry / Hot Springs - microbiology / Humanities and Social Sciences / Hydrogen-Ion Concentration / Metabolic pathways / Metabolism / Metagenome / Microbiota - genetics / Microorganisms / multidisciplinary / National parks / Phylogeny / Redox properties / Science / Science & Technology - Other Topics / Science (multidisciplinary) / Sulfur / Taxonomy / Thermophiles / Thermophilic microorganisms / Volcanic gases