Borton, M. | bioRxiv Science

bioRxiv2025

Stable states in an unstable landscape: microbial resistance at the front line of climate change

Microbiome responses to warming may amplify or ameliorate terrestrial carbon loss and thus are a critical unknown in predicting climate outcomes. Because the rapid thaw of permafrost peatlands makes a very large store of soil carbon available to microbial metabolism, understanding microbiome dynamics in these systems is particularly urgent. We quantified microbial warming response over seven years across three habitats in a thawing permafrost peatland, using large-scale multi-omics data. We integrated analyses of organisms (via taxonomy), functions (via metabolic pathways and proteins), and community organization (via network structure and ecological assembly) to deeply characterize response mechanisms. We consistently found a pattern of within-habitat microbiome stability, with virtually no signal of gradual change in the warming period studied. The resistance to change appeared bolstered by habitat-specific dispersal processes and community-level functional redundancy, particularly via versatile carbon generalists. Our findings also reveal key genome-inferred metabolic processes that underlie microbiome stability. Together, our results highlight the importance of understanding the limits of these stabilizing processes and suggest that future research should reorient towards critical habitat transitions.

microbiology↗

bioRxiv2020

The Diversity and Evolution of Microbial Dissimilatory Phosphite Oxidation

Phosphite is the most energetically favorable chemotrophic electron donor known, with a half-cell potential (E{degrees}) of -650 mV for the PO4 3-/PO3 3- couple. Since the discovery of microbial dissimilatory phosphite oxidation (DPO) in 2000, the environmental distribution, evolution, and diversity of DPO microorganisms (DPOM) has remained enigmatic and only two species have been identified. Here metagenomic sequencing of phosphite enriched microbial communities enabled the reconstruction and metabolic characterization of 21 novel DPOM. These DPOM spanned six classes of bacteria, including the Negativicutes, Desulfotomaculia, Synergistia, Syntrophia, Desulfobacteria and Desulfomonilia_A. Comparing the DPO genes from the genomes of enriched organisms to over 17,000 publicly available metagenomes revealed the global existence of this metabolism in diverse anoxic environments, including wastewaters, sediments, and subsurface aquifers. Despite their newfound environmental and taxonomic diversity, metagenomic analyses suggested that the typical DPOM is a chemolithoautotroph that occupies low-oxygen environments and specializes in phosphite oxidation coupled to CO2 reduction. Phylogenetic analyses indicated that the DPO genes form a highly conserved cluster that likely has ancient origins predating the split of monoderm and diderm bacteria. By coupling microbial cultivation strategies with metagenomics, these studies highlighted the unsampled metabolic versatility latent in microbial communities. We have uncovered the unexpected prevalence, diversity, biochemical specialization, and ancient origins of a unique metabolism central to the redox cycling of phosphorus, a primary nutrient on earth. Significance StatementGeochemical models of the phosphorus (P) cycle uniquely ignore microbial redox transformations. Yet phosphite is a reduced P source that has been detected in several environments at concentrations that suggest a contemporary P redox cycle. Microbial dissimilatory phosphite oxidation (DPO) converts soluble phosphite into phosphate, and a false notion of rarity has limited our understanding of its diversity and environmental distribution. Here we demonstrate that DPO is an ancient energy metabolism hosted by taxonomically diverse, autotrophic bacteria that exist globally throughout anoxic environments. DPO microorganisms are therefore likely to have provided bioavailable phosphate and fixed carbon to anoxic ecosystems throughout Earths history and continue to do so in contemporary environments.

microbiology↗