Search bioRxiv⌕ Search

Biology subjects

Crill, P. M.

Publications and source records attributed to Crill, P. M..

4 recordsLinked to original sources

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↗

Methylotrophy in the Mire: direct and indirect routes for methane production in thawing permafrost

While wetlands are major sources of biogenic methane (CH4), our understanding of resident microbial metabolisms is incomplete, which compromises prediction of CH4 emissions under ongoing climate change. Here, we employed genome-resolved multi-omics to expand our understanding of methanogenesis in the thawing permafrost peatland of Stordalen Mire, in arctic Sweden. In quadrupling the genomic representation of the sites methanogens and examining their encoded metabolisms, we revealed that nearly 20% (72) of the metagenome-assembled genomes (MAGs) encoded potential for methylotrophic methanogenesis. Further, 27% of the transcriptionally active methanogens expressed methylotrophic genes; for Methanosarcinales and Methanobacteriales MAGs, these data indicated use of methylated oxygen compounds (e.g., methanol), while for Methanomassiliicoccales, they primarily implicated methyl sulfides and methylamines. In addition to methanogenic methylotrophy, >1700 bacterial MAGs across 19 phyla encoded anaerobic methylotrophic potential, with expression across 12 phyla. Metabolomic analyses revealed the presence of diverse methylated compounds in the Mire, including some known methylotrophic substrates. Active methylotrophy was observed across all stages of a permafrost thaw gradient in Stordalen, with the most frozen non-methanogenic palsa found to host bacterial methylotrophy, and the partially thawed bog and fully thawed fen seen to house both methanogenic and bacterial methylotrophic activity. Methanogenesis across increasing permafrost thaw is thus revised from sole dominance of hydrogenotrophic production, and the appearance of acetoclastic at full thaw, to consider co-occurrence of methylotrophy throughout. Collectively, these findings indicate that methanogenic and bacterial methylotrophy may be an important and previously underappreciated component of carbon cycling and emissions in these rapidly changing wetland habitats.

microbiology↗

Diverse Arctic lake sediment microbiota shape methane emission temperature sensitivity

Northern post-glacial lakes are a significant and increasing source of atmospheric carbon (C), largely through ebullition (bubbling) of microbially-produced methane (CH4) from the sediments1. Ebullitive CH4 flux correlates strongly with temperature, suggesting that solar radiation is the primary driver of these CH4 emissions2. However, here we show that the slope of the temperature-CH4 flux relationship differs spatially, both within and among lakes. Hypothesizing that differences in microbiota could explain this heterogeneity, we compared site-specific CH4 emissions with underlying sediment microbial (metagenomic and amplicon), isotopic, and geochemical data across two post-glacial lakes in Northern Sweden. The temperature-associated increase in CH4 emissions was greater in lake middles--where methanogens were more abundant--than edges, and sediment microbial communities were distinct between lake edges and middles. Although CH4 emissions projections are typically driven by abiotic factors1, regression modeling revealed that microbial abundances, including those of CH4-cycling microorganisms and syntrophs that generate H2 for methanogenesis, can be useful predictors of porewater CH4 concentrations. Our results suggest that deeper lake regions, which currently emit less CH4 than shallower edges, could add substantially to overall CH4 emissions in a warmer Arctic with longer ice-free seasons and that future CH4 emission predictions from northern lakes may be improved by accounting for spatial variations in sediment microbiota.

microbiology↗

Microbial Network, Phylogenetic Diversity And Community Membership In The Active Layer Across A Permafrost Thaw Gradient

Biogenic production and release of methane (CH4) from thawing permafrost has the potential to be a strong source of radiative forcing. We investigated changes in the active layer microbial community of three sites representative of distinct permafrost thaw stages at a palsa mire in northern Sweden. The palsa sites with intact permafrost, and low radiative forcing signature had a phylogenetically clustered community dominated by Acidobacteria and Proteobacteria. The bog with thawing permafrost and low radiative forcing signature was dominated by hydrogenotrophic methanogens and Acidobacteria, had lower alpha diversity, and midrange phylogenetic clustering, characteristic of ecosystem disturbance affecting habitat filtering, shifting from palsa-like to fen-like at the waterline. The fen had no underlying permafrost, and the highest alpha, beta and phylogenetic diversity, was dominated by Proteobacteria and Euryarchaeota, and was significantly enriched in methanogens. The mire microbial network was modular with module cores consisting of clusters of Acidobacteria, Euryarchaeota, or Xanthomonodales. Loss of underlying permafrost with associated hydrological shifts correlated to changes in microbial composition, alpha, beta, and phylogenetic diversity associated with a higher radiative forcing signature. These results support the complex role of microbial interactions in mediating carbon budget changes and climate feedback in response to climate forcing.

ecology↗