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Depth-associated selection and drift shape persistent microbial populations in Holocene lake sediments.

Paula Rodríguez1, Sophie A Simon2, Alexander J Probst2,3,4

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Summary

Persistent microbial populations in ancient lake sediments show genomic divergence over time, not evolutionary stasis. These cosmopolitan lineages, including Planctomycetes, adapt to increasing burial depth through genetic isolation and selection.

Keywords:
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Area of Science:

  • Microbial Ecology
  • Evolutionary Biology
  • Geomicrobiology

Background:

  • Cosmopolitan microbial lineages inhabit anoxic sediments globally, yet their ecological and evolutionary dynamics are poorly understood.
  • Previous studies suggest microbial 'evolutionary stasis' in subsurface environments due to low metabolic activity and turnover rates.

Purpose of the Study:

  • To investigate genomic variations and evolutionary trajectories of persistent microbial populations within an ~8,000-year sedimentary sequence.
  • To assess the impact of burial depth on genomic diversity, functional gene content, and selection pressures in cosmopolitan microbial lineages.

Main Methods:

  • Construction of pangenomes for persistent populations of Planctomycetes, Chloroflexi Atribacteria, and Candidatus Bathyarchaeia using metagenome-assembled genomes (MAGs).
  • Analysis of enriched functional genes, single-nucleotide polymorphism (SNP) density, dN/dS ratios, and pseudogene content across different sediment depths.
  • Evaluation of genomic signals indicative of isolation, selection, and evolutionary divergence.

Main Results:

  • Most persistent populations exhibited large, variable genomes enriched in energy conservation and transcriptional regulation genes with increasing depth.
  • Planctomycetes maintained a conserved, SNP-poor core genome.
  • SNP analysis revealed progressive genetic isolation with burial, and a subset of core genes showed signatures of positive selection.

Conclusions:

  • Persistent microbial populations in Lake Cadagno's sedimentary record are not in evolutionary stasis but undergo divergence.
  • Depth-associated selection and genetic drift drive the evolution of these lineages over millennial timescales.
  • Genomic analysis provides insights into the adaptation and diversification of cosmopolitan microbes in long-term sedimentary environments.