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

Abstract

Cosmopolitan microbial lineages are found in anoxic sediments worldwide, but the details about their ecology and evolution remain underexplored. In this study, we identified persistent populations from these cosmopolitan lineages belonging to Planctomycetes, Chloroflexi Atribacteria, and Candidatus Bathyarchaeia from an ~8,000-year sedimentary sequence. To investigate the genomic variations within these persistent populations, a pangenome of each population was constructed using all non-redundant metagenome-assembled genomes (MAGs) recovered from the sedimentary sequence and was screened for enriched functional genes, single-nucleotide polymorphism (SNP) density, dN/DS ratios, and pseudogene content. Our results show that the majority of persistent populations studied possess large variable genomes enriched for energy conservation and transcriptional regulation functions with increasing depth, whereas Planctomycetes retain a highly conserved, SNP-poor core genome. Analysis of SNPs across depths indicates progressive isolation with burial, while a subset of core genes shows signatures of positive selection. Collectively, the data support depth-associated selection acting alongside drift across Lake Cadagno's persistent sedimentary lineages.IMPORTANCEThroughout the subsurface, multiple examples of "evolutionary stasis" have been reported in microbial lineages that exhibit lower rates of metabolic activity and cellular turnover. This study uses an ~8,000-year sedimentary record of Lake Cadagno to evaluate how persistent populations of cosmopolitan bacteria and archaea have changed with burial and identifies signals of progressive genetic isolation along with positive selection of population-specific subsets of core genes with depth. Together, these changes show that Lake Cadagno's persistent populations are not in stasis but diverge over time and burial.