pH-driven evolutionary divergence and ongoing speciation in the cosmopolitan cyanobacterium Microcoleus vaginatus

Abstract

Speciation models and the concept of speciation continuum have been well established in multicellular eukaryotes. However, the mechanisms underlying population differentiation and their environmental drivers in prokaryotes remain elusive. Here, we explored the population diversification of the filamentous cyanobacterium Microcoleus vaginatus, a photoautotrophic edificator with significant importance for dryland ecosystems worldwide. By constructing a 132-genome dataset spanning multiple climate zones across four continents, we integrated intraspecific genomics with environmental association analyses to elucidate the population genetic structure and molecular mechanisms underlying the divergence of the M. vaginatus continuum. Our findings reveal that adaptive differentiation is driven by the combined effects of natural selection, homologous recombination, and gene family turnover, with varying contributions across different phylogroups. The evolution of core and accessory genomes exhibits complementary patterns, with genome-wide association studies demonstrating the predominant role of the core genome in population divergence. Selection, followed by neutral evolution and recombination, mediates trade-offs in life-history strategies, while environmental factors shape these evolutionary processes. Notably, while local edaphic variables exert direct influences on Tajimas D values, they demonstrate predominantly indirect modulation through alterations in the selection-to-gene gain ratio (S/G). pH emerges as the principal abiotic driver governing population genetic signatures, operating through coordinated effects on both S/G and the proportion of selected genes undergoing recombination (SUR). This study offers novel insights into the diversification mechanisms of cosmopolitan, dominant cyanobacteria, thereby advancing our understanding of prokaryotic speciation in complex natural settings and providing a framework for predicting microbial adaptation in a changing world.