Macroevolutionary dynamics in micro-organisms: generalists give rise to specialists across biomes in the ubiquitous bacterial phylum Myxococcota.

Abstract

Prokaryotes dominate the Tree of Life, but our understanding of the macroevolutionary processes generating this diversity is still limited. Habitat transitions are thought to be a key driver of prokaryote diversity, but we still know relatively little about how prokaryotes successfully transition and persist across environments, and how this varies between biomes and lineages. Here, we investigate biome transitions and specialisation in natural populations of a focal bacterial phylum, the Myxococcota, sampled across a range of replicated soils and freshwater and marine sediments in Cornwall (UK). By targeted deep sequencing of the protein-coding gene rpoB, we found >2000 unique Myxococcota lineages, with the majority (77%) being biome specialists and <5% able to live across the salt barrier. Discrete character evolution models revealed that biome specialists very rarely transitioned to specialising in another biome. Instead, generalists mediated transitions between biome specialists. Multistate hidden-state speciation and extinction models found variation in speciation rate across the tree, but this variation was independent of biome association and specialisation. Overall, our results help explain how microbes transition between biomes and are consistent with "the jack-of-all-trades" trade-off, where generalists suffer a cost in any individual environment, resulting in rapid evolution of niche specialists.