Macroevolutionary Dynamics in Micro-organisms: Generalists Give Rise to Specialists Across Biomes in the Ubiquitous Bacterial Phylum Myxococcota

Molecular Biology and Evolution, vol. 41

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. However, relatively little is known about how prokaryotes successfully transition and persist across environments, and how these processes might vary between biomes and lineages. Here, we investigate biome transitions and specialization 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 >2,000 unique Myxococcota lineages, with the majority (77%) classified as biome specialists and with only <5% of lineages distributed across the salt barrier. Discrete character evolution models revealed that specialists in one biome rarely transitioned into specialists in another biome. Instead, evolved generalism mediated transitions between biome specialists. State-dependent diversification models found variation in speciation rates across the tree, but this variation was independent of biome association or specialization. Our findings were robust to phylogenetic uncertainty, different levels of species delineation, and different assumed amounts of unsampled diversity resulting in an incomplete phylogeny. Overall, our results are consistent with a "jack-of-all-trades" tradeoff where generalists suffer a cost in any individual environment, resulting in rapid evolution of niche specialists and shed light on how bacteria could transition between biomes.

Authors 5

1. Daniel Padfield corresponding

   University of Exeter

   Affiliation as printed

   Environment and Sustainability Institute, Penryn Campus , Penryn TR10 9FE , UK

2. Suzanne Kay

   University of Exeter

   Affiliation as printed

   Environment and Sustainability Institute, Penryn Campus , Penryn TR10 9FE , UK

3. Rutger Aldo Vos Aachen Institute of Biology Leiden Naturalis Biodiversity Center

   Leiden University · Naturalis Biodiversity Center

   Affiliation as printed

   Institute of Biology Leiden, Leiden University , 2333 BE Leiden , The Netherlands

   Naturalis Biodiversity Center , P.O. Box 9517, 2300 RA Leiden , The Netherlands

   Institute of Biology Leiden, Leiden University, Sylviusweg 72, 2333 BE, Leiden, The Netherlands

4. Christopher Quince

   Quadram Institute · Earlham Institute

   Affiliation as printed

   Gut Microbes and Health, Quadram Institute , Norwich NR4 7UQ , UK

   Organisms and Ecosystems, Earlham Institute , Norwich NR4 7UZ , UK

   Organisms and Ecosystems, Earlham Institute, Norwich, Norwich, NR4 7UZ, UK

5. Michiel Vos

   University of Exeter

   Affiliation as printed

   Environment and Sustainability Institute, Penryn Campus , Penryn TR10 9FE , UK

   European Centre for Environment and Human Health, Penryn Campus , Penryn TR10 9FE , UK