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

bioRxiv (Cold Spring Harbor Laboratory)

Abstract

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.

Authors 5

1. Daniel Padfield corresponding

   University of Exeter

   Affiliation as printed

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

   Environment and Sustainability Institute, Penryn Campus, TR0 9FE, UK

2. Suzanne Kay

   University of Exeter

   Affiliation as printed

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

   Environment and Sustainability Institute, Penryn Campus, TR0 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, Sylviusweg 72, 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, 2 BE, Leiden, The Netherlands

   Naturalis Biodiversity Center, P.O. Box 9517, 300 RA, 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, Norwich, NR4 7UZ, UK

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

5. Michiel Vos

   University of Exeter

   Affiliation as printed

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

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

   Environment and Sustainability Institute, Penryn Campus, TR0 9FE, UK