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

Padfield, Daniel, Kay, Suzanne, Vos, Rutger, Quince, Christopher and Vos, Michiel (2024) Macroevolutionary dynamics in micro-organisms: Generalists give rise to specialists across biomes in the ubiquitous bacterial phylum Myxococcota. Molecular Biology and Evolution, 41 (5). ISSN 0737-4038

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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.

Item Type: Article
Additional Information: Data Availability Statement: All raw sequencing data has been deposited on the European Nucleotide Archive (Study Accession number: PRJEB73761). Processed data and code to recreate all analyses are publicly available on GitHub (https://github.com/padpadpadpad/myxo_diversification) and is archived on Zenodo (https://zenodo.org/doi/10.5281/zenodo.11210843). The analysis code starts with the processed phyloseq objects created after the dada2 workflow. We thank two reviewers for their extensive and detailed comments that significantly improved the analyses. Funding Information: All authors acknowledge funding support from the National Environment Research Council (NERC; grant NE/T008083/1). C.Q. was supported by BBSRC Core Strategic Programme Grant (BB/CSP1720/1, BBS/E/T/000PR9818, and BBS/E/T/000PR9817). D.P. was also funded by a NERC Independent Research Fellowship (NE/W008890/1). We thank Sarah Ashton and Jane Phelps for administrative support, Paul O\u2019Neill and everyone at Exeter Sequencing Service, and Rampal Etienne for providing advice on using secsse. This work would not have been possible without tools generously made and maintained by other researchers.
Uncontrolled Keywords: comparative phylogenetics,diversification,habitat transitions,macroevolution,microbes,myxobacteria,prokaryotes,specialization,ecology, evolution, behavior and systematics,molecular biology,genetics,sdg 14 - life below water ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 23 Oct 2024 11:30
Last Modified: 01 Nov 2024 13:30
URI: https://ueaeprints.uea.ac.uk/id/eprint/97141
DOI: 10.1093/molbev/msae088

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