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Forecasting of phenotypic and genetic outcomes of experimental evolution in Pseudomonas protegens
Umeå University, Faculty of Medicine, Department of Molecular Biology (Faculty of Medicine). (Peter Lind)ORCID iD: 0000-0002-8186-3005
Umeå University, Faculty of Science and Technology, Department of Molecular Biology (Faculty of Science and Technology).ORCID iD: 0000-0003-1510-8324
2021 (English)In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 17, no 8, article id e1009722Article in journal (Refereed) Published
Abstract [en]

Experimental evolution with microbes is often highly repeatable under identical conditions, suggesting the possibility to predict short-term evolution. However, it is not clear to what degree evolutionary forecasts can be extended to related species in non-identical environments, which would allow testing of general predictive models and fundamental biological assumptions. To develop an extended model system for evolutionary forecasting, we used previous data and models of the genotype-to-phenotype map from the wrinkly spreader system in Pseudomonas fluorescens SBW25 to make predictions of evolutionary outcomes on different biological levels for Pseudomonas protegens Pf-5. In addition to sequence divergence (78% amino acid and 81% nucleotide identity) for the genes targeted by mutations, these species also differ in the inability of Pf-5 to make cellulose, which is the main structural basis for the adaptive phenotype in SBW25. The experimental conditions were changed compared to the SBW25 system to test if forecasts were extendable to a non-identical environment. Forty-three mutants with increased ability to colonize the air-liquid interface were isolated, and the majority had reduced motility and was partly dependent on the Pel exopolysaccharide as a structural component. Most (38/43) mutations are expected to disrupt negative regulation of the same three diguanylate cyclases as in SBW25, with a smaller number of mutations in promoter regions, including an uncharacterized polysaccharide synthase operon. A mathematical model developed for SBW25 predicted the order of the three main pathways and the genes targeted by mutations, but differences in fitness between mutants and mutational biases also appear to influence outcomes. Mutated regions in proteins could be predicted in most cases (16/22), but parallelism at the nucleotide level was low and mutational hot spot sites were not conserved. This study demonstrates the potential of short-term evolutionary forecasting in experimental populations and provides testable predictions for evolutionary outcomes in other Pseudomonas species.

Place, publisher, year, edition, pages
Public Library of Science , 2021. Vol. 17, no 8, article id e1009722
National Category
Evolutionary Biology Genetics and Genomics Microbiology
Identifiers
URN: urn:nbn:se:umu:diva-186725DOI: 10.1371/journal.pgen.1009722ISI: 000685254400002PubMedID: 34351900Scopus ID: 2-s2.0-85112263294OAI: oai:DiVA.org:umu-186725DiVA, id: diva2:1586130
Funder
The Kempe Foundations, SMK-1858.1Carl Tryggers foundation , CTS 16:275Magnus Bergvall Foundation, 2016Available from: 2021-08-19 Created: 2021-08-19 Last updated: 2025-02-01Bibliographically approved

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Pentz, Jennifer T.Lind, Peter A.

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