Catabolic pathway acquisition by rhizosphere bacteria readily enables growth with a root exudate component but does not affect root colonization

Christel, Stephan; Carrell, Alyssa A.; Hochanadel, Leah H.; Villalobos Solis, Manuel I.; Abraham, Paul E.; Jawdy, Sara S.; Chaves, Julie E.; Engle, Nancy L.; Berhane, Timkhite-Kulu; Yao, Tao; Chen, Jin-Gui; Muchero, Wellington; Tschaplinski, Timothy J.; Cregger, Melissa A.; Michener, Joshua K.

doi:10.1128/mbio.03016-24

Title: Catabolic pathway acquisition by rhizosphere bacteria readily enables growth with a root exudate component but does not affect root colonization

Journal Article · 10 December 2024 · mBio (Online)

DOI: https://doi.org/10.1128/mbio.03016-24 · OSTI ID:2481012

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^[1]; Hochanadel, Leah H. ^[1]; Villalobos Solis, Manuel I. ^[1];

^[1];

^[1]; Chaves, Julie E. ^[1];

^[1]; Berhane, Timkhite-Kulu ^[1];

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Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Horizontal gene transfer (HGT) is a fundamental evolutionary process that plays a key role in bacterial evolution. The likelihood of a successful transfer event is expected to depend on the precise balance of costs and benefits resulting from pathway acquisition. Most experimental analyses of HGT have focused on phenotypes that have large fitness benefits under appropriate selective conditions, such as antibiotic resistance. However, many examples of HGT involve phenotypes that are predicted to provide smaller benefits, such as the ability to catabolize additional carbon sources. We have experimentally simulated the consequences of one such HGT event in the laboratory, studying the effects of transferring a pathway for catabolism of the plant-derived aromatic compound salicyl alcohol between rhizosphere isolates from the Pseudomonas genus. We find that pathway acquisition enables rapid catabolism of salicyl alcohol with only minor disruptions to the existing metabolic and regulatory networks of the new host. However, this new catabolic potential does not confer a measurable fitness advantage during competitive growth in the rhizosphere. We conclude that the phenotype of salicyl alcohol catabolism is readily transferable but is selectively neutral under environmentally relevant conditions. We propose that this condition is common and that HGT of many pathways will be self-limiting because the selective benefits are small.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 2481012

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 1 Vol. 16; ISSN 2150-7511

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

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