Functional and Evolutionary Integration of a Fungal Gene With a Bacterial Operon

Sun, Liang; David, Kyle T.; Wolters, John F.; Karlen, Steven D.; Gonçalves, Carla; Opulente, Dana A.; LaBella, Abigail Leavitt; Groenewald, Marizeth; Zhou, Xiaofan; Shen, Xing-Xing; Rokas, Antonis; Hittinger, Chris Todd; Townsend, ed., Jeffrey

doi:10.1093/molbev/msae045

Functional and Evolutionary Integration of a Fungal Gene With a Bacterial Operon

Journal Article · Tue Feb 27 23:00:00 EST 2024 · Molecular Biology and Evolution

DOI:https://doi.org/10.1093/molbev/msae045· OSTI ID:2340932

Sun, Liang; David, Kyle T.; Wolters, John F.; Karlen, Steven D.; ; ; LaBella, Abigail Leavitt; Groenewald, Marizeth; ; ; ; ; Townsend, ed., Jeffrey

Abstract

Siderophores are crucial for iron-scavenging in microorganisms. While many yeasts can uptake siderophores produced by other organisms, they are typically unable to synthesize siderophores themselves. In contrast, Wickerhamiella/Starmerella (W/S) clade yeasts gained the capacity to make the siderophore enterobactin following the remarkable horizontal acquisition of a bacterial operon enabling enterobactin synthesis. Yet, how these yeasts absorb the iron bound by enterobactin remains unresolved. Here, we demonstrate that Enb1 is the key enterobactin importer in the W/S-clade species Starmerella bombicola. Through phylogenomic analyses, we show that ENB1 is present in all W/S clade yeast species that retained the enterobactin biosynthetic genes. Conversely, it is absent in species that lost the ent genes, except for Starmerella stellata, making this species the only cheater in the W/S clade that can utilize enterobactin without producing it. Through phylogenetic analyses, we infer that ENB1 is a fungal gene that likely existed in the W/S clade prior to the acquisition of the ent genes and subsequently experienced multiple gene losses and duplications. Through phylogenetic topology tests, we show that ENB1 likely underwent horizontal gene transfer from an ancient W/S clade yeast to the order Saccharomycetales, which includes the model yeast Saccharomyces cerevisiae, followed by extensive secondary losses. Taken together, these results suggest that the fungal ENB1 and bacterial ent genes were cooperatively integrated into a functional unit within the W/S clade that enabled adaptation to iron-limited environments. This integrated fungal-bacterial circuit and its dynamic evolution determine the extant distribution of yeast enterobactin producers and cheaters.

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

Grant/Contract Number:: SC0018409

OSTI ID:: 2340932

Alternate ID(s):: OSTI ID: 2472375

Journal Information:: Molecular Biology and Evolution, Journal Name: Molecular Biology and Evolution Journal Issue: 4 Vol. 41; ISSN 0737-4038

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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