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

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

doi:10.1093/molbev/msae045

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

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

^*Bijbehorende auteur voor dit werk

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

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Samenvatting

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.

Originele taal-2	Engels
Tijdschrift	Molecular Biology and Evolution
Volume	41
Nummer van het tijdschrift	4
DOI's	https://doi.org/10.1093/molbev/msae045
Status	Gepubliceerd - 01 apr. 2024

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10.1093/molbev/msae045

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title = "Functional and Evolutionary Integration of a Fungal Gene With a Bacterial Operon",

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.",

keywords = "bacterial, enterobactin, fungal, iron, operon, siderophore",

author = "Liang Sun and David, {Kyle T.} and Wolters, {John F.} and Karlen, {Steven D.} and Carla Gon{\c c}alves and Opulente, {Dana A.} and LaBella, {Abigail Leavitt} and Marizeth Groenewald and Xiaofan Zhou and Shen, {Xing Xing} and Antonis Rokas and Hittinger, {Chris Todd}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.",

year = "2024",

month = apr,

day = "1",

doi = "10.1093/molbev/msae045",

language = "English",

volume = "41",

journal = "Molecular Biology and Evolution",

issn = "0737-4038",

publisher = "Oxford University Press",

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T1 - Functional and Evolutionary Integration of a Fungal Gene With a Bacterial Operon

AU - Sun, Liang

AU - David, Kyle T.

AU - Wolters, John F.

AU - Karlen, Steven D.

AU - Gonçalves, Carla

AU - Opulente, Dana A.

AU - LaBella, Abigail Leavitt

AU - Groenewald, Marizeth

AU - Zhou, Xiaofan

AU - Shen, Xing Xing

AU - Rokas, Antonis

AU - Hittinger, Chris Todd

N1 - Publisher Copyright: © The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

PY - 2024/4/1

Y1 - 2024/4/1

N2 - 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.

AB - 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.

KW - bacterial

KW - enterobactin

KW - fungal

KW - iron

KW - operon

KW - siderophore

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U2 - 10.1093/molbev/msae045

DO - 10.1093/molbev/msae045

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