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

Author:

Sun Liang12,David Kyle T3,Wolters John F12,Karlen Steven D1,Gonçalves Carla234ORCID,Opulente Dana A125ORCID,LaBella Abigail Leavitt36,Groenewald Marizeth7,Zhou Xiaofan38ORCID,Shen Xing-Xing39ORCID,Rokas Antonis3ORCID,Hittinger Chris Todd12ORCID

Affiliation:

1. DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison , Madison, WI 53726 , USA

2. Laboratory of Genetics, Center for Genomic Science Innovation, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison , Madison, WI 53726 , USA

3. Evolutionary Studies Initiative and Department of Biological Sciences, Vanderbilt University , Nashville, TN 37235 , USA

4. UCIBIO, Department of Life Sciences, NOVA School of Science and Technology, Universidade NOVA de Lisboa , Caparica , Portugal

5. Biology Department, Villanova University , Villanova, PA 19085 , USA

6. Department of Bioinformatics and Genomics, University of North Carolina at Charlotte , Charlotte, NC 28223, USA

7. Westerdijk Fungal Biodiversity Institute , 3584 CT Utrecht , The Netherlands

8. Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Center, South China Agricultural University , Guangzhou 510642 , China

9. College of Agriculture and Biotechnology and Centre for Evolutionary & Organismal Biology, Zhejiang University , Hangzhou 310058 , China

Abstract

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.

Funder

Great Lakes Bioenergy Research Center

U.S. Department of Energy

Office of Science

Office of Biological and Environmental Research

National Science Foundation

National Institute of Food and Agriculture

United States Department of Agriculture

Wisconsin Alumni Research Foundation

National Institutes of Health

National Institute of Allergy and Infectious Diseases

Burroughs Welcome Fund

Publisher

Oxford University Press (OUP)

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