Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts

Authors: OPULENTE, DANA - Villanova University; LABELLA, ABIGAIL - Vanderbilt University; HARRISON, MARIE-CLAIRE - Vanderbilt University; WOLTERS, JOHN - University Of Wisconsin; LIU, CHAO - Zhejiang University; LI, YONGLIN - South China Agricultural Univerisity; KOMINEK, JACEK - University Of Wisconsin; KURTZMAN, CLETUS - Former ARS Employee; ROKAS, ANTONIS - Vanderbilt University; HITTINGER, CHRIS - University Of Wisconsin

Submitted to: Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/22/2024
Publication Date: 4/26/2024
Citation: Opulente, D.A., Labella, A.L., Harrison, M.-C., Wolters, J.F., Liu, C., Li, Y., Kominek, J., Kurtzman, C.P., Rokas, A., Hittinger, C.T., et al. 2024. Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts. Science. https://doi.org/10.1126/science.adj4503.
DOI: https://doi.org/10.1126/science.adj4503

Interpretive Summary: Organisms both big and small show an extensive variation in their ability to exist and grow in a range of specific environmental conditions or niches. Specialist organisms can only occupy a specific niche, whereas generalists are able to occupy a range of niches. Theories proposed to explain this variation either cite trade-offs between efficiency of resource use by specialist and breadth of resource use by generalist, or they suggest underlying internal genetic or external environmental forces are driving this evolution. An ARS researcher in Peoria, Illinois, collaborated with scientists at the University of Wisconsin and Vanderbilt University to assemble genomic, metabolic, and ecological data from nearly all known species of yeast fungi to examine niche range evolution. The study found that closely related species of yeast had large differences in the ability to utilize various carbon resources that is the result of internal differences in genes encoding specific metabolic pathways. There was no evidence of trade-offs between resource use efficiency vs breadth, and a limited role of external ecological factors on ability to utilize carbon resources. These comprehensive data strongly suggest internal genetic factors are driving microbial resource use variation. These results regarding resource utilization by yeast will be of particular interest to fermentation scientists and the fermentation industry. The evolution of genetic and metabolic pathways and genome resources will be of interest to the synthetic biology industry.

Technical Abstract: Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Paradigms proposed to explain this variation either invoke tradeoffs between performance efficiency and breadth or underlying intrinsic or extrinsic factors. We assembled genomic (1,154 yeast strains from 1,049 species), metabolic (quantitative measures of growth of 843 species in 24 conditions), and ecological (environmental ontology of 1,088 species) data from nearly all known species of the ancient fungal subphylum Saccharomycotina to examine niche breadth evolution. We found large interspecific differences in carbon breadth stem from intrinsic differences in genes encoding specific metabolic pathways but no evidence of trade-offs and a limited role of extrinsic ecological factors. These comprehensive data argue that intrinsic factors driving microbial niche breadth variation.