Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts
Open accessAbstract
Organisms exhibit extensive variation in ecological niche breadth, from very narrow (specialists) to very broad (generalists). Two general paradigms have been proposed to explain this variation: (i) trade-offs between performance efficiency and breadth and (ii) the joint influence of extrinsic (environmental) and intrinsic (genomic) factors. We assembled genomic, metabolic, and ecological data from nearly all known species of the ancient fungal subphylum Saccharomycotina (1154 yeast strains from 1051 species), grown in 24 different environmental conditions, to examine niche breadth evolution. We found that large differences in the breadth of carbon utilization traits between yeasts stem from intrinsic differences in genes encoding specific metabolic pathways, but we found limited evidence for trade-offs. These comprehensive data argue that intrinsic factors shape niche breadth variation in microbes.
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C. albicans and S. cerevisiae are separated by at least 234 MYA according to a time tree calculated using phylogenomic data.
“are separated by a considerable evolutionary distance of at least 234 MYA according to the time tree calculated using phylogenomic data (Opulente et al. 2024)”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Opulente et al. 2024
The 'Genome sequencing, annotation, and phylogenomics' section says the authors used phylogenomic data to estimate a yeast time tree. The Introduction identifies C. albicans among the yeasts studied, but the passages in our copy do not give a divergence date for C. albicans and S. cerevisiae or substantiate the claimed minimum of 234 MYA (searched: 234, divergence time, and million years ago). (LLM, conf=0.84)
Experimental — accuracy not yet measuredThe duplication event occurred during the evolution of the subphylum Saccharomycotina, after the split of Lipomycetales, Trigonopsidales, and Dipodascales, and before the ancestor of the remaining lineages, about 234 MYA.
“This event occurred during the evolution of the subphylum Saccharomycotina, after the split of the three earliest branching orders—Lipomycetales, Trigonopsidales, and Dipodascales that still contain a single Rtg ortholog—and the ancestor of the remaining lineages, about 234 MYA according to the time tree estimation based on recent phylogenomic data (Opulente et al. 2024).”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Opulente et al. 2024
The Introduction describes a genome-scale Saccharomycotina phylogeny, and “Genome sequencing, annotation, and phylogenomics” says the authors estimated a yeast time tree. The passages do not date the specified ancestor to about 234 MYA or place the Rtg duplication between the named orders and the remaining lineages (searched: 234, the order names, and Rtg ortholog duplication). (LLM, conf=0.82)
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Self-citationTranslating microbial kinetics into quantitative responses and testable hypotheses using Kinbiont
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The genome sequence of a marine yeast, Metschnikowia zobellii (Uden & Cast.-Branco, 1961)
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Self-citationGenome sequence of the yeast Candida solani UCD1087, isolated from soil in Ireland
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Genomic factors limiting the diversity of Saccharomycotina plant pathogens
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Self-citationMicrobial Life in Extreme Habitats
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A Global Synthesis of Yeast in Microbiomes
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Complete diploid genome of the type strain Yarrowia lipolytica YB-423 (ATCC 18942™)
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The role and possible mechanism of intestinal fungi in the progression of chronic liver diseases
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Nitrogen management in the optimization of microbial plastic waste upcycling
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Description of Deakozyma peteri sp. nov., a yeast isolated from substrates of neotropical regions
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Self-citationStable hypermutators revealed by the genomic landscape of DNA repair genes among yeast speciesPreprint
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Self-citationEcology and evolution of microbial community assembly
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Proposal of two new genera and seventy-seven new species of ascomycetous yeasts isolated from ChinaPreprint
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The macroevolution of filamentation morphology across the Saccharomycotina yeast subphylum
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- Authors
- Opulente, D. A., LaBella, A. L., Harrison, M.-C., Wolters, J. F., Liu, C., Li, Y., Kominek, J., Steenwyk, J. L., Stoneman, H. R., VanDenAvond, J., Miller, C. R., Langdon, Q. K., Silva, M., Gonçalves, C., Ubbelohde, E. J., Li, Y., Buh, K. V., Jarzyna, M., Haase, M. A. B., Rosa, C. A., ČCadež, N., Libkind, D., DeVirgilio, J. H., Hulfachor, A. B., Kurtzman, C. P., Sampaio, J. P., Gonçalves, P., Zhou, X., Shen, X.-X., Groenewald, M., Rokas, A., & Hittinger, C. T.
- Affiliations
- University of Wisconsin–Madison (US)
- University of North Carolina at Charlotte (US)
- Vanderbilt University (US)
- Zhejiang University (CN)
- South China Agricultural University (CN)
- Howard Hughes Medical Institute (US)
- Universidade Nova de Lisboa (PT)
- Universidade Federal de Minas Gerais (BR)
- Food Science and Technology Department, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.
- Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
- Agricultural Research Service (US)
- Westerdijk Fungal Biodiversity Institute (NL)
- Corresponding author
- Opulente, Dana A.
- LaBella, Abigail Leavitt
- Harrison, Marie-Claire
- Wolters, John F.
- Rokas, Antonis
- Hittinger, Chris Todd
- ORCID
- Opulente, Dana A.
- LaBella, Abigail Leavitt
- Harrison, Marie-Claire
- Wolters, John F.
- Liu, Chao
- Li, Yonglin
- Kominek, Jacek
- Steenwyk, Jacob L.
- Stoneman, Hayley R.
- VanDenAvond, Jenna
- Miller, Caroline R.
- Langdon, Quinn K.
- Silva, Margarida
- Gonçalves, Carla
- Ubbelohde, Emily J.
- Li, Yuanning
- Jarzyna, Martin
- Haase, Max A. B.
- Rosa, Carlos A.
- ČCadež, Neža
- Libkind, Diego
- DeVirgilio, Jeremy H.
- Hulfachor, Amanda Beth
- Kurtzman, Cletus P.
- Sampaio, José Paulo
- Gonçalves, Paula
- Zhou, Xiaofan
- Shen, Xing-Xing
- Groenewald, Marizeth
- Rokas, Antonis
- Hittinger, Chris Todd
- Venue
- Science
- Published
- 2024-04-26
- Volume
- 384
- Issue
- 6694
- Pages
- eadj4503-eadj4503
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC11298794
- OpenAlex
- W4395447529
- Cited by
- 121
- References
- 197
- Citations by year
- 2026: 47 · 2025: 55 · 2024: 18 · 2023: 1
- FWCI
- 16.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Science (publishedVersion, cc-by)
- PubMed (publishedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion)
- CONICET Digital (CONICET) (publishedVersion, cc-by-nc-sa)
- PubMed Central (acceptedVersion)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- Funders
- U.S. Department of Energy (DESC0018409)
- National Human Genome Research Institute (T32HG002760)
- National Institute of General Medical Sciences (T32GM007133)
- National Institute of Allergy and Infectious Diseases (R56AI146096, R01AI153356)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Keywords
- niche breadth, carbon metabolism, nitrogen metabolism, metabolic specialization, genomic factors, metabolic pathway genes
- MeSH terms
- Ascomycota, Carbon, Nitrogen, Phylogeny, Genome, Fungal, Metabolic Networks and Pathways, Gene-Environment Interaction
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