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

Dana A. Opulente; Abigail Leavitt LaBella; Marie Claire Harrison; John F. Wolters; Chao Liu; Yonglin Li; Jacek Kominek; Jacob L. Steenwyk; Hayley R. Stoneman; Jenna VanDenAvond; Caroline R. Miller; Quinn K. Langdon; Margarida Silva; Carla Gonçalves; Emily J. Ubbelohde; Yuanning Li; Kelly V. Buh; Martin Jarzyna; Max A.B. Haase; Carlos A. Rosa; Neža Čadež; Diego Libkind; Jeremy H. DeVirgilio; Amanda Beth Hulfachor; Cletus P. Kurtzman; José Paulo Sampaio; Paula Gonçalves; Xiaofan Zhou; Xing Xing Shen; Marizeth Groenewald; Antonis Rokas; Chris Todd Hittinger

doi:10.1126/science.adj4503

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

Dana A. Opulente, Abigail Leavitt LaBella, Marie Claire Harrison, John F. Wolters, Chao Liu, Yonglin Li, Jacek Kominek, Jacob L. Steenwyk, Hayley R. Stoneman, Jenna VanDenAvond, Caroline R. Miller, Quinn K. Langdon, Margarida Silva, Carla Gonçalves, Emily J. Ubbelohde, Yuanning Li, Kelly V. Buh, Martin Jarzyna, Max A.B. Haase, Carlos A. RosaNeža Čadež, Diego Libkind, Jeremy H. DeVirgilio, Amanda Beth Hulfachor, Cletus P. Kurtzman, José Paulo Sampaio, Paula Gonçalves, Xiaofan Zhou, Xing Xing Shen, Marizeth Groenewald, Antonis Rokas^*, Chris Todd Hittinger^*

^*Bijbehorende auteur voor dit werk

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

9 Citaten (Scopus)

Samenvatting

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.

Originele taal-2	Engels
Artikelnummer	eadj4503
Tijdschrift	Science
Volume	384
Nummer van het tijdschrift	6694
DOI's	https://doi.org/10.1126/science.adj4503
Status	Gepubliceerd - 26 apr. 2024

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10.1126/science.adj4503

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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., ... Hittinger, C. T. (2024). Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts. Science, 384(6694), Artikel eadj4503. https://doi.org/10.1126/science.adj4503

@article{6839b0a09bec4841bf98dd502e67274a,

title = "Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts",

abstract = "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.",

author = "Opulente, {Dana A.} and LaBella, {Abigail Leavitt} and Harrison, {Marie Claire} and Wolters, {John F.} and Chao Liu and Yonglin Li and Jacek Kominek and Steenwyk, {Jacob L.} and Stoneman, {Hayley R.} and Jenna VanDenAvond and Miller, {Caroline R.} and Langdon, {Quinn K.} and Margarida Silva and Carla Gon{\c c}alves and Ubbelohde, {Emily J.} and Yuanning Li and Buh, {Kelly V.} and Martin Jarzyna and Haase, {Max A.B.} and Rosa, {Carlos A.} and Ne{\v z}a {\v C}ade{\v z} and Diego Libkind and DeVirgilio, {Jeremy H.} and Hulfachor, {Amanda Beth} and Kurtzman, {Cletus P.} and Sampaio, {Jos{\'e} Paulo} and Paula Gon{\c c}alves and Xiaofan Zhou and Shen, {Xing Xing} and Marizeth Groenewald and Antonis Rokas and Hittinger, {Chris Todd}",

year = "2024",

month = apr,

day = "26",

doi = "10.1126/science.adj4503",

language = "English",

volume = "384",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science (AAAS)",

number = "6694",

}

Opulente, DA, LaBella, AL, Harrison, MC, Wolters, JF, Liu, C, Li, Y, Kominek, J, Steenwyk, JL, Stoneman, HR, VanDenAvond, J, Miller, CR, Langdon, QK, Silva, M, Gonçalves, C, Ubbelohde, EJ, Li, Y, Buh, KV, Jarzyna, M, Haase, MAB, Rosa, CA, Čadež, N, Libkind, D, DeVirgilio, JH, Hulfachor, AB, Kurtzman, CP, Sampaio, JP, Gonçalves, P, Zhou, X, Shen, XX, Groenewald, M, Rokas, A & Hittinger, CT 2024, 'Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts', Science, vol. 384, nr. 6694, eadj4503. https://doi.org/10.1126/science.adj4503

TY - JOUR

T1 - Genomic factors shape carbon and nitrogen metabolic niche breadth across Saccharomycotina yeasts

AU - Opulente, Dana A.

AU - LaBella, Abigail Leavitt

AU - Harrison, Marie Claire

AU - Wolters, John F.

AU - Liu, Chao

AU - Li, Yonglin

AU - Kominek, Jacek

AU - Steenwyk, Jacob L.

AU - Stoneman, Hayley R.

AU - VanDenAvond, Jenna

AU - Miller, Caroline R.

AU - Langdon, Quinn K.

AU - Silva, Margarida

AU - Gonçalves, Carla

AU - Ubbelohde, Emily J.

AU - Li, Yuanning

AU - Buh, Kelly V.

AU - Jarzyna, Martin

AU - Haase, Max A.B.

AU - Rosa, Carlos A.

AU - Čadež, Neža

AU - Libkind, Diego

AU - DeVirgilio, Jeremy H.

AU - Hulfachor, Amanda Beth

AU - Kurtzman, Cletus P.

AU - Sampaio, José Paulo

AU - Gonçalves, Paula

AU - Zhou, Xiaofan

AU - Shen, Xing Xing

AU - Groenewald, Marizeth

AU - Rokas, Antonis

AU - Hittinger, Chris Todd

PY - 2024/4/26

Y1 - 2024/4/26

N2 - 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.

AB - 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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U2 - 10.1126/science.adj4503

DO - 10.1126/science.adj4503

M3 - Article

C2 - 38662846

AN - SCOPUS:85191492230

SN - 0036-8075

VL - 384

JO - Science

JF - Science

IS - 6694

M1 - eadj4503

ER -