Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection

Abstract Yeasts are known to have versatile metabolic traits, while how these metabolic traits have evolved has not been elucidated systematically. We performed integrative evolution analysis to investigate how genomic evolution determines trait generation by reconstructing genome‐scale metabolic mo...

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Autores principales:	Hongzhong Lu, Feiran Li, Le Yuan, Iván Domenzain, Rosemary Yu, Hao Wang, Gang Li, Yu Chen, Boyang Ji, Eduard J Kerkhoven, Jens Nielsen
Formato:	article
Lenguaje:	EN
Publicado:	Wiley 2021
Materias:	genome analysis genome‐scale metabolic models metabolic innovation systems biology Biology (General) QH301-705.5 Medicine (General) R5-920
Acceso en línea:	https://doaj.org/article/1b0b1695d181441c8971f35c8d7fd4cc
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spelling	oai:doaj.org-article:1b0b1695d181441c8971f35c8d7fd4cc2021-11-11T11:30:47ZYeast metabolic innovations emerged via expanded metabolic network and gene positive selection1744-429210.15252/msb.202110427https://doaj.org/article/1b0b1695d181441c8971f35c8d7fd4cc2021-10-01T00:00:00Zhttps://doi.org/10.15252/msb.202110427https://doaj.org/toc/1744-4292Abstract Yeasts are known to have versatile metabolic traits, while how these metabolic traits have evolved has not been elucidated systematically. We performed integrative evolution analysis to investigate how genomic evolution determines trait generation by reconstructing genome‐scale metabolic models (GEMs) for 332 yeasts. These GEMs could comprehensively characterize trait diversity and predict enzyme functionality, thereby signifying that sequence‐level evolution has shaped reaction networks towards new metabolic functions. Strikingly, using GEMs, we can mechanistically map different evolutionary events, e.g. horizontal gene transfer and gene duplication, onto relevant subpathways to explain metabolic plasticity. This demonstrates that gene family expansion and enzyme promiscuity are prominent mechanisms for metabolic trait gains, while GEM simulations reveal that additional factors, such as gene loss from distant pathways, contribute to trait losses. Furthermore, our analysis could pinpoint to specific genes and pathways that have been under positive selection and relevant for the formulation of complex metabolic traits, i.e. thermotolerance and the Crabtree effect. Our findings illustrate how multidimensional evolution in both metabolic network structure and individual enzymes drives phenotypic variations.Hongzhong LuFeiran LiLe YuanIván DomenzainRosemary YuHao WangGang LiYu ChenBoyang JiEduard J KerkhovenJens NielsenWileyarticlegenome analysisgenome‐scale metabolic modelsmetabolic innovationsystems biologyBiology (General)QH301-705.5Medicine (General)R5-920ENMolecular Systems Biology, Vol 17, Iss 10, Pp n/a-n/a (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	genome analysis genome‐scale metabolic models metabolic innovation systems biology Biology (General) QH301-705.5 Medicine (General) R5-920
spellingShingle	genome analysis genome‐scale metabolic models metabolic innovation systems biology Biology (General) QH301-705.5 Medicine (General) R5-920 Hongzhong Lu Feiran Li Le Yuan Iván Domenzain Rosemary Yu Hao Wang Gang Li Yu Chen Boyang Ji Eduard J Kerkhoven Jens Nielsen Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection
description	Abstract Yeasts are known to have versatile metabolic traits, while how these metabolic traits have evolved has not been elucidated systematically. We performed integrative evolution analysis to investigate how genomic evolution determines trait generation by reconstructing genome‐scale metabolic models (GEMs) for 332 yeasts. These GEMs could comprehensively characterize trait diversity and predict enzyme functionality, thereby signifying that sequence‐level evolution has shaped reaction networks towards new metabolic functions. Strikingly, using GEMs, we can mechanistically map different evolutionary events, e.g. horizontal gene transfer and gene duplication, onto relevant subpathways to explain metabolic plasticity. This demonstrates that gene family expansion and enzyme promiscuity are prominent mechanisms for metabolic trait gains, while GEM simulations reveal that additional factors, such as gene loss from distant pathways, contribute to trait losses. Furthermore, our analysis could pinpoint to specific genes and pathways that have been under positive selection and relevant for the formulation of complex metabolic traits, i.e. thermotolerance and the Crabtree effect. Our findings illustrate how multidimensional evolution in both metabolic network structure and individual enzymes drives phenotypic variations.
format	article
author	Hongzhong Lu Feiran Li Le Yuan Iván Domenzain Rosemary Yu Hao Wang Gang Li Yu Chen Boyang Ji Eduard J Kerkhoven Jens Nielsen
author_facet	Hongzhong Lu Feiran Li Le Yuan Iván Domenzain Rosemary Yu Hao Wang Gang Li Yu Chen Boyang Ji Eduard J Kerkhoven Jens Nielsen
author_sort	Hongzhong Lu
title	Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection
title_short	Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection
title_full	Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection
title_fullStr	Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection
title_full_unstemmed	Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection
title_sort	yeast metabolic innovations emerged via expanded metabolic network and gene positive selection
publisher	Wiley
publishDate	2021
url	https://doaj.org/article/1b0b1695d181441c8971f35c8d7fd4cc
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Yeast metabolic innovations emerged via expanded metabolic network and gene positive selection

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