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Article: Sign epistasis limits evolutionary trade-offs at the confluence of single- and multi-carbon metabolism in Methylobacterium extorquens AM1

TitleSign epistasis limits evolutionary trade-offs at the confluence of single- and multi-carbon metabolism in Methylobacterium extorquens AM1
Authors
KeywordsAntagonistic pleiotropy
ecological specialization
experimental evolution
formate-tetrahydrofolate ligase
loss of function
methylotrophy
Issue Date2014
PublisherSociety for the Study of Evolution.
Citation
Evolution: International Journal of Organic Evolution, 2014, v. 68 n. 3, p. 761-771 How to Cite?
AbstractAdaptation of one set of traits is often accompanied by attenuation of traits important in other selective environments, leading to fitness trade-offs. The mechanisms that either promote or prevent the emergence of trade-offs remain largely unknown, and are difficult to discern in most systems. Here, we investigate the basis of trade-offs that emerged during experimental evolution of Methylobacterium extorquens AM1 to distinct growth substrates. After 1500 generations of adaptation to a multi-carbon substrate, succinate (S), many lineages had lost the ability to use one-carbon compounds such as methanol (M), generating a mixture of M(+) and M(-) evolved phenotypes. We show that trade-offs in M(-) strains consistently arise via antagonistic pleiotropy through recurrent selection for loss-of-function mutations to ftfL (formate-tetrahydrofolate ligase), which improved growth on S while simultaneously eliminating growth on M. But if loss of FtfL was beneficial, why were M trade-offs not found in all populations? We discovered that eliminating FtfL was not universally beneficial on S, as it was neutral or even deleterious in certain evolved lineages that remained M(+) . This suggests that sign epistasis with earlier arising mutations prevented the emergence of mutations that drove trade-offs through antagonistic pleiotropy, limiting the evolution of metabolic specialists in some populations.
Persistent Identifierhttp://hdl.handle.net/10722/226668
ISSN
2015 Impact Factor: 4.007
2015 SCImago Journal Rankings: 3.204
ISI Accession Number ID

 

DC FieldValueLanguage
dc.contributor.authorCarroll, SM-
dc.contributor.authorLee, MC-
dc.contributor.authorMarx, CJ-
dc.date.accessioned2016-06-22T07:28:51Z-
dc.date.available2016-06-22T07:28:51Z-
dc.date.issued2014-
dc.identifier.citationEvolution: International Journal of Organic Evolution, 2014, v. 68 n. 3, p. 761-771-
dc.identifier.issn0014-3820-
dc.identifier.urihttp://hdl.handle.net/10722/226668-
dc.description.abstractAdaptation of one set of traits is often accompanied by attenuation of traits important in other selective environments, leading to fitness trade-offs. The mechanisms that either promote or prevent the emergence of trade-offs remain largely unknown, and are difficult to discern in most systems. Here, we investigate the basis of trade-offs that emerged during experimental evolution of Methylobacterium extorquens AM1 to distinct growth substrates. After 1500 generations of adaptation to a multi-carbon substrate, succinate (S), many lineages had lost the ability to use one-carbon compounds such as methanol (M), generating a mixture of M(+) and M(-) evolved phenotypes. We show that trade-offs in M(-) strains consistently arise via antagonistic pleiotropy through recurrent selection for loss-of-function mutations to ftfL (formate-tetrahydrofolate ligase), which improved growth on S while simultaneously eliminating growth on M. But if loss of FtfL was beneficial, why were M trade-offs not found in all populations? We discovered that eliminating FtfL was not universally beneficial on S, as it was neutral or even deleterious in certain evolved lineages that remained M(+) . This suggests that sign epistasis with earlier arising mutations prevented the emergence of mutations that drove trade-offs through antagonistic pleiotropy, limiting the evolution of metabolic specialists in some populations.-
dc.languageeng-
dc.publisherSociety for the Study of Evolution.-
dc.relation.ispartofEvolution; International Journal of Organic Evolution-
dc.subjectAntagonistic pleiotropy-
dc.subjectecological specialization-
dc.subjectexperimental evolution-
dc.subjectformate-tetrahydrofolate ligase-
dc.subjectloss of function-
dc.subjectmethylotrophy-
dc.titleSign epistasis limits evolutionary trade-offs at the confluence of single- and multi-carbon metabolism in Methylobacterium extorquens AM1-
dc.typeArticle-
dc.description.naturelink_to_subscribed_fulltext-
dc.identifier.doi10.1111/evo.12301-
dc.identifier.pmid24164359-
dc.identifier.volume68-
dc.identifier.issue3-
dc.identifier.spage761-
dc.identifier.epage771-
dc.identifier.isiWOS:000332046700013-
dc.publisher.placeUnited States-

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