Mutational Pathways and Trade-Offs Between HisA and TrpF Functions: Implications for Evolution via Gene Duplication and Divergence

When a new activity evolves by changes in a pre-existing enzyme this is likely to reduce the original activity, generating a functional trade-off. The properties of this trade-off will affect the continued evolution of both functions. If the trade-off is strong, gene duplication and subsequent diver...

Full description

Bibliographic Details
Main Authors: Erik Lundin, Joakim Näsvall, Dan I. Andersson
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.588235/full
_version_ 1819228086977167360
author Erik Lundin
Joakim Näsvall
Dan I. Andersson
author_facet Erik Lundin
Joakim Näsvall
Dan I. Andersson
author_sort Erik Lundin
collection DOAJ
description When a new activity evolves by changes in a pre-existing enzyme this is likely to reduce the original activity, generating a functional trade-off. The properties of this trade-off will affect the continued evolution of both functions. If the trade-off is strong, gene duplication and subsequent divergence would be favored whereas if the trade-off is weak a bi-functional enzyme could evolve that performs both functions. We previously showed that when a bi-functional HisA enzyme was evolved under selection for both HisA and TrpF functions, evolution mainly proceeded via duplication-divergence and specialization, implying that the trade-off is strong between these two functions. Here, we examined this hypothesis by identifying the mutational pathways (i.e., the mutational landscape) in the Salmonella enterica HisA enzyme that conferred a TrpF-like activity, and examining the trade-offs between the original and new activity. For the HisA enzyme there are many different paths toward the new TrpF function, each with its own unique trade-off. A total of 16 single mutations resulted in HisA enzyme variants that acquired TrpF activity and only three of them maintained HisA activity. Twelve mutants were evolved further toward increased TrpF activity and during evolution toward improved TrpF activity the original HisA activity was completely lost in all lineages. We propose that, aside from various relevant ecological factors, two main genetic factors influence whether evolution of a new function proceeds via duplication – divergence (specialization) or by evolution of a generalist: (i) the relative mutation supply of the two pathways and (ii) the shape of the trade-off curve between the native and new function.
first_indexed 2024-12-23T10:51:42Z
format Article
id doaj.art-e545a50af4d64a17958899625dd27593
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-23T10:51:42Z
publishDate 2020-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-e545a50af4d64a17958899625dd275932022-12-21T17:49:53ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-10-011110.3389/fmicb.2020.588235588235Mutational Pathways and Trade-Offs Between HisA and TrpF Functions: Implications for Evolution via Gene Duplication and DivergenceErik LundinJoakim NäsvallDan I. AnderssonWhen a new activity evolves by changes in a pre-existing enzyme this is likely to reduce the original activity, generating a functional trade-off. The properties of this trade-off will affect the continued evolution of both functions. If the trade-off is strong, gene duplication and subsequent divergence would be favored whereas if the trade-off is weak a bi-functional enzyme could evolve that performs both functions. We previously showed that when a bi-functional HisA enzyme was evolved under selection for both HisA and TrpF functions, evolution mainly proceeded via duplication-divergence and specialization, implying that the trade-off is strong between these two functions. Here, we examined this hypothesis by identifying the mutational pathways (i.e., the mutational landscape) in the Salmonella enterica HisA enzyme that conferred a TrpF-like activity, and examining the trade-offs between the original and new activity. For the HisA enzyme there are many different paths toward the new TrpF function, each with its own unique trade-off. A total of 16 single mutations resulted in HisA enzyme variants that acquired TrpF activity and only three of them maintained HisA activity. Twelve mutants were evolved further toward increased TrpF activity and during evolution toward improved TrpF activity the original HisA activity was completely lost in all lineages. We propose that, aside from various relevant ecological factors, two main genetic factors influence whether evolution of a new function proceeds via duplication – divergence (specialization) or by evolution of a generalist: (i) the relative mutation supply of the two pathways and (ii) the shape of the trade-off curve between the native and new function.https://www.frontiersin.org/article/10.3389/fmicb.2020.588235/fullduplicationdivergencetrade-offHISATrpFSalmonella enterica
spellingShingle Erik Lundin
Joakim Näsvall
Dan I. Andersson
Mutational Pathways and Trade-Offs Between HisA and TrpF Functions: Implications for Evolution via Gene Duplication and Divergence
Frontiers in Microbiology
duplication
divergence
trade-off
HISA
TrpF
Salmonella enterica
title Mutational Pathways and Trade-Offs Between HisA and TrpF Functions: Implications for Evolution via Gene Duplication and Divergence
title_full Mutational Pathways and Trade-Offs Between HisA and TrpF Functions: Implications for Evolution via Gene Duplication and Divergence
title_fullStr Mutational Pathways and Trade-Offs Between HisA and TrpF Functions: Implications for Evolution via Gene Duplication and Divergence
title_full_unstemmed Mutational Pathways and Trade-Offs Between HisA and TrpF Functions: Implications for Evolution via Gene Duplication and Divergence
title_short Mutational Pathways and Trade-Offs Between HisA and TrpF Functions: Implications for Evolution via Gene Duplication and Divergence
title_sort mutational pathways and trade offs between hisa and trpf functions implications for evolution via gene duplication and divergence
topic duplication
divergence
trade-off
HISA
TrpF
Salmonella enterica
url https://www.frontiersin.org/article/10.3389/fmicb.2020.588235/full
work_keys_str_mv AT eriklundin mutationalpathwaysandtradeoffsbetweenhisaandtrpffunctionsimplicationsforevolutionviageneduplicationanddivergence
AT joakimnasvall mutationalpathwaysandtradeoffsbetweenhisaandtrpffunctionsimplicationsforevolutionviageneduplicationanddivergence
AT daniandersson mutationalpathwaysandtradeoffsbetweenhisaandtrpffunctionsimplicationsforevolutionviageneduplicationanddivergence