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Genetic Context Significantly Influences the Maintenance and Evolution of Degenerate Pathways

Understanding the evolution of novel physiological traits is highly relevant for expanding the characterization and manipulation of biological systems. Acquisition of new traits can be achieved through horizontal gene transfer (HGT). Here, we investigate drivers that promote or deter the maintenance...

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Autores principales: Bruger, Eric L, Chubiz, Lon M, Rojas Echenique, José I, Renshaw, Caleb J, Espericueta, Nora Victoria, Draghi, Jeremy A, Marx, Christopher J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8214414/
https://www.ncbi.nlm.nih.gov/pubmed/33885815
http://dx.doi.org/10.1093/gbe/evab082
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author Bruger, Eric L
Chubiz, Lon M
Rojas Echenique, José I
Renshaw, Caleb J
Espericueta, Nora Victoria
Draghi, Jeremy A
Marx, Christopher J
author_facet Bruger, Eric L
Chubiz, Lon M
Rojas Echenique, José I
Renshaw, Caleb J
Espericueta, Nora Victoria
Draghi, Jeremy A
Marx, Christopher J
author_sort Bruger, Eric L
collection PubMed
description Understanding the evolution of novel physiological traits is highly relevant for expanding the characterization and manipulation of biological systems. Acquisition of new traits can be achieved through horizontal gene transfer (HGT). Here, we investigate drivers that promote or deter the maintenance of HGT-driven degeneracy, occurring when processes accomplish identical functions through nonidentical components. Subsequent evolution can optimize newly acquired functions; for example, beneficial alleles identified in an engineered Methylorubrum extorquens strain allowed it to utilize a “Foreign” formaldehyde oxidation pathway substituted for its Native pathway for methylotrophic growth. We examined the fitness consequences of interactions between these alleles when they were combined with the Native pathway or both (Dual) pathways. Unlike the Foreign pathway context where they evolved, these alleles were often neutral or deleterious when moved into these alternative genetic backgrounds. However, there were instances where combinations of multiple alleles resulted in higher fitness outcomes than individual allelic substitutions could provide. Importantly, the genetic context accompanying these allelic substitutions significantly altered the fitness landscape, shifting local fitness peaks and restricting the set of accessible evolutionary trajectories. These findings highlight how genetic context can negatively impact the probability of maintaining native and HGT-introduced functions together, making it difficult for degeneracy to evolve. However, in cases where the cost of maintaining degeneracy was mitigated by adding evolved alleles impacting the function of these pathways, we observed rare opportunities for pathway coevolution to occur. Together, our results highlight the importance of genetic context and resulting epistasis in retaining or losing HGT-acquired degenerate functions.
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spelling pubmed-82144142021-06-21 Genetic Context Significantly Influences the Maintenance and Evolution of Degenerate Pathways Bruger, Eric L Chubiz, Lon M Rojas Echenique, José I Renshaw, Caleb J Espericueta, Nora Victoria Draghi, Jeremy A Marx, Christopher J Genome Biol Evol Research Article Understanding the evolution of novel physiological traits is highly relevant for expanding the characterization and manipulation of biological systems. Acquisition of new traits can be achieved through horizontal gene transfer (HGT). Here, we investigate drivers that promote or deter the maintenance of HGT-driven degeneracy, occurring when processes accomplish identical functions through nonidentical components. Subsequent evolution can optimize newly acquired functions; for example, beneficial alleles identified in an engineered Methylorubrum extorquens strain allowed it to utilize a “Foreign” formaldehyde oxidation pathway substituted for its Native pathway for methylotrophic growth. We examined the fitness consequences of interactions between these alleles when they were combined with the Native pathway or both (Dual) pathways. Unlike the Foreign pathway context where they evolved, these alleles were often neutral or deleterious when moved into these alternative genetic backgrounds. However, there were instances where combinations of multiple alleles resulted in higher fitness outcomes than individual allelic substitutions could provide. Importantly, the genetic context accompanying these allelic substitutions significantly altered the fitness landscape, shifting local fitness peaks and restricting the set of accessible evolutionary trajectories. These findings highlight how genetic context can negatively impact the probability of maintaining native and HGT-introduced functions together, making it difficult for degeneracy to evolve. However, in cases where the cost of maintaining degeneracy was mitigated by adding evolved alleles impacting the function of these pathways, we observed rare opportunities for pathway coevolution to occur. Together, our results highlight the importance of genetic context and resulting epistasis in retaining or losing HGT-acquired degenerate functions. Oxford University Press 2021-04-22 /pmc/articles/PMC8214414/ /pubmed/33885815 http://dx.doi.org/10.1093/gbe/evab082 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) ), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Bruger, Eric L
Chubiz, Lon M
Rojas Echenique, José I
Renshaw, Caleb J
Espericueta, Nora Victoria
Draghi, Jeremy A
Marx, Christopher J
Genetic Context Significantly Influences the Maintenance and Evolution of Degenerate Pathways
title Genetic Context Significantly Influences the Maintenance and Evolution of Degenerate Pathways
title_full Genetic Context Significantly Influences the Maintenance and Evolution of Degenerate Pathways
title_fullStr Genetic Context Significantly Influences the Maintenance and Evolution of Degenerate Pathways
title_full_unstemmed Genetic Context Significantly Influences the Maintenance and Evolution of Degenerate Pathways
title_short Genetic Context Significantly Influences the Maintenance and Evolution of Degenerate Pathways
title_sort genetic context significantly influences the maintenance and evolution of degenerate pathways
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8214414/
https://www.ncbi.nlm.nih.gov/pubmed/33885815
http://dx.doi.org/10.1093/gbe/evab082
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