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Evolutionary Rescue of an Environmental Pseudomonas otitidis in Response to Anthropogenic Perturbation

Anthropogenic perturbations introduce novel selective pressures to natural environments, impacting the genomic variability of organisms and thus altering the evolutionary trajectory of populations. Water overexploitation for agricultural purposes and defective policies in Cuatro Cienegas, Coahuila,...

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Autores principales: García-Ulloa, Manuel II, Escalante, Ana Elena, Moreno-Letelier, Alejandra, Eguiarte, Luis E., Souza, Valeria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7856823/
https://www.ncbi.nlm.nih.gov/pubmed/33552002
http://dx.doi.org/10.3389/fmicb.2020.563885
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author García-Ulloa, Manuel II
Escalante, Ana Elena
Moreno-Letelier, Alejandra
Eguiarte, Luis E.
Souza, Valeria
author_facet García-Ulloa, Manuel II
Escalante, Ana Elena
Moreno-Letelier, Alejandra
Eguiarte, Luis E.
Souza, Valeria
author_sort García-Ulloa, Manuel II
collection PubMed
description Anthropogenic perturbations introduce novel selective pressures to natural environments, impacting the genomic variability of organisms and thus altering the evolutionary trajectory of populations. Water overexploitation for agricultural purposes and defective policies in Cuatro Cienegas, Coahuila, Mexico, have strongly impacted its water reservoir, pushing entire hydrological systems to the brink of extinction along with their native populations. Here, we studied the effects of continuous water overexploitation on an environmental aquatic lineage of Pseudomonas otitidis over a 13-year period which encompasses three desiccation events. By comparing the genomes of a population sample from 2003 (original state) and 2015 (perturbed state), we analyzed the demographic history and evolutionary response to perturbation of this lineage. Through coalescent simulations, we obtained a demographic model of contraction-expansion-contraction which points to the occurrence of an evolutionary rescue event. Loss of genomic and nucleotide variation alongside an increment in mean and variance of Tajima’s D, characteristic of sudden population expansions, support this observation. In addition, a significant increase in recombination rate (R/θ) was observed, pointing to horizontal gene transfer playing a role in population recovery. Furthermore, the gain of phosphorylation, DNA recombination, small-molecule metabolism and transport and loss of biosynthetic and regulatory genes suggest a functional shift in response to the environmental perturbation. Despite subsequent sampling events in the studied site, no pseudomonad was found until the lagoon completely dried in 2017. We speculate about the causes of P. otitidis final decline or possible extinction. Overall our results are evidence of adaptive responses at the genomic level of bacterial populations in a heavily exploited aquifer.
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spelling pubmed-78568232021-02-04 Evolutionary Rescue of an Environmental Pseudomonas otitidis in Response to Anthropogenic Perturbation García-Ulloa, Manuel II Escalante, Ana Elena Moreno-Letelier, Alejandra Eguiarte, Luis E. Souza, Valeria Front Microbiol Microbiology Anthropogenic perturbations introduce novel selective pressures to natural environments, impacting the genomic variability of organisms and thus altering the evolutionary trajectory of populations. Water overexploitation for agricultural purposes and defective policies in Cuatro Cienegas, Coahuila, Mexico, have strongly impacted its water reservoir, pushing entire hydrological systems to the brink of extinction along with their native populations. Here, we studied the effects of continuous water overexploitation on an environmental aquatic lineage of Pseudomonas otitidis over a 13-year period which encompasses three desiccation events. By comparing the genomes of a population sample from 2003 (original state) and 2015 (perturbed state), we analyzed the demographic history and evolutionary response to perturbation of this lineage. Through coalescent simulations, we obtained a demographic model of contraction-expansion-contraction which points to the occurrence of an evolutionary rescue event. Loss of genomic and nucleotide variation alongside an increment in mean and variance of Tajima’s D, characteristic of sudden population expansions, support this observation. In addition, a significant increase in recombination rate (R/θ) was observed, pointing to horizontal gene transfer playing a role in population recovery. Furthermore, the gain of phosphorylation, DNA recombination, small-molecule metabolism and transport and loss of biosynthetic and regulatory genes suggest a functional shift in response to the environmental perturbation. Despite subsequent sampling events in the studied site, no pseudomonad was found until the lagoon completely dried in 2017. We speculate about the causes of P. otitidis final decline or possible extinction. Overall our results are evidence of adaptive responses at the genomic level of bacterial populations in a heavily exploited aquifer. Frontiers Media S.A. 2021-01-18 /pmc/articles/PMC7856823/ /pubmed/33552002 http://dx.doi.org/10.3389/fmicb.2020.563885 Text en Copyright © 2021 García-Ulloa, Escalante, Moreno-Letelier, Eguiarte and Souza. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
García-Ulloa, Manuel II
Escalante, Ana Elena
Moreno-Letelier, Alejandra
Eguiarte, Luis E.
Souza, Valeria
Evolutionary Rescue of an Environmental Pseudomonas otitidis in Response to Anthropogenic Perturbation
title Evolutionary Rescue of an Environmental Pseudomonas otitidis in Response to Anthropogenic Perturbation
title_full Evolutionary Rescue of an Environmental Pseudomonas otitidis in Response to Anthropogenic Perturbation
title_fullStr Evolutionary Rescue of an Environmental Pseudomonas otitidis in Response to Anthropogenic Perturbation
title_full_unstemmed Evolutionary Rescue of an Environmental Pseudomonas otitidis in Response to Anthropogenic Perturbation
title_short Evolutionary Rescue of an Environmental Pseudomonas otitidis in Response to Anthropogenic Perturbation
title_sort evolutionary rescue of an environmental pseudomonas otitidis in response to anthropogenic perturbation
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7856823/
https://www.ncbi.nlm.nih.gov/pubmed/33552002
http://dx.doi.org/10.3389/fmicb.2020.563885
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