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A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH

The genome streamlining theory suggests that reduction of microbial genome size optimizes energy utilization in stressful environments. Although this hypothesis has been explored in several cases of low-nutrient (oligotrophic) and high-temperature environments, little work has been carried out on mi...

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Autores principales: Cortez, Diego, Neira, Gonzalo, González, Carolina, Vergara, Eva, Holmes, David S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8978632/
https://www.ncbi.nlm.nih.gov/pubmed/35387071
http://dx.doi.org/10.3389/fmicb.2022.803241
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author Cortez, Diego
Neira, Gonzalo
González, Carolina
Vergara, Eva
Holmes, David S.
author_facet Cortez, Diego
Neira, Gonzalo
González, Carolina
Vergara, Eva
Holmes, David S.
author_sort Cortez, Diego
collection PubMed
description The genome streamlining theory suggests that reduction of microbial genome size optimizes energy utilization in stressful environments. Although this hypothesis has been explored in several cases of low-nutrient (oligotrophic) and high-temperature environments, little work has been carried out on microorganisms from low-pH environments, and what has been reported is inconclusive. In this study, we performed a large-scale comparative genomics investigation of more than 260 bacterial high-quality genome sequences of acidophiles, together with genomes of their closest phylogenetic relatives that live at circum-neutral pH. A statistically supported correlation is reported between reduction of genome size and decreasing pH that we demonstrate is due to gene loss and reduced gene sizes. This trend is independent from other genome size constraints such as temperature and G + C content. Genome streamlining in the evolution of acidophilic bacteria is thus supported by our results. The analyses of predicted Clusters of Orthologous Genes (COG) categories and subcellular location predictions indicate that acidophiles have a lower representation of genes encoding extracellular proteins, signal transduction mechanisms, and proteins with unknown function but are enriched in inner membrane proteins, chaperones, basic metabolism, and core cellular functions. Contrary to other reports for genome streamlining, there was no significant change in paralog frequencies across pH. However, a detailed analysis of COG categories revealed a higher proportion of genes in acidophiles in the following categories: “replication and repair,” “amino acid transport,” and “intracellular trafficking”. This study brings increasing clarity regarding the genomic adaptations of acidophiles to life at low pH while putting elements, such as the reduction of average gene size, under the spotlight of streamlining theory.
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spelling pubmed-89786322022-04-05 A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH Cortez, Diego Neira, Gonzalo González, Carolina Vergara, Eva Holmes, David S. Front Microbiol Microbiology The genome streamlining theory suggests that reduction of microbial genome size optimizes energy utilization in stressful environments. Although this hypothesis has been explored in several cases of low-nutrient (oligotrophic) and high-temperature environments, little work has been carried out on microorganisms from low-pH environments, and what has been reported is inconclusive. In this study, we performed a large-scale comparative genomics investigation of more than 260 bacterial high-quality genome sequences of acidophiles, together with genomes of their closest phylogenetic relatives that live at circum-neutral pH. A statistically supported correlation is reported between reduction of genome size and decreasing pH that we demonstrate is due to gene loss and reduced gene sizes. This trend is independent from other genome size constraints such as temperature and G + C content. Genome streamlining in the evolution of acidophilic bacteria is thus supported by our results. The analyses of predicted Clusters of Orthologous Genes (COG) categories and subcellular location predictions indicate that acidophiles have a lower representation of genes encoding extracellular proteins, signal transduction mechanisms, and proteins with unknown function but are enriched in inner membrane proteins, chaperones, basic metabolism, and core cellular functions. Contrary to other reports for genome streamlining, there was no significant change in paralog frequencies across pH. However, a detailed analysis of COG categories revealed a higher proportion of genes in acidophiles in the following categories: “replication and repair,” “amino acid transport,” and “intracellular trafficking”. This study brings increasing clarity regarding the genomic adaptations of acidophiles to life at low pH while putting elements, such as the reduction of average gene size, under the spotlight of streamlining theory. Frontiers Media S.A. 2022-03-21 /pmc/articles/PMC8978632/ /pubmed/35387071 http://dx.doi.org/10.3389/fmicb.2022.803241 Text en Copyright © 2022 Cortez, Neira, González, Vergara and Holmes. https://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
Cortez, Diego
Neira, Gonzalo
González, Carolina
Vergara, Eva
Holmes, David S.
A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH
title A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH
title_full A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH
title_fullStr A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH
title_full_unstemmed A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH
title_short A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH
title_sort large-scale genome-based survey of acidophilic bacteria suggests that genome streamlining is an adaption for life at low ph
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8978632/
https://www.ncbi.nlm.nih.gov/pubmed/35387071
http://dx.doi.org/10.3389/fmicb.2022.803241
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