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Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem

The ribosomal RNA (rrn) operon is a key suite of genes related to the production of protein synthesis machinery and thus to bacterial growth physiology. Experimental evidence has suggested an intrinsic relationship between the number of copies of this operon and environmental resource availability,...

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Autores principales: Valdivia-Anistro, Jorge A., Eguiarte-Fruns, Luis E., Delgado-Sapién, Gabriela, Márquez-Zacarías, Pedro, Gasca-Pineda, Jaime, Learned, Jennifer, Elser, James J., Olmedo-Alvarez, Gabriela, Souza, Valeria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4700252/
https://www.ncbi.nlm.nih.gov/pubmed/26779143
http://dx.doi.org/10.3389/fmicb.2015.01486
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author Valdivia-Anistro, Jorge A.
Eguiarte-Fruns, Luis E.
Delgado-Sapién, Gabriela
Márquez-Zacarías, Pedro
Gasca-Pineda, Jaime
Learned, Jennifer
Elser, James J.
Olmedo-Alvarez, Gabriela
Souza, Valeria
author_facet Valdivia-Anistro, Jorge A.
Eguiarte-Fruns, Luis E.
Delgado-Sapién, Gabriela
Márquez-Zacarías, Pedro
Gasca-Pineda, Jaime
Learned, Jennifer
Elser, James J.
Olmedo-Alvarez, Gabriela
Souza, Valeria
author_sort Valdivia-Anistro, Jorge A.
collection PubMed
description The ribosomal RNA (rrn) operon is a key suite of genes related to the production of protein synthesis machinery and thus to bacterial growth physiology. Experimental evidence has suggested an intrinsic relationship between the number of copies of this operon and environmental resource availability, especially the availability of phosphorus (P), because bacteria that live in oligotrophic ecosystems usually have few rrn operons and a slow growth rate. The Cuatro Ciénegas Basin (CCB) is a complex aquatic ecosystem that contains an unusually high microbial diversity that is able to persist under highly oligotrophic conditions. These environmental conditions impose a variety of strong selective pressures that shape the genome dynamics of their inhabitants. The genus Bacillus is one of the most abundant cultivable bacterial groups in the CCB and usually possesses a relatively large number of rrn operon copies (6–15 copies). The main goal of this study was to analyze the variation in the number of rrn operon copies of Bacillus in the CCB and to assess their growth-related properties as well as their stoichiometric balance (N and P content). We defined 18 phylogenetic groups within the Bacilli clade and documented a range of from six to 14 copies of the rrn operon. The growth dynamic of these Bacilli was heterogeneous and did not show a direct relation to the number of operon copies. Physiologically, our results were not consistent with the Growth Rate Hypothesis, since the copies of the rrn operon were decoupled from growth rate. However, we speculate that the diversity of the growth properties of these Bacilli as well as the low P content of their cells in an ample range of rrn copy number is an adaptive response to oligotrophy of the CCB and could represent an ecological mechanism that allows these taxa to coexist. These findings increase the knowledge of the variability in the number of copies of the rrn operon in the genus Bacillus and give insights about the physiology of this bacterial group under extreme oligotrophic conditions.
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spelling pubmed-47002522016-01-15 Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem Valdivia-Anistro, Jorge A. Eguiarte-Fruns, Luis E. Delgado-Sapién, Gabriela Márquez-Zacarías, Pedro Gasca-Pineda, Jaime Learned, Jennifer Elser, James J. Olmedo-Alvarez, Gabriela Souza, Valeria Front Microbiol Microbiology The ribosomal RNA (rrn) operon is a key suite of genes related to the production of protein synthesis machinery and thus to bacterial growth physiology. Experimental evidence has suggested an intrinsic relationship between the number of copies of this operon and environmental resource availability, especially the availability of phosphorus (P), because bacteria that live in oligotrophic ecosystems usually have few rrn operons and a slow growth rate. The Cuatro Ciénegas Basin (CCB) is a complex aquatic ecosystem that contains an unusually high microbial diversity that is able to persist under highly oligotrophic conditions. These environmental conditions impose a variety of strong selective pressures that shape the genome dynamics of their inhabitants. The genus Bacillus is one of the most abundant cultivable bacterial groups in the CCB and usually possesses a relatively large number of rrn operon copies (6–15 copies). The main goal of this study was to analyze the variation in the number of rrn operon copies of Bacillus in the CCB and to assess their growth-related properties as well as their stoichiometric balance (N and P content). We defined 18 phylogenetic groups within the Bacilli clade and documented a range of from six to 14 copies of the rrn operon. The growth dynamic of these Bacilli was heterogeneous and did not show a direct relation to the number of operon copies. Physiologically, our results were not consistent with the Growth Rate Hypothesis, since the copies of the rrn operon were decoupled from growth rate. However, we speculate that the diversity of the growth properties of these Bacilli as well as the low P content of their cells in an ample range of rrn copy number is an adaptive response to oligotrophy of the CCB and could represent an ecological mechanism that allows these taxa to coexist. These findings increase the knowledge of the variability in the number of copies of the rrn operon in the genus Bacillus and give insights about the physiology of this bacterial group under extreme oligotrophic conditions. Frontiers Media S.A. 2016-01-05 /pmc/articles/PMC4700252/ /pubmed/26779143 http://dx.doi.org/10.3389/fmicb.2015.01486 Text en Copyright © 2016 Valdivia-Anistro, Eguiarte-Fruns, Delgado-Sapién, Márquez-Zacarías, Gasca-Pineda, Learned, Elser, Olmedo-Alvarez 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) or licensor 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
Valdivia-Anistro, Jorge A.
Eguiarte-Fruns, Luis E.
Delgado-Sapién, Gabriela
Márquez-Zacarías, Pedro
Gasca-Pineda, Jaime
Learned, Jennifer
Elser, James J.
Olmedo-Alvarez, Gabriela
Souza, Valeria
Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem
title Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem
title_full Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem
title_fullStr Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem
title_full_unstemmed Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem
title_short Variability of rRNA Operon Copy Number and Growth Rate Dynamics of Bacillus Isolated from an Extremely Oligotrophic Aquatic Ecosystem
title_sort variability of rrna operon copy number and growth rate dynamics of bacillus isolated from an extremely oligotrophic aquatic ecosystem
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4700252/
https://www.ncbi.nlm.nih.gov/pubmed/26779143
http://dx.doi.org/10.3389/fmicb.2015.01486
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