Bacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements

ABSTRACT Horizontal gene transfer (HGT) promotes the spread of genes within bacterial communities. Among the HGT mechanisms, natural transformation stands out as being encoded by the bacterial core genome. Natural transformation is often viewed as a way to acquire new genes and to generate genetic m...

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Autores principales:	Gabriel Carvalho, David Fouchet, Gonché Danesh, Anne-Sophie Godeux, Maria-Halima Laaberki, Dominique Pontier, Xavier Charpentier, Samuel Venner
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	natural transformation horizontal gene transfer mobile genetic elements resistance genes stochastic environment Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/70f53cfafd744a159b0fa465f0a24e28
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spelling	oai:doaj.org-article:70f53cfafd744a159b0fa465f0a24e282021-11-15T15:57:02ZBacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements10.1128/mBio.02443-192150-7511https://doaj.org/article/70f53cfafd744a159b0fa465f0a24e282020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02443-19https://doaj.org/toc/2150-7511ABSTRACT Horizontal gene transfer (HGT) promotes the spread of genes within bacterial communities. Among the HGT mechanisms, natural transformation stands out as being encoded by the bacterial core genome. Natural transformation is often viewed as a way to acquire new genes and to generate genetic mixing within bacterial populations. Another recently proposed function is the curing of bacterial genomes of their infectious parasitic mobile genetic elements (MGEs). Here, we propose that these seemingly opposing theoretical points of view can be unified. Although costly for bacterial cells, MGEs can carry functions that are at points in time beneficial to bacteria under stressful conditions (e.g., antibiotic resistance genes). Using computational modeling, we show that, in stochastic environments, an intermediate transformation rate maximizes bacterial fitness by allowing the reversible integration of MGEs carrying resistance genes, although these MGEs are costly for host cell replication. Based on this dual function (MGE acquisition and removal), transformation would be a key mechanism for stabilizing the bacterial genome in the long term, and this would explain its striking conservation. IMPORTANCE Natural transformation is the acquisition, controlled by bacteria, of extracellular DNA and is one of the most common mechanisms of horizontal gene transfer, promoting the spread of resistance genes. However, its evolutionary function remains elusive, and two main roles have been proposed: (i) the new gene acquisition and genetic mixing within bacterial populations and (ii) the removal of infectious parasitic mobile genetic elements (MGEs). While the first one promotes genetic diversification, the other one promotes the removal of foreign DNA and thus genome stability, making these two functions apparently antagonistic. Using a computational model, we show that intermediate transformation rates, commonly observed in bacteria, allow the acquisition then removal of MGEs. The transient acquisition of costly MGEs with resistance genes maximizes bacterial fitness in environments with stochastic stress exposure. Thus, transformation would ensure both a strong dynamic of the bacterial genome in the short term and its long-term stabilization.Gabriel CarvalhoDavid FouchetGonché DaneshAnne-Sophie GodeuxMaria-Halima LaaberkiDominique PontierXavier CharpentierSamuel VennerAmerican Society for Microbiologyarticlenatural transformationhorizontal gene transfermobile genetic elementsresistance genesstochastic environmentMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	natural transformation horizontal gene transfer mobile genetic elements resistance genes stochastic environment Microbiology QR1-502
spellingShingle	natural transformation horizontal gene transfer mobile genetic elements resistance genes stochastic environment Microbiology QR1-502 Gabriel Carvalho David Fouchet Gonché Danesh Anne-Sophie Godeux Maria-Halima Laaberki Dominique Pontier Xavier Charpentier Samuel Venner Bacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements
description	ABSTRACT Horizontal gene transfer (HGT) promotes the spread of genes within bacterial communities. Among the HGT mechanisms, natural transformation stands out as being encoded by the bacterial core genome. Natural transformation is often viewed as a way to acquire new genes and to generate genetic mixing within bacterial populations. Another recently proposed function is the curing of bacterial genomes of their infectious parasitic mobile genetic elements (MGEs). Here, we propose that these seemingly opposing theoretical points of view can be unified. Although costly for bacterial cells, MGEs can carry functions that are at points in time beneficial to bacteria under stressful conditions (e.g., antibiotic resistance genes). Using computational modeling, we show that, in stochastic environments, an intermediate transformation rate maximizes bacterial fitness by allowing the reversible integration of MGEs carrying resistance genes, although these MGEs are costly for host cell replication. Based on this dual function (MGE acquisition and removal), transformation would be a key mechanism for stabilizing the bacterial genome in the long term, and this would explain its striking conservation. IMPORTANCE Natural transformation is the acquisition, controlled by bacteria, of extracellular DNA and is one of the most common mechanisms of horizontal gene transfer, promoting the spread of resistance genes. However, its evolutionary function remains elusive, and two main roles have been proposed: (i) the new gene acquisition and genetic mixing within bacterial populations and (ii) the removal of infectious parasitic mobile genetic elements (MGEs). While the first one promotes genetic diversification, the other one promotes the removal of foreign DNA and thus genome stability, making these two functions apparently antagonistic. Using a computational model, we show that intermediate transformation rates, commonly observed in bacteria, allow the acquisition then removal of MGEs. The transient acquisition of costly MGEs with resistance genes maximizes bacterial fitness in environments with stochastic stress exposure. Thus, transformation would ensure both a strong dynamic of the bacterial genome in the short term and its long-term stabilization.
format	article
author	Gabriel Carvalho David Fouchet Gonché Danesh Anne-Sophie Godeux Maria-Halima Laaberki Dominique Pontier Xavier Charpentier Samuel Venner
author_facet	Gabriel Carvalho David Fouchet Gonché Danesh Anne-Sophie Godeux Maria-Halima Laaberki Dominique Pontier Xavier Charpentier Samuel Venner
author_sort	Gabriel Carvalho
title	Bacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements
title_short	Bacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements
title_full	Bacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements
title_fullStr	Bacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements
title_full_unstemmed	Bacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements
title_sort	bacterial transformation buffers environmental fluctuations through the reversible integration of mobile genetic elements
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/70f53cfafd744a159b0fa465f0a24e28
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Bacterial Transformation Buffers Environmental Fluctuations through the Reversible Integration of Mobile Genetic Elements

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