Selection for Reducing Energy Cost of Protein Production Drives the GC Content and Amino Acid Composition Bias in Gene Transfer Agents

ABSTRACT Gene transfer agents (GTAs) are virus-like elements integrated into bacterial genomes, particularly, those of Alphaproteobacteria. The GTAs can be induced under conditions of nutritional stress, incorporate random fragments of bacterial DNA into miniphage particles, lyse the host cells, and...

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Autores principales:	Roman Kogay, Yuri I. Wolf, Eugene V. Koonin, Olga Zhaxybayeva
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	GTA nutrient depletion metabolic efficiency virus exaptation alphaproteobacteria bacteriophages Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6db22c92840347e8b1cd844467f75198
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spelling	oai:doaj.org-article:6db22c92840347e8b1cd844467f751982021-11-15T15:56:43ZSelection for Reducing Energy Cost of Protein Production Drives the GC Content and Amino Acid Composition Bias in Gene Transfer Agents10.1128/mBio.01206-202150-7511https://doaj.org/article/6db22c92840347e8b1cd844467f751982020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01206-20https://doaj.org/toc/2150-7511ABSTRACT Gene transfer agents (GTAs) are virus-like elements integrated into bacterial genomes, particularly, those of Alphaproteobacteria. The GTAs can be induced under conditions of nutritional stress, incorporate random fragments of bacterial DNA into miniphage particles, lyse the host cells, and infect neighboring bacteria, thus enhancing horizontal gene transfer. We show that GTA genes evolve under conditions of pronounced positive selection for the reduction of the energy cost of protein production as shown by comparison of the amino acid compositions with those of both homologous viral genes and host genes. The energy saving in GTA genes is comparable to or even more pronounced than that in the genes encoding the most abundant, essential bacterial proteins. In cases in which viruses acquire genes from GTAs, the bias in amino acid composition disappears in the course of evolution, showing that reduction of the energy cost of protein production is an important factor of evolution of GTAs but not bacterial viruses. These findings strongly suggest that GTAs represent bacterial adaptations rather than selfish, virus-like elements. Because GTA production kills the host cell and does not propagate the GTA genome, it appears likely that the GTAs are retained in the course of evolution via kin or group selection. Therefore, we hypothesize that GTAs facilitate the survival of bacterial populations under energy-limiting conditions through the spread of metabolic and transport capabilities via horizontal gene transfer and increases in nutrient availability resulting from the altruistic suicide of GTA-producing cells. IMPORTANCE Kin selection and group selection remain controversial topics in evolutionary biology. We argue that these types of selection are likely to operate in bacterial populations by showing that bacterial gene transfer agents (GTAs), but not related viruses, evolve under conditions of positive selection for the reduction of the energy cost of GTA particle production. We hypothesize that GTAs are dedicated devices mediating the survival of bacteria under conditions of nutrient limitation. The benefits conferred by GTAs under nutritional stress conditions appear to include horizontal dissemination of genes that could provide bacteria with enhanced capabilities for nutrient utilization and increases of nutrient availability occurring through the lysis of GTA-producing bacteria.Roman KogayYuri I. WolfEugene V. KooninOlga ZhaxybayevaAmerican Society for MicrobiologyarticleGTAnutrient depletionmetabolic efficiencyvirus exaptationalphaproteobacteriabacteriophagesMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	GTA nutrient depletion metabolic efficiency virus exaptation alphaproteobacteria bacteriophages Microbiology QR1-502
spellingShingle	GTA nutrient depletion metabolic efficiency virus exaptation alphaproteobacteria bacteriophages Microbiology QR1-502 Roman Kogay Yuri I. Wolf Eugene V. Koonin Olga Zhaxybayeva Selection for Reducing Energy Cost of Protein Production Drives the GC Content and Amino Acid Composition Bias in Gene Transfer Agents
description	ABSTRACT Gene transfer agents (GTAs) are virus-like elements integrated into bacterial genomes, particularly, those of Alphaproteobacteria. The GTAs can be induced under conditions of nutritional stress, incorporate random fragments of bacterial DNA into miniphage particles, lyse the host cells, and infect neighboring bacteria, thus enhancing horizontal gene transfer. We show that GTA genes evolve under conditions of pronounced positive selection for the reduction of the energy cost of protein production as shown by comparison of the amino acid compositions with those of both homologous viral genes and host genes. The energy saving in GTA genes is comparable to or even more pronounced than that in the genes encoding the most abundant, essential bacterial proteins. In cases in which viruses acquire genes from GTAs, the bias in amino acid composition disappears in the course of evolution, showing that reduction of the energy cost of protein production is an important factor of evolution of GTAs but not bacterial viruses. These findings strongly suggest that GTAs represent bacterial adaptations rather than selfish, virus-like elements. Because GTA production kills the host cell and does not propagate the GTA genome, it appears likely that the GTAs are retained in the course of evolution via kin or group selection. Therefore, we hypothesize that GTAs facilitate the survival of bacterial populations under energy-limiting conditions through the spread of metabolic and transport capabilities via horizontal gene transfer and increases in nutrient availability resulting from the altruistic suicide of GTA-producing cells. IMPORTANCE Kin selection and group selection remain controversial topics in evolutionary biology. We argue that these types of selection are likely to operate in bacterial populations by showing that bacterial gene transfer agents (GTAs), but not related viruses, evolve under conditions of positive selection for the reduction of the energy cost of GTA particle production. We hypothesize that GTAs are dedicated devices mediating the survival of bacteria under conditions of nutrient limitation. The benefits conferred by GTAs under nutritional stress conditions appear to include horizontal dissemination of genes that could provide bacteria with enhanced capabilities for nutrient utilization and increases of nutrient availability occurring through the lysis of GTA-producing bacteria.
format	article
author	Roman Kogay Yuri I. Wolf Eugene V. Koonin Olga Zhaxybayeva
author_facet	Roman Kogay Yuri I. Wolf Eugene V. Koonin Olga Zhaxybayeva
author_sort	Roman Kogay
title	Selection for Reducing Energy Cost of Protein Production Drives the GC Content and Amino Acid Composition Bias in Gene Transfer Agents
title_short	Selection for Reducing Energy Cost of Protein Production Drives the GC Content and Amino Acid Composition Bias in Gene Transfer Agents
title_full	Selection for Reducing Energy Cost of Protein Production Drives the GC Content and Amino Acid Composition Bias in Gene Transfer Agents
title_fullStr	Selection for Reducing Energy Cost of Protein Production Drives the GC Content and Amino Acid Composition Bias in Gene Transfer Agents
title_full_unstemmed	Selection for Reducing Energy Cost of Protein Production Drives the GC Content and Amino Acid Composition Bias in Gene Transfer Agents
title_sort	selection for reducing energy cost of protein production drives the gc content and amino acid composition bias in gene transfer agents
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/6db22c92840347e8b1cd844467f75198
work_keys_str_mv	AT romankogay selectionforreducingenergycostofproteinproductiondrivesthegccontentandaminoacidcompositionbiasingenetransferagents AT yuriiwolf selectionforreducingenergycostofproteinproductiondrivesthegccontentandaminoacidcompositionbiasingenetransferagents AT eugenevkoonin selectionforreducingenergycostofproteinproductiondrivesthegccontentandaminoacidcompositionbiasingenetransferagents AT olgazhaxybayeva selectionforreducingenergycostofproteinproductiondrivesthegccontentandaminoacidcompositionbiasingenetransferagents
_version_	1718427094918103040

Selection for Reducing Energy Cost of Protein Production Drives the GC Content and Amino Acid Composition Bias in Gene Transfer Agents

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