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Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti

Bacterial genome evolution is characterized by gains, losses, and rearrangements of functional genetic segments. The extent to which large-scale genomic alterations influence genotype-phenotype relationships has not been investigated in a high-throughput manner. In the symbiotic soil bacterium Sinor...

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Autores principales: diCenzo, George C., Benedict, Alex B., Fondi, Marco, Walker, Graham C., Finan, Turlough M., Mengoni, Alessio, Griffitts, Joel S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5929573/
https://www.ncbi.nlm.nih.gov/pubmed/29672509
http://dx.doi.org/10.1371/journal.pgen.1007357
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author diCenzo, George C.
Benedict, Alex B.
Fondi, Marco
Walker, Graham C.
Finan, Turlough M.
Mengoni, Alessio
Griffitts, Joel S.
author_facet diCenzo, George C.
Benedict, Alex B.
Fondi, Marco
Walker, Graham C.
Finan, Turlough M.
Mengoni, Alessio
Griffitts, Joel S.
author_sort diCenzo, George C.
collection PubMed
description Bacterial genome evolution is characterized by gains, losses, and rearrangements of functional genetic segments. The extent to which large-scale genomic alterations influence genotype-phenotype relationships has not been investigated in a high-throughput manner. In the symbiotic soil bacterium Sinorhizobium meliloti, the genome is composed of a chromosome and two large extrachromosomal replicons (pSymA and pSymB, which together constitute 45% of the genome). Massively parallel transposon insertion sequencing (Tn-seq) was employed to evaluate the contributions of chromosomal genes to growth fitness in both the presence and absence of these extrachromosomal replicons. Ten percent of chromosomal genes from diverse functional categories are shown to genetically interact with pSymA and pSymB. These results demonstrate the pervasive robustness provided by the extrachromosomal replicons, which is further supported by constraint-based metabolic modeling. A comprehensive picture of core S. meliloti metabolism was generated through a Tn-seq-guided in silico metabolic network reconstruction, producing a core network encompassing 726 genes. This integrated approach facilitated functional assignments for previously uncharacterized genes, while also revealing that Tn-seq alone missed over a quarter of wild-type metabolism. This work highlights the many functional dependencies and epistatic relationships that may arise between bacterial replicons and across a genome, while also demonstrating how Tn-seq and metabolic modeling can be used together to yield insights not obtainable by either method alone.
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spelling pubmed-59295732018-05-11 Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti diCenzo, George C. Benedict, Alex B. Fondi, Marco Walker, Graham C. Finan, Turlough M. Mengoni, Alessio Griffitts, Joel S. PLoS Genet Research Article Bacterial genome evolution is characterized by gains, losses, and rearrangements of functional genetic segments. The extent to which large-scale genomic alterations influence genotype-phenotype relationships has not been investigated in a high-throughput manner. In the symbiotic soil bacterium Sinorhizobium meliloti, the genome is composed of a chromosome and two large extrachromosomal replicons (pSymA and pSymB, which together constitute 45% of the genome). Massively parallel transposon insertion sequencing (Tn-seq) was employed to evaluate the contributions of chromosomal genes to growth fitness in both the presence and absence of these extrachromosomal replicons. Ten percent of chromosomal genes from diverse functional categories are shown to genetically interact with pSymA and pSymB. These results demonstrate the pervasive robustness provided by the extrachromosomal replicons, which is further supported by constraint-based metabolic modeling. A comprehensive picture of core S. meliloti metabolism was generated through a Tn-seq-guided in silico metabolic network reconstruction, producing a core network encompassing 726 genes. This integrated approach facilitated functional assignments for previously uncharacterized genes, while also revealing that Tn-seq alone missed over a quarter of wild-type metabolism. This work highlights the many functional dependencies and epistatic relationships that may arise between bacterial replicons and across a genome, while also demonstrating how Tn-seq and metabolic modeling can be used together to yield insights not obtainable by either method alone. Public Library of Science 2018-04-19 /pmc/articles/PMC5929573/ /pubmed/29672509 http://dx.doi.org/10.1371/journal.pgen.1007357 Text en © 2018 diCenzo et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
diCenzo, George C.
Benedict, Alex B.
Fondi, Marco
Walker, Graham C.
Finan, Turlough M.
Mengoni, Alessio
Griffitts, Joel S.
Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti
title Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti
title_full Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti
title_fullStr Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti
title_full_unstemmed Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti
title_short Robustness encoded across essential and accessory replicons of the ecologically versatile bacterium Sinorhizobium meliloti
title_sort robustness encoded across essential and accessory replicons of the ecologically versatile bacterium sinorhizobium meliloti
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5929573/
https://www.ncbi.nlm.nih.gov/pubmed/29672509
http://dx.doi.org/10.1371/journal.pgen.1007357
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