Phylogenomics and the Dynamic Genome Evolution of the Genus Streptococcus

The genus Streptococcus comprises important pathogens that have a severe impact on human health and are responsible for substantial economic losses to agriculture. Here, we utilize 46 Streptococcus genome sequences (44 species), including eight species sequenced here, to provide the first genomic le...

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Main Authors: Richards, Vincent P., Palmer, Sara R., Pavinski Bitar, Paulina D., Qin, Xiang, Weinstock, George M., Highlander, Sarah K., Town, Christopher D., Burne, Robert A., Stanhope, Michael J.
Format: Online
Language:English
Published: Oxford University Press 2014
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4007547/
id pubmed-4007547
recordtype oai_dc
spelling pubmed-40075472014-05-02 Phylogenomics and the Dynamic Genome Evolution of the Genus Streptococcus Richards, Vincent P. Palmer, Sara R. Pavinski Bitar, Paulina D. Qin, Xiang Weinstock, George M. Highlander, Sarah K. Town, Christopher D. Burne, Robert A. Stanhope, Michael J. Research Article The genus Streptococcus comprises important pathogens that have a severe impact on human health and are responsible for substantial economic losses to agriculture. Here, we utilize 46 Streptococcus genome sequences (44 species), including eight species sequenced here, to provide the first genomic level insight into the evolutionary history and genetic basis underlying the functional diversity of all major groups of this genus. Gene gain/loss analysis revealed a dynamic pattern of genome evolution characterized by an initial period of gene gain followed by a period of loss, as the major groups within the genus diversified. This was followed by a period of genome expansion associated with the origins of the present extant species. The pattern is concordant with an emerging view that genomes evolve through a dynamic process of expansion and streamlining. A large proportion of the pan-genome has experienced lateral gene transfer (LGT) with causative factors, such as relatedness and shared environment, operating over different evolutionary scales. Multiple gene ontology terms were significantly enriched for each group, and mapping terms onto the phylogeny showed that those corresponding to genes born on branches leading to the major groups represented approximately one-fifth of those enriched. Furthermore, despite the extensive LGT, several biochemical characteristics have been retained since group formation, suggesting genomic cohesiveness through time, and that these characteristics may be fundamental to each group. For example, proteolysis: mitis group; urea metabolism: salivarius group; carbohydrate metabolism: pyogenic group; and transcription regulation: bovis group. Oxford University Press 2014-03-12 /pmc/articles/PMC4007547/ /pubmed/24625962 http://dx.doi.org/10.1093/gbe/evu048 Text en © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Richards, Vincent P.
Palmer, Sara R.
Pavinski Bitar, Paulina D.
Qin, Xiang
Weinstock, George M.
Highlander, Sarah K.
Town, Christopher D.
Burne, Robert A.
Stanhope, Michael J.
spellingShingle Richards, Vincent P.
Palmer, Sara R.
Pavinski Bitar, Paulina D.
Qin, Xiang
Weinstock, George M.
Highlander, Sarah K.
Town, Christopher D.
Burne, Robert A.
Stanhope, Michael J.
Phylogenomics and the Dynamic Genome Evolution of the Genus Streptococcus
author_facet Richards, Vincent P.
Palmer, Sara R.
Pavinski Bitar, Paulina D.
Qin, Xiang
Weinstock, George M.
Highlander, Sarah K.
Town, Christopher D.
Burne, Robert A.
Stanhope, Michael J.
author_sort Richards, Vincent P.
title Phylogenomics and the Dynamic Genome Evolution of the Genus Streptococcus
title_short Phylogenomics and the Dynamic Genome Evolution of the Genus Streptococcus
title_full Phylogenomics and the Dynamic Genome Evolution of the Genus Streptococcus
title_fullStr Phylogenomics and the Dynamic Genome Evolution of the Genus Streptococcus
title_full_unstemmed Phylogenomics and the Dynamic Genome Evolution of the Genus Streptococcus
title_sort phylogenomics and the dynamic genome evolution of the genus streptococcus
description The genus Streptococcus comprises important pathogens that have a severe impact on human health and are responsible for substantial economic losses to agriculture. Here, we utilize 46 Streptococcus genome sequences (44 species), including eight species sequenced here, to provide the first genomic level insight into the evolutionary history and genetic basis underlying the functional diversity of all major groups of this genus. Gene gain/loss analysis revealed a dynamic pattern of genome evolution characterized by an initial period of gene gain followed by a period of loss, as the major groups within the genus diversified. This was followed by a period of genome expansion associated with the origins of the present extant species. The pattern is concordant with an emerging view that genomes evolve through a dynamic process of expansion and streamlining. A large proportion of the pan-genome has experienced lateral gene transfer (LGT) with causative factors, such as relatedness and shared environment, operating over different evolutionary scales. Multiple gene ontology terms were significantly enriched for each group, and mapping terms onto the phylogeny showed that those corresponding to genes born on branches leading to the major groups represented approximately one-fifth of those enriched. Furthermore, despite the extensive LGT, several biochemical characteristics have been retained since group formation, suggesting genomic cohesiveness through time, and that these characteristics may be fundamental to each group. For example, proteolysis: mitis group; urea metabolism: salivarius group; carbohydrate metabolism: pyogenic group; and transcription regulation: bovis group.
publisher Oxford University Press
publishDate 2014
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4007547/
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