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Systematic Search for Evidence of Interdomain Horizontal Gene Transfer from Prokaryotes to Oomycete Lineages

While most commonly associated with prokaryotes, horizontal gene transfer (HGT) can also have a significant influence on the evolution of microscopic eukaryotes. Systematic analysis of HGT in the genomes of the oomycetes, filamentous eukaryotic microorganisms in the Stramenopiles-Alveolates-Rhizaria...

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Autores principales: McCarthy, Charley G. P., Fitzpatrick, David A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5023847/
https://www.ncbi.nlm.nih.gov/pubmed/27642638
http://dx.doi.org/10.1128/mSphere.00195-16
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author McCarthy, Charley G. P.
Fitzpatrick, David A.
author_facet McCarthy, Charley G. P.
Fitzpatrick, David A.
author_sort McCarthy, Charley G. P.
collection PubMed
description While most commonly associated with prokaryotes, horizontal gene transfer (HGT) can also have a significant influence on the evolution of microscopic eukaryotes. Systematic analysis of HGT in the genomes of the oomycetes, filamentous eukaryotic microorganisms in the Stramenopiles-Alveolates-Rhizaria (SAR) supergroup, has to date focused mainly on intradomain transfer events between oomycetes and fungi. Using systematic whole-genome analysis followed by phylogenetic reconstruction, we have investigated the extent of interdomain HGT between bacteria and plant-pathogenic oomycetes. We report five putative instances of HGT from bacteria into the oomycetes. Two transfers were found in Phytophthora species, including one unique to the cucurbit pathogen Phytophthora capsici. Two were found in Pythium species only, and the final transfer event was present in Phytopythium and Pythium species, the first reported bacterium-inherited genes in these genera. Our putative transfers included one protein that appears to be a member of the Pythium secretome, metabolic proteins, and enzymes that could potentially break down xenobiotics within the cell. Our findings complement both previous reports of bacterial genes in oomycete and SAR genomes and the growing body of evidence suggesting that interdomain transfer from prokaryotes into eukaryotes occurs more frequently than previously thought. IMPORTANCE Horizontal gene transfer (HGT) is the nonvertical inheritance of genetic material by transfer between different species. HGT is an important evolutionary mechanism for prokaryotes and in some cases is responsible for the spread of antibiotic resistance from resistant to benign species. Genome analysis has shown that examples of HGT are not as frequent in eukaryotes, but when they do occur they may have important evolutionary consequences. For example, the acquisition of fungal genes by an ancestral Phytophthora (plant destroyer) species is responsible for the large repertoire of enzymes in the plant-degrading arsenal of modern-day Phytophthora species. In this analysis, we set out to systematically search oomycete genomes for evidence of interdomain HGT (transfer of bacterial genes into oomycete species). Our results show that interdomain HGT is rare in oomycetes but has occurred. We located five well-supported examples, including one that could potentially break down xenobiotics within the cell.
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spelling pubmed-50238472016-09-16 Systematic Search for Evidence of Interdomain Horizontal Gene Transfer from Prokaryotes to Oomycete Lineages McCarthy, Charley G. P. Fitzpatrick, David A. mSphere Research Article While most commonly associated with prokaryotes, horizontal gene transfer (HGT) can also have a significant influence on the evolution of microscopic eukaryotes. Systematic analysis of HGT in the genomes of the oomycetes, filamentous eukaryotic microorganisms in the Stramenopiles-Alveolates-Rhizaria (SAR) supergroup, has to date focused mainly on intradomain transfer events between oomycetes and fungi. Using systematic whole-genome analysis followed by phylogenetic reconstruction, we have investigated the extent of interdomain HGT between bacteria and plant-pathogenic oomycetes. We report five putative instances of HGT from bacteria into the oomycetes. Two transfers were found in Phytophthora species, including one unique to the cucurbit pathogen Phytophthora capsici. Two were found in Pythium species only, and the final transfer event was present in Phytopythium and Pythium species, the first reported bacterium-inherited genes in these genera. Our putative transfers included one protein that appears to be a member of the Pythium secretome, metabolic proteins, and enzymes that could potentially break down xenobiotics within the cell. Our findings complement both previous reports of bacterial genes in oomycete and SAR genomes and the growing body of evidence suggesting that interdomain transfer from prokaryotes into eukaryotes occurs more frequently than previously thought. IMPORTANCE Horizontal gene transfer (HGT) is the nonvertical inheritance of genetic material by transfer between different species. HGT is an important evolutionary mechanism for prokaryotes and in some cases is responsible for the spread of antibiotic resistance from resistant to benign species. Genome analysis has shown that examples of HGT are not as frequent in eukaryotes, but when they do occur they may have important evolutionary consequences. For example, the acquisition of fungal genes by an ancestral Phytophthora (plant destroyer) species is responsible for the large repertoire of enzymes in the plant-degrading arsenal of modern-day Phytophthora species. In this analysis, we set out to systematically search oomycete genomes for evidence of interdomain HGT (transfer of bacterial genes into oomycete species). Our results show that interdomain HGT is rare in oomycetes but has occurred. We located five well-supported examples, including one that could potentially break down xenobiotics within the cell. American Society for Microbiology 2016-09-14 /pmc/articles/PMC5023847/ /pubmed/27642638 http://dx.doi.org/10.1128/mSphere.00195-16 Text en Copyright © 2016 McCarthy and Fitzpatrick. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
McCarthy, Charley G. P.
Fitzpatrick, David A.
Systematic Search for Evidence of Interdomain Horizontal Gene Transfer from Prokaryotes to Oomycete Lineages
title Systematic Search for Evidence of Interdomain Horizontal Gene Transfer from Prokaryotes to Oomycete Lineages
title_full Systematic Search for Evidence of Interdomain Horizontal Gene Transfer from Prokaryotes to Oomycete Lineages
title_fullStr Systematic Search for Evidence of Interdomain Horizontal Gene Transfer from Prokaryotes to Oomycete Lineages
title_full_unstemmed Systematic Search for Evidence of Interdomain Horizontal Gene Transfer from Prokaryotes to Oomycete Lineages
title_short Systematic Search for Evidence of Interdomain Horizontal Gene Transfer from Prokaryotes to Oomycete Lineages
title_sort systematic search for evidence of interdomain horizontal gene transfer from prokaryotes to oomycete lineages
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5023847/
https://www.ncbi.nlm.nih.gov/pubmed/27642638
http://dx.doi.org/10.1128/mSphere.00195-16
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