Metabolic Environments and Genomic Features Associated with Pathogenic and Mutualistic Interactions Between Bacteria and Plants

Genomic characteristics discriminating parasitic and mutualistic relationship of bacterial symbionts with plants are poorly understood. This study comparatively analyzed the genomes of 54 mutualists and pathogens to discover genomic markers associated with the different phenotypes. Using metabolic n...

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Main Authors: Tatiana V. Karpinets, Byung H. Park, Mustafa H. Syed, Martin G. Klotz, Edward C. Uberbacher
Format: Article
Language:English
Published: The American Phytopathological Society 2014-07-01
Series:Molecular Plant-Microbe Interactions
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-12-13-0368-R
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author Tatiana V. Karpinets
Byung H. Park
Mustafa H. Syed
Martin G. Klotz
Edward C. Uberbacher
author_facet Tatiana V. Karpinets
Byung H. Park
Mustafa H. Syed
Martin G. Klotz
Edward C. Uberbacher
author_sort Tatiana V. Karpinets
collection DOAJ
description Genomic characteristics discriminating parasitic and mutualistic relationship of bacterial symbionts with plants are poorly understood. This study comparatively analyzed the genomes of 54 mutualists and pathogens to discover genomic markers associated with the different phenotypes. Using metabolic network models, we predict external environments associated with free-living and symbiotic lifestyles and quantify dependences of symbionts on the host in terms of the consumed metabolites. We show that specific differences between the phenotypes are pronounced at the levels of metabolic enzymes, especially carbohydrate active, and protein functions. Overall, biosynthetic functions are enriched and more diverse in plant mutualists whereas processes and functions involved in degradation and host invasion are enriched and more diverse in pathogens. A distinctive characteristic of plant pathogens is a putative novel secretion system with a circadian rhythm regulator. A specific marker of plant mutualists is the co-residence of genes encoding nitrogenase and ribulose bisphosphate carboxylase/oxygenase (RuBisCO). We predict that RuBisCO is likely used in a putative metabolic pathway to supplement carbon obtained heterotrophically with low-cost assimilation of carbon from CO2. We validate results of the comparative analysis by predicting correct phenotype, pathogenic or mutualistic, for 20 symbionts in an independent set of 30 pathogens, mutualists, and commensals.
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spelling doaj.art-7ab60dc0bfde4ad692e685e76bab28662022-12-21T21:18:25ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062014-07-0127766467710.1094/MPMI-12-13-0368-RMetabolic Environments and Genomic Features Associated with Pathogenic and Mutualistic Interactions Between Bacteria and PlantsTatiana V. KarpinetsByung H. ParkMustafa H. SyedMartin G. KlotzEdward C. UberbacherGenomic characteristics discriminating parasitic and mutualistic relationship of bacterial symbionts with plants are poorly understood. This study comparatively analyzed the genomes of 54 mutualists and pathogens to discover genomic markers associated with the different phenotypes. Using metabolic network models, we predict external environments associated with free-living and symbiotic lifestyles and quantify dependences of symbionts on the host in terms of the consumed metabolites. We show that specific differences between the phenotypes are pronounced at the levels of metabolic enzymes, especially carbohydrate active, and protein functions. Overall, biosynthetic functions are enriched and more diverse in plant mutualists whereas processes and functions involved in degradation and host invasion are enriched and more diverse in pathogens. A distinctive characteristic of plant pathogens is a putative novel secretion system with a circadian rhythm regulator. A specific marker of plant mutualists is the co-residence of genes encoding nitrogenase and ribulose bisphosphate carboxylase/oxygenase (RuBisCO). We predict that RuBisCO is likely used in a putative metabolic pathway to supplement carbon obtained heterotrophically with low-cost assimilation of carbon from CO2. We validate results of the comparative analysis by predicting correct phenotype, pathogenic or mutualistic, for 20 symbionts in an independent set of 30 pathogens, mutualists, and commensals.https://apsjournals.apsnet.org/doi/10.1094/MPMI-12-13-0368-R
spellingShingle Tatiana V. Karpinets
Byung H. Park
Mustafa H. Syed
Martin G. Klotz
Edward C. Uberbacher
Metabolic Environments and Genomic Features Associated with Pathogenic and Mutualistic Interactions Between Bacteria and Plants
Molecular Plant-Microbe Interactions
title Metabolic Environments and Genomic Features Associated with Pathogenic and Mutualistic Interactions Between Bacteria and Plants
title_full Metabolic Environments and Genomic Features Associated with Pathogenic and Mutualistic Interactions Between Bacteria and Plants
title_fullStr Metabolic Environments and Genomic Features Associated with Pathogenic and Mutualistic Interactions Between Bacteria and Plants
title_full_unstemmed Metabolic Environments and Genomic Features Associated with Pathogenic and Mutualistic Interactions Between Bacteria and Plants
title_short Metabolic Environments and Genomic Features Associated with Pathogenic and Mutualistic Interactions Between Bacteria and Plants
title_sort metabolic environments and genomic features associated with pathogenic and mutualistic interactions between bacteria and plants
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-12-13-0368-R
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