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

July 2014 , Volume 27 , Number  7
Pages  664 - 677

Tatiana V. Karpinets,1 Byung H. Park,2 Mustafa H. Syed,1 Martin G. Klotz,3 and Edward C. Uberbacher1

1Biosciences Division, and 2Computer Science and Mathematics Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, U.S.A.; 3Department of Biological Sciences, University of North Carolina, Charlotte, NC 28223, U.S.A.

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Accepted 12 February 2014.

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.

This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of the source. The American Phytopathological Society, 2014.