Functional Characteristics of an Endophyte Community Colonizing Rice Roots as Revealed by Metagenomic Analysis

Abstract

Roots are the primary site of interaction between plants and microorganisms. To meet food demands in changing climates, improved yields and stress resistance are increasingly important, stimulating efforts to identify factors that affect plant productivity. The role of bacterial endophytes that reside inside plants remains largely unexplored, because analysis of their specific functions is impeded by difficulties in cultivating most prokaryotes. Here, we present the first metagenomic approach to analyze an endophytic bacterial community resident inside roots of rice, one of the most important staple foods. Metagenome sequences were obtained from endophyte cells extracted from roots of field-grown plants. Putative functions were deduced from protein domains or similarity analyses of protein-encoding gene fragments, and allowed insights into the capacities of endophyte cells. This allowed us to predict traits and metabolic processes important for the endophytic lifestyle, suggesting that the endorhizosphere is an exclusive microhabitat requiring numerous adaptations. Prominent features included flagella, plant-polymer-degrading enzymes, protein secretion systems, iron acquisition and storage, quorum sensing, and detoxification of reactive oxygen species. Surprisingly, endophytes might be involved in the entire nitrogen cycle, as protein domains involved in N(2)-fixation, denitrification, and nitrification were detected and selected genes expressed. Our data suggest a high potential of the endophyte community for plant-growth promotion, improvement of plant stress resistance, biocontrol against pathogens, and bioremediation, regardless of their culturability.

Antimicrobial drimane sesquiterpenes and their effect on endophyte communities in the medical tree Warburgia ugandensis

“…Due to potential hydroxyl radical formation following reduction of molecular oxygen in the presence of ferrous iron catalysts, drimane sesquiterpenes may cause oxidative stress in the affected plant tissue. A study exploring the metagenome of the rice root endophytic community identified the expression of glutathione synthase genes, a metabolite that is known to mitigate oxidative stress, as consequence of endophyte colonization amongst others (Sessitsch et al, 2012). Tolerance against oxidative stress may represent a widespread trait in soil microbes; their nutrition depends on the decomposition of organic polymers, an oxidative process that also may involve the formation of hydroxyl radicals in the Fenton reaction or the activity of oxidative enzymes (ten Have and Teunissen, 2001).…”

Root surface as a frontier for plant microbiome research

“…Complementary to such cultivation approaches, the direct sequencing of complex mixtures of DNA from various organisms of a habitat (metagenomics) reveals the metabolic capacity of a microbiome. In rice, numerous microbial traits such as nitrogen fixation, the flagellum, protein secretion systems, or quorum sensing, and their habitat specificity were predicted using metagenomics (17,18).…”

The effect of crop rotation between wetland rice and upland maize on the microbial communities associated with roots

“…Flooding impedes the transport of oxygen, so that the bulk of the soil becomes anoxic and supportive for anaerobic degradation of organic matter and CH 4 production (Liesack et al 2000). However, the rice gas vascular system allows the transport of oxygen into the roots and the rhizosphere thus providing a habitat for both aerobic and anaerobic bacteria involved in redox reactions of the C, N and S cycle (Liesack et al 2000;Sessitsch et al 2012). Maize, on the other hand, is a crop grown in aerated upland soil, which is usually oxic and supportive for aerobic degradation of organic matter to CO 2 .…”