Cooperation, Competition, and Specialized Metabolism in a Simplified Root Nodule Microbiome

Abstract

Microbiomes associated with various plant structures often contain members with the potential to make specialized metabolites, e.g., molecules with antibacterial, antifungal, or siderophore activities. However, when and where microbes associated with plants produce specialized metabolites, and the potential role of these molecules in mediating intramicrobiome interactions, is not well understood. Root nodules of legume plants are organs devoted to hosting symbiotic bacteria that fix atmospheric nitrogen and have recently been shown to harbor a relatively simple accessory microbiome containing members with the ability to produce specialized metabolites in vitro. On the basis of these observations, we sought to develop a model nodule microbiome system for evaluating specialized microbial metabolism in planta. Starting with an inoculum derived from field-grown Medicago sativa nodules, serial passaging through gnotobiotic nodules yielded a simplified accessory community composed of four members: Brevibacillus brevis, Paenibacillus sp., Pantoea agglomerans, and Pseudomonas sp. Some members of this community exhibited clear cooperation in planta, while others were antagonistic and capable of disrupting cooperation between other partners. Using matrix-assisted laser desorption ionization–imaging mass spectrometry, we found that metabolites associated with individual taxa had unique distributions, indicating that some members of the nodule community were spatially segregated. Finally, we identified two families of molecules produced by B. brevis in planta as the antibacterial tyrocidines and a novel set of gramicidin-type molecules, which we term the britacidins. Collectively, these results indicate that in addition to nitrogen fixation, legume root nodules are likely also sites of active antimicrobial production.

Rhizobium-Linked Nutritional and Phytochemical Changes Under Multitrophic Functional Contexts in Sustainable Food Systems

“…and Paenibacillus sp. (Hansen et al, 2020). Apart from competing for infection sites on leguminous roots (Spaink, 1995;Mendoza-Suárez et al, 2020), free-living rhizobia, and other rhizosphere microbes compete for organic carbon in root exudates (Olanrewaju et al, 2019).…”

“…Albert Bernhard Frank (1839-1900 (Hassen et al, 2020). Such bacteria are part of complex microbiomes that exist endophytically in root nodules of leguminous plants (Martínez-Hidalgo and Hirsch, 2017;Hansen et al, 2020). With the advent of modern molecular identification tools (Young and Haukka, 1996;Deng et al, 2011), root nodulating rhizobia have currently been sub-classified into at least 15 genera including the alphaproteobacteria Rhizobium, Ensifer (syn.…”

Paenibacillussp. strain UY79, isolated from a root nodule ofArachis villosa, displays a broad spectrum of antifungal activity

“…The copyright holder for this preprint this version posted March 28, 2021. ; https://doi.org/10.1101/2021.03.26.437297 doi: bioRxiv preprint together with the ability to produce diverse diffusible and volatile compounds against fungi/oomycetes suggest that strain UY79 could either coexist or interfere with various soil and plant-associated microorganisms, perhaps modulating the microbiota associated with plants, as has been described for other nodule-inhabiting Paenibacillus strains (14,70).…”

The Role of Secretion Systems, Effectors, and Secondary Metabolites of Beneficial Rhizobacteria in Interactions With Plants and Microbes

“…Sequencing of the strain's genome led to assignment of these antimicrobials to their cognate biosynthetic gene clusters. It is yet unknown whether these antimicrobials are used in competition between the natural nodule microbiome or protect it from pathogen infection (Hansen et al, 2020).…”