Non-Rhizobial Endophytes (NREs) of the Nodule Microbiome Have Synergistic Roles in Beneficial Tripartite Plant-Microbe Interactions

Abstract

Microbial symbioses deal with the symbiotic interactions between a given microorganism and another host. The most widely known and investigated microbial symbiosis is the association between leguminous plants and nitrogen-fixing rhizobia. It is one of the best-studied plant-microbe interactions that occur in the soil rhizosphere and one of the oldest plant-microbe interactions extensively studied for the past several decades globally. Until recently, it used to be a common understanding among scientists in the field of rhizobia and microbial ecology that the root nodules of thousands of leguminous species only contain nitrogen-fixing symbiotic rhizobia. With the advancement of molecular microbiology and the coming into being of state-of-the-art biotechnology innovations, including next-generation sequencing, it has now been revealed that rhizobia living in the root nodules of legumes are not alone. Microbiome studies such as metagenomics of the root nodule microbial community showed that, in addition to symbiotic rhizobia, other bacteria referred to as non-rhizobial endophytes (NREs) exist in the nodules. This review provides an insight into the occurrence of non-rhizobial endophytes in the root nodules of several legume species and the beneficial roles of the tripartite interactions between the legumes, the rhizobia and the non-rhizobial endophytes (NREs).

Keywords: endophytes; metagenomics; microbiome; nitrogen fixation; nodules; rhizobia; synergism.

Figure 1

Signaling among microorganisms and inter-kingdom signaling between microorganisms and plants in the rhizosphere. Source [18] with permission.

Figure 2

One of the proposed mechanisms of how non-rhizobial endophytes enter the root nodules and become part of the nodule microbiome that includes both the symbiotic rhizobia and the once free-living rhizobacteria, which were part of the rhizosphere soil. Rhizobium species are colored in purple, while free-living NRE are colored in red, blue and green. Created with BioRender.com [32].

Figure 3

Microbial diversity of the nodule microbiome of Actinorhizal plants determined using shotgun metagenomics. The core microbiome of the nodules retrieved from greenhouse (A) and field (B) samples, comprising a total of 27 and 41 families, respectively. Source: [37] with permission.

Figure 4

A schematic representation of how PGPR are involved in the mitigation of various abiotic stresses, including drought, salinity, and nutrient deficiency (fertility) stress, and elicit induced systemic tolerance (IST) in plants. Source: [65] with permission.

Figure 5

(A) In vitro siderophore production by non-rhizobial endophytes Herbaspirillum seropedicae and Burkholderia sp. isolated from the nodules of Aspalathus linearis (rooibos). (B) Aspalathus linearis inoculated with the non-rhizobial endophytic strain Herbaspirillum lucitanum (left) as compared to the non-inoculated control (right). Source: [96].