Microbiome profiling reveals that Pseudomonas antagonises parasitic nodule colonisation of cheater rhizobia in Lotus

Abstract

Summary Nodule microbiota are dominated by symbiotic nitrogen‐fixing rhizobia, however, other non‐rhizobial bacteria also colonise this niche. Although many of these bacteria harbour plant‐growth‐promoting functions, it is not clear whether these less abundant nodule colonisers impact root–nodule symbiosis. We assessed the relationship between the nodule microbiome and nodulation as influenced by the soil microbiome, by using a metabarcoding approach to characterise the communities inside nodules of healthy and starved Lotus species. A machine learning algorithm and network analyses were used to identify nodule bacteria of interest, which were re‐inoculated onto plants in controlled conditions to observe their potential functionality. The nodule microbiome of all tested species differed according to inoculum, but only that of Lotus burttii varied with plant health. Amplicon sequence variants representative of Pseudomonas species were the most indicative non‐rhizobial signatures inside healthy L. burttii nodules and negatively correlated with Rhizobium sequences. A representative Pseudomonas isolate co‐colonised nodules infected with a beneficial Mesorhizobium, but not with an ineffective Rhizobium isolate and another even reduced the number of ineffective nodules induced on Lotus japonicus. Our results show that nodule endophytes influence the overall outcome of the root–nodule symbiosis, albeit in a plant host‐specific manner.

Microbiome of Nodules and Roots of Soybean and Common Bean: Searching for Differences Associated with Contrasting Performances in Symbiotic Nitrogen Fixation

“…One hypothesis is that other bacteria living inside the nodules and that probably entered the nodule together with rhizobia are endophytes that can help in plant-growth promotion by other microbial processes, such as the synthesis of phytohormones, antimicrobial molecules, siderophores, mineral solubilization capacity, among others [ 27 , 28 , 29 , 30 ]. As an example of benefit, an interesting study of nodule endophytes performed with Lotus burtii pointed out that in healthy nodules of this legume, Pseudomonas species were the prevalent non-rhizobia, and when used as inoculum infected the plant together with a beneficial Mesorhizobium , but not with an ineffective Rhizobium , benefiting the symbiosis by decreasing the number of ineffective nodules [ 31 ].…”

“…In addition, in our study, other potential diazotrophic bacteria, such as Methylobacterium , Paraburkholderia , and Cupriavidus , were detected on nodule microbiomes, delineating that their contribution to the N nutrition deserves further investigation; these three genera might also be symbiotic to the soybean. One possible role relies on the increasing number of studies reporting other plant-growth-promoting properties in rhizobia, e.g., [ 31 , 38 , 39 ], indicating that their benefits as endophytes might go far beyond BNF.…”

Contribution of Biofertilizers to Pulse Crops: From Single-Strain Inoculants to New Technologies Based on Microbiomes Strategies

“…Plants live in close association with microbial communities that perform functions related to nutrition and protection against biotic and abiotic stresses [ 220 ]. Plant microbiomes are spread across plant tissues and organs; among the best known are the rhizosphere, nodule, root, and seed microbiomes.…”

“…The presence of Pseudomonas in different nodule microbiomes is worth noting since species of this genus have several PGPR and biocontrol properties. When studying microbial communities in Lotus burttii nodules, Crosbie et al [ 220 ] discovered that a representative of Pseudomonas was present in healthier plants and that it co-colonized nodules infected by an effective strain of Mesorhizobium, but not with an ineffective Rhizobium strain. Additionally, co-inoculation with the Pseudomonas strain decreased nodulation with the ineffective Rhizobium rather than the effective Mesorhizobium .…”

Bacterial Communities in the Rhizosphere of Common Bean Plants (Phaseolus vulgaris L.) Grown in an Arable Soil Amended with TiO2 Nanoparticles

“…Interestingly, the relative abundance of Pseudoxanthomonas, whose species were detected recently in the nodule of Phaseolus vulgaris plants [88] and some members have N 2 -fixing and indoleacetic acid (IAA) production capacity (P. mexicana) [89], was strongly reduced by the application of 150 and 300 mg TiO 2 -NPs kg −1 . Additionally, the relative abundance of members of Pseudomonas, a genus that includes species that have a N 2 -fixing capacity [90] and others that were detected inside healthy Lotus burttii nodules [91], increased, while that of Devosia, N 2 -fixing bacteria capable of forming nodules [92], was strongly reduced by the application of TiO 2 -NPs in the rhizosphere after 90 days.…”