The symbiotic capacity of rhizobium shapes root-associated microbiomes

Abstract

Background: Root-microbiome interactions are of central importance for plant performance and yield. A distinctive feature of legumes in this context is that they engage in symbiosis with rhizobia, which are abundant in soils and include both symbiotic and non-symbiotic bacterial strains. If and how the capacity of rhizobia to form symbiosis modulates root-associated microbiomes are not well understood. Results: We address this question by inoculating soybean (Glycine max) plants with wild type (WT) or a noeI mutant of Bradyrhizobium diazoefficiens. The noeI mutant produces a defective Nod factor and is thus compromised in its ability to establish functional symbiosis. Compared to soybean plants inoculated with WT rhizobia, plants inoculated with the noeI mutant showed a significant decrease in nodulation and root-flavonoid exudation, and exhibited strong changes in microbiome assembly in the rhizosphere and the rhizoplane. NoeI mutant-inoculated roots exhibited reduced diversity, co-occurrence interactions and a substantial depletion of beneficial microbes on the roots. The effects of the noeI mutation were absent in soils without plants, demonstrating that they are plant dependent. Complementation experiments showed that flavonoid supplementation is sufficient to restore recruitment of beneficial microbes. Conclusion: The results illustrate that the capacity of a rhizobium to form microbial symbiosis dramatically alters root-associated microbiomes, most likely by changing root exudation patterns. The results of this study have important implications for our understanding of the evolution of plant-microbiome interactions in the context of plant-bacterial symbioses.

Triterpenoid and Steroidal Saponins Differentially Influence Soil Bacterial Genera

“…In this study, we treated soil with saponins that had either steroid- or oleanane-type aglycones. The bacterial α-diversity was found to decrease with all four saponin treatments, which was consistent with previous results for benzoxazolin-2(3H)-one (BOA), quercetin, daidzein, flavonoid mixture, α-tomatine, and tomatidine [ 20 , 22 , 37 , 47 ]. The decreases found in the bacterial α-diversity were in accordance with previous observations made for the rhizosphere when affected by root exudates [ 48 , 49 ].…”

“…Treating soil with pure compounds has revealed the strong influences PSMs have in shaping the microbiota [ 19 , 20 , 21 , 22 , 35 , 37 , 47 ]. In this study, we treated soil with saponins that had either steroid- or oleanane-type aglycones.…”

“…These variations may be caused by differences in the concentrations of the PSMs between our study and that of Schütz et al [ 22 ] (the former: 1250 nmol g soil −1 and the latter: 33 nmol g soil −1 ) and the promotion and inhibition effects of the PSMs on the growth of soil microbes. There are some taxa commonly enriched by the PSM treatments and in the host plant rhizosphere and roots, such as: Comamonadaceae and Microbacteriaceae by daidzein and soybean root; Arthrobacter of Micrococcaceae by santhopine, nicotine, and tobacco roots; Sphingobium of Sphingomonadaceae by α-tomatine, tomatidine, and tomato root; and Caulobacteraceae and Novosphingobium of Sphingomonadaceae by soyasaponin Bb and soybean root [ 20 , 21 , 35 , 47 ]. It has also been reported that the bacterial communities in the soils treated with daidzein, α-tomatine, nicotine, and santhopine are closer to those of the rhizosphere or endosphere of the respective host plants than the bulk soils, defined as a soil that does not adhere to plant roots [ 20 , 21 , 47 ].…”

“…There are some taxa commonly enriched by the PSM treatments and in the host plant rhizosphere and roots, such as: Comamonadaceae and Microbacteriaceae by daidzein and soybean root; Arthrobacter of Micrococcaceae by santhopine, nicotine, and tobacco roots; Sphingobium of Sphingomonadaceae by α-tomatine, tomatidine, and tomato root; and Caulobacteraceae and Novosphingobium of Sphingomonadaceae by soyasaponin Bb and soybean root [ 20 , 21 , 35 , 47 ]. It has also been reported that the bacterial communities in the soils treated with daidzein, α-tomatine, nicotine, and santhopine are closer to those of the rhizosphere or endosphere of the respective host plants than the bulk soils, defined as a soil that does not adhere to plant roots [ 20 , 21 , 47 ]. Rhizosphere and root microbiota have been reported in several saponin-synthesizing plants.…”

Profound Change in Soil Microbial Assembly Process and Co-occurrence Pattern in Co-inoculation of Bradyrhizobium japonicum 5038 and Bacillus aryabhattai MB35-5 on Soybean

“…For fungi, Bradyrhizobium japonicum 5038 inoculation in the soybean also facilitated an increase in the number of connections between fungi, including the hub fungi shift to Phaeosphaeria, Sporobolomyces, Septoria, Edenia, and Leptospora (Xu et al, 2020). Moreover, by building mutants with a defective Nod factor, previous research confirmed that the symbiosis compromised NoeI mutant-inoculation could reduce microbial diversity and co-occurrence interactions, and decrease the abundance of beneficial microbes (Liu et al, 2020). This could be because the inoculated Bradyrhizobium japonicum 5038 forms a more symbiotic system with the host plant, which was changed by altering plant root exudates such as flavonoid (White et al, 2015), Catechin (Mommer et al, 2016), and some volatile organic compounds to change the soil physical and chemical environment and influence the prevalence of rhizosphere microorganisms (Vishwakarma et al, 2020).…”