Reduced chemodiversity suppresses rhizosphere microbiome functioning in the mono-cropped agroecosystems

Abstract

Background Rhizodeposits regulate rhizosphere interactions, processes, nutrient and energy flow, and plant-microbe communication and thus play a vital role in maintaining soil and plant health. However, it remains unclear whether and how alteration in belowground carbon allocation and chemodiversity of rhizodeposits influences microbiome functioning in the rhizosphere ecosystems. To address this research gap, we investigated the relationship of rhizosphere carbon allocation and chemodiversity with microbiome biodiversity and functioning during peanut (Arachis hypogaea) continuous mono-cropping. After continuously labeling plants with 13CO2, we studied the chemodiversity and composition of rhizodeposits, along with the composition and diversity of active rhizosphere microbiome using metabolomic, amplicon, and shotgun metagenomic sequencing approaches based on DNA stable-isotope probing (DNA-SIP). Results Our results indicated that enrichment and depletion of rhizodeposits and active microbial taxa varied across plant growth stages and cropping durations. Specifically, a gradual decrease in the rhizosphere carbon allocation, chemodiversity, biodiversity and abundance of plant-beneficial taxa (such as Gemmatimonas, Streptomyces, Ramlibacter, and Lysobacter), and functional gene pathways (such as quorum sensing and biosynthesis of antibiotics) was observed with years of mono-cropping. We detected significant and strong correlations between rhizodeposits and rhizosphere microbiome biodiversity and functioning, though these were regulated by different ecological processes. For instance, rhizodeposits and active bacterial communities were mainly governed by deterministic and stochastic processes, respectively. Overall, the reduction in carbon deposition and chemodiversity during peanut continuous mono-cropping tended to suppress microbial biodiversity and its functions in the rhizosphere ecosystem. Conclusions Our results, for the first time, provide the evidence underlying the mechanism of rhizosphere microbiome malfunctioning in mono-cropped systems. Our study opens new avenues to deeply disentangle the complex plant-microbe interactions from the perspective of rhizodeposits chemodiversity and composition and will serve to guide future microbiome research for improving the functioning and services of soil ecosystems.

Characterizing bacterial communities in Phragmites australis rhizosphere and non-rhizosphere sediments under pressure of antibiotics in a shallow lake

“…Although reported that pH and EC played the most significant role in shaping bacterial communities. However, in current study, pH and EC presented no significant correlation with all phyla in non-rhizosphere sediments and significant correlation with several phyla in rhizosphere sediments, which might explain the positive association of oxygen regulation by bacterial communities (Huang et al, 2020) and root exudates (Lv et al, 2020).…”

“…Aquatic plants, as an important part of the lake ecosystem, also play an important role in the fate of pollutants in lakes ( Zhang et al, 2022 ). Rhizosphere sediment regulates rhizosphere interactions, processes, antibiotics migration and transformation and thus play a vital role in maintaining plant health and ecosystem stability ( Li et al, 2022 ). However, rhizosphere bacterial community also received much attention due to their associations with plant growth and pollution in lake ecosystems ( Marschner et al, 2004 ).…”

Silicon quantum dots promote radish resistance to root herbivores without impairing rhizosphere microenvironment health

“…17 Ramlibacter, as a PGPR, is capable of not only N fixation, N degradation and assimilatory nitrate reduction, thus promoting the accumulation of ammonium in soil ecosystem, 59 but also inhibiting pathogens and in turn increasing plant disease resistance. 60 Similarly, Saccharimonadales was found to be the dominant bacteria in salt stress and synergistically influenced the abundance soil nitrogen cycling-related genes. 61 Hydrogenophaga could not only act as denitrifying species and bacteria degrading organic substances to improve soil nutrient (e.g., C, N, P) turnover and cycling 62 but also acts as a PGPR, upregulating several functional enzymes in soybean plants such as carbonic anhydrases (related to photosynthesis), asparagine synthetase 2 (related to asparagine synthesis), and glutathione S-transferase (related to antioxidant processes), thus increasing soybean plant growth and resistance under salt stress conditions.…”

Diseased-induced multifaceted variations in community assembly and functions of plant-associated microbiomes

“…Plant-associated microorganisms play a major role in affecting plant growth and health (Muller et al, 2016 ; Theis et al, 2016 ; Singh et al, 2020 ; Woodhams et al, 2020 ). The rhizosphere, a hot spot for plants to exchange substances and energy with the surrounding environment, has drawn the most attention (Li et al, 2020 ; Li P. et al, 2022 ). There is an emerging consensus about the dominant role of the rhizosphere microbiome in influencing host performance, especially regarding resistance to disease (Berendsen et al, 2012 ; Li X. et al, 2019 ); for example, disrupting the balance between the abundances of Firmicutes and Actinobacteria in the tomato rhizosphere causes increased incidence of bacterial wilt disease (BWD; Lee et al, 2021 ).…”