Xihui Xu

Microbial communities play a vital role in biogeochemical cycles, allowing the biodegradation of a wide range of pollutants. The composition of the community and the interactions between its members affect degradation rate and determine the identity of the final products. Here, we demonstrate the application of sequencing technologies and metabolic modeling approaches towards enhancing biodegradation of atrazine-a herbicide causing environmental pollution. Treatment of agriculture soil with atrazine is shown to induce significant changes in community structure and functional performances. Genome-scale metabolic models were constructed for Arthrobacter, the atrazine degrader, and four other non-atrazine degrading species whose relative abundance in soil was changed following exposure to the herbicide. By modeling community function we show that consortia including the direct degrader and non-degrader differentially abundant species perform better than Arthrobacter alone. Simulations predict that growth/degradation enhancement is derived by metabolic exchanges between community members. Based on simulations we designed endogenous consortia optimized for enhanced degradation whose performances were validated in vitro and biostimulation strategies that were tested in pot experiments. Overall, our analysis demonstrates that understanding community function in its wider context, beyond the single direct degrader perspective, promotes the design of biostimulation strategies.

Engineering natural microbiomes for biotechnological applications remains challenging, as metabolic interactions within microbiomes are largely unknown, and practical principles and tools for microbiome engineering are still lacking. Here, we present a combinatory top-down and bottom-up framework to engineer natural microbiomes for the construction of function-enhanced synthetic microbiomes. We show that application of herbicide and herbicide-degrader inoculation drives a convergent succession of different natural microbiomes toward functional microbiomes (e.g., enhanced bioremediation of herbicide-contaminated soils). We develop a metabolic modeling pipeline, SuperCC, that can be used to document metabolic interactions within microbiomes and to simulate the performances of different microbiomes. Using SuperCC, we construct bioremediation-enhanced synthetic microbiomes based on 18 keystone species identified from natural microbiomes. Our results highlight the importance of metabolic interactions in shaping microbiome functions and provide practical guidance for engineering natural microbiomes.

The extensive use of phthalic acid esters (PAEs) has led to their widespread distribution across various environments. As PAEs pose significant threats to human health, it is urgent to develop efficient strategies to eliminate them from environments. Bacteria-driven PAE biodegradation has been considered as an inexpensive yet effective strategy to restore the contaminated environments. Despite great advances in bacterial culturing and sequencing, the inherent complexity of indigenous microbial community hinders us to mechanistically understand in situ PAE biodegradation and efficiently harness the degrading power of bacteria. The synthetic microbial ecology provides us a simple and controllable model system to address this problem. In this review, we focus on the current progress of PAE biodegradation mediated by bacterial isolates and indigenous bacterial communities, and discuss the prospective of synthetic PAE-degrading bacterial communities in PAE biodegradation research. It is anticipated that the theories and approaches of synthetic microbial ecology will revolutionize the study of bacteria-driven PAE biodegradation and provide novel insights for developing effective bioremediation solutions.

Arbuscular mycorrhizal fungi (AMF) affect multiple ecosystem functions and processes, the assemblages of which vary across ecosystems. However, the influences of environmental factors on AMF communities which may shape these communities are still largely unknown. In this study, AMF communities from roots and rhizosphere soils of Chenopodium ambrosioides in different natural soils were investigated. The root habitat showed significantly smaller numbers of OTUs and lower community richness compared to the rhizosphere soil habitat. Most OTUs in the root habitat were shared by the soil habitat from the same sampling site, indicating that rhizosphere soils represent a pool of AMF species, a fraction of which is recruited by plants. Most of the AMF in root habitats were Glomeraceae, suggesting recruitment preferences of AMF by plants. The relative contributions of environmental factors to explain variations in AMF community composition and phylogenetic structure were assessed. The results revealed soil properties predominantly explained the variation, followed by geographic and climate parameters which explained a small fraction independently, while the host plant showed few explanations. Overall, our results indicated that soil and root habitats as well as soil characters, especially pH, nitrogen and micronutrients (Zn and Cu) affected AMF communities significantly.

BACKGROUND: Soil microbiomes are considered a cornerstone of the next green revolution, and plant growth-promoting bacteria (PGPB) are critical for microbiome engineering. However, taking plant-beneficial microorganisms from discovery to agricultural application remains challenging, as the mechanisms underlying the interactions between beneficial strains and plants in native soils are still largely unknown. Increasing numbers of studies have indicated that strains introduced to manipulate microbiomes are usually eliminated in soils, while others have reported that application of PGPB as inocula significantly improves plant growth. This contradiction suggests the need for a deeper understanding of the mechanisms underlying microbe-induced growth promotion. RESULTS: We showed PGPB-induced long-term plant growth promotion after elimination of the PGPB inoculum in soils and explored the three-way interactions among the exogenous inoculum, indigenous microbiome, and plant, which were key elements of the plant growth-promoting process. We found the rhizosphere microbiome assembly was mainly driven by plant development and root recruitments greatly attenuated the influence of inocula on the rhizosphere microbiome. Neither changes in the rhizosphere microbiome nor colonization of inocula in roots was necessary for plant growth promotion. In roots, modification of DNA methylation in response to inoculation affects gene expression related to PGPB-induced growth promotion, and disruptions of the inoculation-induced DNA methylation patterns greatly weakened the plant growth promotion. Together, our results showed PGPB-induced DNA methylation modifications in roots mediated the promotion process and these modifications remained functional after elimination of the inoculum from the microbiome. CONCLUSION: This study suggests a new mechanism in which PGPB affect DNA methylation in roots to promote plant growth, which provides important insights into microbiome-plant interactions and offers new strategies for plant microbiome engineering beyond the perspective of maintaining inoculum persistence in soils. Video abstract.