Chinese Black Truffle (Tuber indicum) Alters the Ectomycorrhizosphere and Endoectomycosphere Microbiome and Metabolic Profiles of the Host Tree Quercus aliena

Abstract

Truffles are one group of the most famous ectomycorrhizal fungi in the world. There is little information on the ecological mechanisms of truffle ectomycorrhizal synthesis in vitro. In this study, we investigated the ecological effects of Tuber indicum – Quercus aliena ectomycorrhizal synthesis on microbial communities in the host plant roots and the surrounding soil using high-throughput sequencing and on the metabolic profiles of host plant roots using metabolomics approaches. We observed an increase in the diversity and richness of prokaryotic communities and a decrease in richness of fungal communities in the presence of T. indicum. The microbial community structures in the host roots and the surrounding soil were altered by ectomycorrhizal synthesis in the greenhouse. Bacterial genera Pedomicrobium, Variibacter, and Woodsholea and fungal genera Aspergillus, Phaeoacremonium, and Pochonia were significantly more abundant in ectomycorhizae and the ectomycorrhizosphere soil compared with the corresponding T. indicum-free controls (P < 0.05). Truffle-colonization reduced the abundance of some fungal genera surrounding the host tree, such as Acremonium, Aspergillus, and Penicillium. Putative prokaryotic metabolic functions and fungal functional groups (guilds) were also differentiated by ectomycorrhizal synthesis. The ectomycorrhizal synthesis had great impact on the measured soil physicochemical properties. Metabolic profiling analysis uncovered 55 named differentially abundant metabolites between the ectomycorhizae and the control roots, including 44 upregulated and 11 downregulated metabolites. Organic acids and carbohydrates were two major upregulated metabolites in ectomycorhizae, which were found formed dense interactions with other metabolites, suggesting their crucial roles in sustaining the metabolic functions in the truffle ectomycorrhization system. This study revealed the effects of truffle-colonization on the metabolites of ectomycorrhiza and illustrates an interactive network between truffles, the host plant, soil and associated microbial communities, shedding light on understanding the ecological effects of truffles.

Tuber melanosporum shapes nirS-type denitrifying and ammonia-oxidizing bacterial communities in Carya illinoinensis ectomycorrhizosphere soils

“…The most abundant genera of AOB were Nitrosospira and Nitrosomonas. Li et al (2018a) and Li et al (2018b) reported that the Nitrosospira and Nitrosomonas were the most abundant AOB in ectomycorrhizosphere soil of Pinus massoniana Lamb colonized by Pisolithus tinctorius under field condition, which is basically the same with the findings of our study. In addition, the relative abundance of Nitrosococcus and an unclassified AOB genus of Betaproteobacteria in ectomycorrhizosphere soils was significantly greater than that in rhizosphere soils while another unclassified genus was significantly lower than that in rhizosphere soils (P < 0.05).…”

“…Soil microorganisms and physicochemical properties in the rhizosphere of host plant can vary with the growth of truffles, from the occurrence of ectomycorrhizae to the formation of their mature fruiting bodies (Ponce et al, 2014;Barbieri et al, 2007;Garcia-Barreda et al, 2017). The microbial communities of ectomycorrhizosphere soils are verified to be different from that of rhizosphere soils in both artificial conditions and the wild Li et al, 2018a;Li et al, 2018b). There were numerous classified and unclassified microorganisms detected in the ectomycorrhizosphere soils of Tuber (Garcia-Barreda & Reyna, 2012), which made it difficult to analyze the taxonomy and function of all the bacteria simultaneously.…”

Micro-community associated with ectomycorrhizalRussulasymbiosis and sporocarp-producingRussulain Fagaceae dominant nature areas in southern China

“…T. melanosporum grounds also have shown a reduced fungal biodiversity, a reduced presence of both ECM Basidiomycota (57). Truffle-colonization reduced the abundance of some fungal genera surrounding the host tree, such as Acremonium (55). Russula fruiting body decreased the Chao richness bacterial index and Shannon diversity of bacterial index in rhizosphere soil.…”

“…The microorganisms associated with mycorrhizal fungi may either have positive or negative impacts on fungal spore germination, growth, nutrient acquisition and plant colonization (43, 54). Tuber indicum altered the ectomycorrhizosphere and endoectomycosphere microbiome and metabolic profiles of the host tree Quercus aliena (55). Tuber borchii shapes the ectomycorrhizosphere microbial communities of Corylus avellana (56).…”

Compartmentalization Rather Than Host Tree Drives Truffle Microbiome

“…Previous researches have explored the microbiome composition of some tru es and the physiology of associated trees by studying a single host species. For example, Tuber indicum can shape microbiome in ectomycorhizophere soil in a Pinus armandii forest while in uence the host physiology in a Quercus acutissima stand [2] and metabolic pro les in a Q. aliena stand [3]. Microbiome`s long-term stability is vital due to the fact that the uninterrupted presence of bene cial microbes and their associated functions guarantee host health and tness.…”