A core microbiota of the plant-earthworm interaction conserved across soils

Abstract

The core microbiota defines the fraction of microorganisms common to all individuals from the same host species regardless of the abiotic context, be they located inside (e.g. animal guts) or outside (e.g. plant rhizospheres). While the core microbiota of many host species have been documented, no studies attempted to decipher how these core microbiota could be altered when their respective host species are interacting. We thus tested the hypothesis that interactions between different host species possessing external microbiota could result in a novel emerging entity: a core microbiota of an interaction. This is particularly true in soils, where such interactions are likely to occur between different host species harboring external microbiota, like plants through rhizospheres and earthworms through drilospheres. Using three contrasting soils (sand, loam or clay) and a meticulous sampling of different microhabitats (rhizospheres, casts and bulk) coupled to a "sourcesink approach" derived from the meta-community theory, we evidenced the presence of a conserved core microbiota of bacterial OTUs resulting from plant-earthworm interactions in all soils. This interaction was also evidenced using a tailored network analysis, revealing the presence of signature OTUs always found in earthworms casts and plant rhizospheres, and whose co-occurrence patterns were indicative of soil type. Furthermore, qPCR abundance estimates revealed that not only bacteria, but also fungi and archeae, are affected by plant-earthworm interactions. Our findings provide a new framework to explore aboveground-belowground interactions through the prism of microbial communities.

Rhizosphere Bacterial Networks, but Not Diversity, Are Impacted by Pea-Wheat Intercropping

“…Moreover, StARS method also allowed reducing possible biais in OTUs relative abundances between the two experiments, through the use of partial correlations. Hereafter we elaborated a network approach based on edge arithmetic ( Jacquiod et al, 2020 ) to identify OTU correlations that were specific of intercropping ( Supplementary Figure 2 ). Briefly, in the matrix of the pea and the wheat intercropping, we systematically removed all correlation interferences that were attributed to (i) the bare soil, (ii) the pea monocropping, and (iii) the wheat monocropping ( Supplementary Figure 2 ).…”

“…An increasing attention is given to interaction networks between rhizosphere organisms ( van der Heijden and Hartmann, 2016 ) and the impact of IC on these networks has recently been stressed ( Liu et al, 2021 ; Tang et al, 2021 ). Thus, co-occurrence networks have been proposed as an additional parameter to characterize microbial communities ( Barberán et al, 2012 ; Berry and Widder, 2014 ; Morriën et al, 2017 ; de Vries et al, 2018 ; Li and Wu, 2018 ; Jacquiod et al, 2020 ). Concerning IC co-occurrence network, Tang et al (2021) showed, through a shotgun metagenome analysis, that sugarcane and peanut IC increased the abundance of bacterial genes involved in organic matter turnover comparing to SC, without correlating these differences to changes in microbiota diversity.…”

Changes in wheat rhizosphere microbiota in response to chemical inputs, plant genotype and phenotypic plasticity

“…We investigated the structure of the modern and ancient wheat varieties rhizosphere microbiota using a network approach based on edge arithmetic (Jacquiod et al 2020) to focus on OTU correlations that are specific of each type of breeding. We first calculated two separated partial correlation matrices amongst dominant rhizosphere OTUs (total summed counts = 100 minimum, occurrence = 25/51 samples), one for the modern and one for the ancient varieties using Poisson Log Normal models (PLN, package ‘ PLNmodels ‘, Chiquet et al 2019).…”

Communities, ecosystem engineers, and functional domains

“…In the case of autogenic engineers, the functional domain is delineated by the engineering organism itself while in the case of allogenic engineers its boundary corresponds to the part of the environment which is modified by the activity of the engineering organism. Another consequence of the distinction between allo-and autogenic engineers is that the former allows positive interactions with another organism having engineering properties, as in the intermingling functional domains of roots and earthworms, with a function synergy between them (Jacquiod et al, 2020), a typical case of "cooperative ecosystem engineering" (Passarelli et al, 2014). In the case of autogenic engineers, a synergy may exist between their functional domains provided they are self-compatible.…”

“…Processing chains can explain successions observed in the course of decomposition (Paradise, 2000;Ponge, 2005b). Several engineers may also interact and display synergetic effects, like in core microbiota of plant-earthworm interactions (Jacquiod et al, 2020).…”