Assembly Patterns of the Rhizosphere Microbiome Along the Longitudinal Root Axis of Maize (Zea mays L.).

Lioba Rüger,Ye Deng,Jule Freudenthal,Michael Bonkowski,Kenneth Dumack,Frank Hochholdinger,Monica Wilson,Kai Feng,Yan Chen,Doris Vetterlein,Ruibo Sun,Peng Yu,Bo Sun

doi:10.3389/fmicb.2021.614501

Abstract

It is by now well proven that different plant species within their specific root systems select for distinct subsets of microbiota from bulk soil – their individual rhizosphere microbiomes. In maize, root growth advances several centimeters each day, with the locations, quality and quantity of rhizodeposition changing. We investigated the assembly of communities of prokaryotes (archaea and bacteria) and their protistan predators (Cercozoa, Rhizaria) along the longitudinal root axis of maize (Zea mays L.). We grew maize plants in an agricultural loamy soil and sampled rhizosphere soil at distinct locations along maize roots. We applied high-throughput sequencing, followed by diversity and network analyses in order to track changes in relative abundances, diversity and co-occurrence of rhizosphere microbiota along the root axis. Apart from a reduction of operational taxonomic unit (OTU) richness and a strong shift in community composition between bulk soil and root tips, patterns of microbial community assembly along maize-roots were more complex than expected. High variation in beta diversity at root tips and the root hair zone indicated substantial randomness of community assembly. Root hair zone communities were characterized by massive co-occurrence of microbial taxa, likely fueled by abundant resource supply from rhizodeposition. Further up the root where lateral roots emerged processes of community assembly appeared to be more deterministic (e.g., through competition and predation). This shift toward significance of deterministic processes was revealed by low variability of beta diversity, changes in network topology, and the appearance of regular phylogenetic co-occurrence patterns in bipartite networks between prokaryotes and their potential protistan predators. Such patterns were strongest in regions with fully developed laterals, suggesting that a consistent rhizosphere microbiome finally assembled. For the targeted improvement of microbiome function, such knowledge on the processes of microbiome assembly on roots and its temporal and spatial variability is crucially important.

Highlights

The predictable assembly of specific subsets of the soil microbiota in the rhizosphere of plants has led to the characterization of plant species-specific “microbiomes” (Hirsch and Mauchline, 2012; Lundberg et al, 2012; Peiffer et al, 2013; Berg et al, 2014)
Root exudation does not stimulate rhizobacteria uniformly, rather, rhizodeposition selects for certain fast-growing, copiotrophic bacterial taxa (Maloney et al, 1997; Zelenev et al, 2005; Fierer et al, 2007), leading to reduced taxonomic diversity in the rhizosphere compared to bulk soil (Bulgarelli et al, 2012; Shi et al, 2015; Fan et al, 2017)
To gain insights into the self-organization of the rhizosphere microbiome, we investigated the assembly of rhizosphere specific microbial communities of prokaryotes and their protistan predators along the longitudinal root axis of maize plants at clearly defined root regions

Summary

Introduction

The predictable assembly of specific subsets of the soil microbiota in the rhizosphere of plants has led to the characterization of plant species-specific “microbiomes” (Hirsch and Mauchline, 2012; Lundberg et al, 2012; Peiffer et al, 2013; Berg et al, 2014). The vast majority of microorganisms in bulk soil rest in an inactive dormant state of starvation, because their activity is severely limited by the availability of energy from readily accessible carbon molecules (Blagodatskaya and Kuzyakov, 2013). This carbon limitation is temporarily offset by pulses of exudates released by the growing root that triggers the bulk soil bacteria into activity (Boddy et al, 2007). It is thought that differences in the amount and composition of rhizodeposits further select for the adapted plant speciesand genotype-specific bacterial microbiomes (Bais et al, 2006; Hartmann et al, 2009; Bulgarelli et al, 2012)

Methods

Results

Conclusion