Abstract

Despite the availability of data on the functional and phylogenetic diversity of plant-associated microbiota, the molecular mechanisms governing the successful establishment of plant bacterial communities remain mostly elusive. To investigate bacterial traits associated with successful colonization of plants, we sequenced the genome of 26 bacteria of a synthetic microbial community (SynCom), 12 of which displayed robust and 14 displayed non-robust colonization lifestyles when inoculated in maize plants. We examined the colonization profile of individual bacteria in inoculated plants and inspected their genomes for traits correlated to the colonization lifestyle. Comparative genomic analysis between robust and non-robust bacteria revealed that commonly investigated plant growth-promoting features such as auxin production, nitrogen (N) fixation, phosphate acquisition, and ACC deaminase are not deterministic for robust colonization. Functions related to carbon (C) and N acquisition, including transporters of carbohydrates and amino acids, and kinases involved in signaling mechanisms associated with C and N uptake, were enriched in robust colonizers. While enrichment of carbohydrate transporters was linked to a wide range of metabolites, amino acid transporters were primarily related to the uptake of branched-chain amino acids. Our findings identify diversification of nutrient uptake phenotypes in bacteria as determinants for successful bacterial colonization of plants.

Highlights

  • Plants and microorganisms establish mutual beneficial associations (Bonfante and Genre, 2010; Vandenkoornhuyse et al, 2015; Sánchez-Cañizares et al, 2017)

  • Plant microbiome profiling has revealed rich and diverse communities of bacteria and fungi that may be important for the growth and health of their hosts (Karthikeyan et al, 2007; Lundberg et al, 2012; Bulgarelli et al, 2015; Zarraonaindia et al, 2015; Castrillo et al, 2017)

  • Sequencing of ribosomal genes and metagenomes has enabled the discovery of communities’ assemblage dynamics, a deep understanding of mechanisms involved in plant–microbe interaction and microbiota functions that benefit plant growth still requires methods to systematically isolate and cultivate microorganisms for their use in controlled experiments, or to assess their encoded function by sequencing (Lebeis et al, 2012; Bai et al, 2015; Browne et al, 2016; Liu et al, 2017)

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Summary

Introduction

Plants and microorganisms establish mutual beneficial associations (Bonfante and Genre, 2010; Vandenkoornhuyse et al, 2015; Sánchez-Cañizares et al, 2017). By serving their hosts with a range of functions, microbes help plant growth under a variety of stressful conditions, such as drought, nutrient scarcity, and pathogen attack (Bulgarelli et al, 2013; Coleman-Derr and Tringe, 2014; Coleman-Derr et al, 2016; Gdanetz and Trail, 2017; Pineda et al, 2017). Uncovering traits underlying efficient and persistent colonization has the potential to provide resources to manipulate plant microbiomes to benefit crop production under normal and stressful conditions

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