Genome Sequences of a Plant Beneficial Synthetic Bacterial Community Reveal Genetic Features for Successful Plant Colonization

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.

From Microbiome to Traits: Designing Synthetic Microbial Communities for Improved Crop Resiliency

“…Traditionally, the selection of microbes for agricultural application has essentially involved in vitro screening for well-known taxa or PGP activities such as nitrogen fixation, phytohormone production, and 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity ( Glick, 2012 ). However, except in some extensively investigated cases, such as rhizobium–legume interactions and mycorrhizal fungi, there is still no clear correlation between these traits and their effectiveness in plant growth promotion or their contribution to sustaining stable plant–microbe associations ( Finkel et al, 2017 ; de Souza et al, 2019 ). Furthermore, inoculants designed with these conventional approaches are often unable to establish and sustain associations with plants under field conditions, yielding unsatisfactory results ( Nadeem et al, 2014 ; Zimmer et al, 2016 ).…”

“…Bacterial strains isolated from lodgepole pine significantly improve maize plant biomass accumulation ( Puri et al, 2015 ). The genome sequences of core microbiome members isolated from sugarcane shows that robust-colonizing strains are enriched in genes coding for carbon metabolism when compared with non-core microbiome strains ( de Souza et al, 2019 ). As the genome sequences of plant microbiomes become increasingly available, comparative genomics would help to identify specific genomic markers for key traits, which will guide the selection of beneficial microbes ( Finkel et al, 2017 ; Toju et al, 2018 ).…”

“…This rationale is driven by using genomic information and gene expression profiles to select microbes containing plant-beneficial functional traits or metabolic capabilities that will help in designing the best microbial combination for inoculants ( Vorholt et al, 2017 ; Toju et al, 2018 ). Because important traits such as colonization efficiency and prevalence are likely associated with multiple genes, genome surveys for multiple gene markers will be key to identifying relevant microbes ( Cole et al, 2017 ; Levy et al, 2018 ; de Souza et al, 2019 ). Ultimately, genomics-available datasets will make it easier to screen microbial candidates based on genomic markers as the use of these datasets tend to be less laborious than traditional procedures ( Finkel et al, 2017 ).…”

“…Such a strategy is built on the rationale of selecting microbes in a culture collection based on empirical evidence from microbial surveys, regardless of taxonomic classification or preselected traits ( Figure 1 ). By using this approach, microbes are targeted based on relevant traits, such as robust colonization and prevalence ( Armanhi et al, 2018 ; de Souza et al, 2019 ).…”

Modes of Action of Microbial Biocontrol in the Phyllosphere

“…Production of IAA can occur via several pathways, as reviewed by Duca et al (2014) . The presence of these pathways can be detected by the presence of the following essential genes: ipd C and ald H for the indole-3-pyruvate pathway (encoding the enzymes necessary for the decarboxylation of indole-3-pyruvate and subsequent oxidation, respectively), dcc and ald H for the tryptamine pathway (encoding the enzymes necessary for the decarboxylation of tryptophan and subsequent oxidation, respectively), iaa M and iaa H for the indole-3-acetamide pathway (encoding for tryptophan-2-monooxygenase and indole-3-acetamide hydrolase, respectively), and nth A for the indole-3-acetonitrile pathway (encoding for nitrile hydratase α) ( de Souza et al, 2019 ). It is important to note that although the indole-3-acetamide pathway was considered as being exclusive for the excessive IAA production by gall forming bacteria like P. savastanoi , Erwinia spp., and Agrobacterium transformed plant tissue ( Jameson, 2000 ), these genes are also present in methylotrophic rhizosphere microorganisms ( Li et al, 2019 ).…”