Cofunctioning of bacterial exometabolites drives root microbiota establishment

Abstract

Soil-dwelling microbes are the principal inoculum for the root microbiota, but our understanding of microbe–microbe interactions in microbiota establishment remains fragmentary. We tested 39,204 binary interbacterial interactions for inhibitory activities in vitro, allowing us to identify taxonomic signatures in bacterial inhibition profiles. Using genetic and metabolomic approaches, we identified the antimicrobial 2,4-diacetylphloroglucinol (DAPG) and the iron chelator pyoverdine as exometabolites whose combined functions explain most of the inhibitory activity of the strongly antagonistic Pseudomonas brassicacearum R401. Microbiota reconstitution with a core of Arabidopsis thaliana root commensals in the presence of wild-type or mutant strains revealed a root niche-specific cofunction of these exometabolites as root competence determinants and drivers of predictable changes in the root-associated community. In natural environments, both the corresponding biosynthetic operons are enriched in roots, a pattern likely linked to their role as iron sinks, indicating that these cofunctioning exometabolites are adaptive traits contributing to pseudomonad pervasiveness throughout the root microbiota.

An iron fist in a velvet glove: The cooperation of a novel pyoverdine from Pseudomonas donghuensisP482 with 7‐hydroxytropolone is pivotal for its antibacterial activity

“…Due to their metabolic plasticity, Pseudomonas spp. can thrive in various environmental niches (Bai et al, 2015; Getzke et al, 2023; Loper et al, 2012; Raaijmakers et al, 2008; Zboralski & Filion, 2020) using available sources of carbon and nitrogen to establish and outcompete competitors via the production of antimicrobials (Duffy & Defago, 1999).…”

Simultaneous tracking of near-isogenic bacterial strains in syntheticArabidopsismicrobiota by chromosomally-integrated barcodes

“…Only a small number of genetic determinants in bacterial commensals influencing microbe-microbe and microbe-host interactions during plant microbiota establishment have thus far been identified (Getzke et al, 2023;Hemmerle et al, 2022;Liu et al, 2022). Bacterial DNA barcoding was applied to investigate antagonistic interactions of Pseudomonads leaf strains co-occurring on Arabidopsis (Shalev et al, 2022).…”

“…To validate MoBacTag as a spike-in plasmid using the bacterial 16S-, fungal ITS-, plant ITS-and barcode-specific primers, 0.15 ng of pBCC069 plasmid were mixed with 5 ng of extracted DNA from root and peat matrix samples, prepared by Getzke et al (2023). The standard curve was prepared with pBCC084 plasmid in tenfold dilution series from 1.5 to 0.00015 ng per PCR reaction.…”

“…Establishment of the plant microbiota is dependent on microbe-microbe and microbehost interactions. Numerous factors influence the composition of these plantassociated microbial assemblages: edaphic factors such as soil pH or soil-derived nutrients (Castrillo et al, 2017;Harbort et al, 2020), microbial competition or cooperation for plant-derived carbohydrates (Berendsen et al, 2018;Hemmerle et al, 2022), specialized plant-or microbe-derived exometabolites (Getzke et al, 2023;Hu et al, 2018;Huang et al, 2019;Voges et al, 2019), including antimicrobials, or pathogen effectors released by co-colonizing phytopathogens (Snelders et al, 2021;Snelders et al, 2020).…”

Root-associatedStreptomycesproduce galbonolides to modulate plant immunity and promote rhizosphere colonisation

“…Cross-kingdom communications play a significant role in shaping interactions between organisms within diverse ecological niches 1 . Microbe-microbe communication is often mediated by the secretion of small and diffusible specialised metabolites [2][3][4][5][6] . Throughout their lifecycle, eukaryotic organisms such as plants, are known to associate with the abundant and diverse community of microorganisms [7][8][9] .…”