Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots

Abstract

In nature, roots of healthy plants are colonized by multikingdom microbial communities that include bacteria, fungi, and oomycetes. A key question is how plants control the assembly of these diverse microbes in roots to maintain host–microbe homeostasis and health. Using microbiota reconstitution experiments with a set of immunocompromised Arabidopsis thaliana mutants and a multikingdom synthetic microbial community (SynCom) representative of the natural A. thaliana root microbiota, we observed that microbiota-mediated plant growth promotion was abolished in most of the tested immunocompromised mutants. Notably, more than 40% of between-genotype variation in these microbiota-induced growth differences was explained by fungal but not bacterial or oomycete load in roots. Extensive fungal overgrowth in roots and altered plant growth was evident at both vegetative and reproductive stages for a mutant impaired in the production of tryptophan-derived, specialized metabolites (cyp79b2/b3). Microbiota manipulation experiments with single- and multikingdom microbial SynComs further demonstrated that 1) the presence of fungi in the multikingdom SynCom was the direct cause of the dysbiotic phenotype in the cyp79b2/b3 mutant and 2) bacterial commensals and host tryptophan metabolism are both necessary to control fungal load, thereby promoting A. thaliana growth and survival. Our results indicate that protective activities of bacterial root commensals are as critical as the host tryptophan metabolic pathway in preventing fungal dysbiosis in the A. thaliana root endosphere.

Lifestyle Transitions in Fusarioid Fungi are Frequent and Lack Clear Genomic Signatures

“…There is no single role that endophytes play in the plant host, as the endophytic lifestyle represents a functional range between pathogenicity and mutualism, which has been dubbed the “endophytic continuum” ( Schulz and Boyle 2005 ). The outcome of endophyte colonisation can be highly dependent on the context of the plant–fungal interaction, such as the status of the plant immune system and nutrient conditions ( Junker et al 2012 ; Lahrmann et al 2015 ; Hacquard et al 2016 ; Hiruma et al 2016 ), as well as the presence of other endophytes within the microbiome ( Redman et al 2001 ; Durán et al 2018 ; Mesny et al 2021 ; Wolinska et al 2021 ) and even light conditions ( Álvarez-Loayza et al 2011 ). The transient status of endophytism for many taxa is evident from observations of endophytes becoming decayers (saprotrophs) or pathogens following some change in host or abiotic conditions ( Slippers and Wingfield 2007 ; Arnold et al 2009 ; Promputtha et al 2010 ; Swett and Gordon 2015 ; Nelson et al 2020 ).…”

Microbiota-mediated nitrogen fixation and homeostasis in aerial root-mucilage

“…Such as, plant special metabolites triterpenes, coumarin, flavonoid and benzoxazinoid are key compounds modulating plant microbiota composition (Cadot et al, 2021, Cotton et al, 2019, Harbort et al, 2020, Hu et al, 2018, Kudjordjie et al, 2019, Pang et al, 2021, Schütz et al, 2019, and root secretes coumarin to against pathogens and impact the assembly of rhizosphere microbiota (Stringlis et al, 2018). Moreover, the important of plant metabolites or root exudates in defense pathogens and maintain microbial homeostasis in the rhizosphere is increasingly recognized, such as volatile organic compounds, tryptophan, phytohormones and camalexin (Hammerbacher et al, 2019, Koprivova et al, 2019, Macabuhay et al, 2021, Pang et al, 2021, Sharifi et al, 2018, Stassen et al, 2020, Wolinska et al, 2021. It is reasonable to speculate that the specialized compounds of aerial root mucilage to recruit special microbiota as nutrients, but also some proteins and compounds that could serve as antibiotics to defense pathogenic and environmental microbe or maintain the homeostasis of the mucilage-microbiota system.…”

“…The current hypothesis is that microbial homeostasis in plant roots is main maintain by both microbiotamicrobiota and host plant-microbiota and interactions, whereas little is known of those distinct outputs in maintaining microbial homeostatic between the plant and its root microbiota (Getzke et al, 2019, Wolinska et al, 2021. Our discovery of Chaetomella raphigera (F-XTBG8)-the ''police'' fungi that helps mucilage and diazotrophic bacteria withstand pathogenic and environmental microbes-establishes that the existence of such beneficial partnerships in aerial root-mucilage microhabitat.…”

“…A recent study showed that soil bacteria Paraburkholderia edwinii as a toxin sponge to protect fungi by sequestering antibiotic phenazines (Dahlstrom and Newman 2022). Interestingly, host-microbe and microbe-microbe interactions can also simultaneously produce synergistic effects to maintain microbial homeostasis in plant roots, such as Arabidopsis root bacterial microbial communities and plant metabolite tryptophan jointly control soil fungal pathogens Plectosphaerella cucumerina to promote plant growth and health (Wolinska et al, 2021).…”

Modulation of Arabidopsis growth by volatile organic compounds from a root-derived bacterial community

“…While such specialized plant metabolites help to shape the bacterial microbiome (Jacoby et al, 2021; Wolinska et al, 2021), the role of underground metabolites from the bacterial communities in plant-microbiota interaction is less clear. In particular, bacteria release Volatile Organic Compounds (bVOCs) that are characterized by a low molecular mass (< 300 Da), low boiling point and high vapor pressure allowing interaction and signaling in short- and long-distance via soil, air and water (Schulz & Dickschat, 2007; Weisskopf et al, 2021).…”