Bacterial tolerance to host-exuded specialized metabolites structures the maize root microbiome

Author:

Thoenen Lisa12ORCID,Giroud Caitlin2ORCID,Kreuzer Marco3ORCID,Waelchli Jan2,Gfeller Valentin1ORCID,Deslandes-Hérold Gabriel1ORCID,Mateo Pierre1ORCID,Robert Christelle A. M.1,Ahrens Christian H.4ORCID,Rubio-Somoza Ignacio5,Bruggmann Rémy3,Erb Matthias1,Schlaeppi Klaus12ORCID

Affiliation:

1. Institute of Plant Sciences, University of Bern, Bern 3013, Switzerland

2. Department of Environmental Sciences, University of Basel, Basel 4056, Switzerland

3. Interfaculty Bioinformatics Unit, University of Bern, Bern 3012, Switzerland

4. Method Development and Analytics, Group Molecular Ecology, Agroscope, Zürich 8046, Switzerland

5. Molecular Reprogramming and Evolution Lab, Centre for Research in Agricultural Genomics, Barcelona 08193, Spain

Abstract

Plants exude specialized metabolites from their roots, and these compounds are known to structure the root microbiome. However, the underlying mechanisms are poorly understood. We established a representative collection of maize root bacteria and tested their tolerance against benzoxazinoids (BXs), the dominant specialized and bioactive metabolites in the root exudates of maize plants. In vitro experiments revealed that BXs inhibited bacterial growth in a strain- and compound-dependent manner. Tolerance against these selective antimicrobial compounds depended on bacterial cell wall structure. Further, we found that native root bacteria isolated from maize tolerated the BXs better compared to nonhost Arabidopsis bacteria. This finding suggests the adaptation of the root bacteria to the specialized metabolites of their host plant. Bacterial tolerance to 6-methoxy-benzoxazolin-2-one (MBOA), the most abundant and selective antimicrobial metabolite in the maize rhizosphere, correlated significantly with the abundance of these bacteria on BX-exuding maize roots. Thus, strain-dependent tolerance to BXs largely explained the abundance pattern of bacteria on maize roots. Abundant bacteria generally tolerated MBOA, while low abundant root microbiome members were sensitive to this compound. Our findings reveal that tolerance to plant specialized metabolites is an important competence determinant for root colonization. We propose that bacterial tolerance to root-derived antimicrobial compounds is an underlying mechanism determining the structure of host-specific microbial communities.

Funder

One Health University of Bern

MINECO

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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