The lactonase BxdA mediates metabolic adaptation of maize root bacteria to benzoxazinoids

Author:

Thoenen LisaORCID,Kreuzer MarcoORCID,Florean MatildeORCID,Mateo PierreORCID,Züst TobiasORCID,Giroud CaitlinORCID,Rouyer LizaORCID,Gfeller ValentinORCID,Notter Matheus D.ORCID,Knoch EvaORCID,Hapfelmeier SiegfriedORCID,Becker ClaudeORCID,Schandry NiklasORCID,Robert Christelle A. M.ORCID,Köllner Tobias G.ORCID,Bruggmann RémyORCID,Erb MatthiasORCID,Schlaeppi KlausORCID

Abstract

AbstractRoot exudates contain secondary metabolites that affect the plant’s root microbiome. How microbes cope with these bioactive compounds, and how this ability shapes root microbiomes remain largely unknown. We investigated how maize root bacteria metabolise benzoxazinoids, the main specialised metabolites of maize. Diverse and abundant bacteria metabolised the major compound (6-methoxy-benzoxazolin-2-one, MBOA) in the maize rhizosphere to 2-amino-7-methoxyphenoxazin-3-one (AMPO). By contrast, bacteria isolated from Arabidopsis, which does not produce benzoxazinoids, were unable to metabolise MBOA. AmongMicrobacteriastrains, this differential metabolisation allowed to identify a conserved gene cluster containing the lactonasebxdA. BxdA converts MBOA to AMPO in vitro and we show that this capacity provided bacteria a growth benefit under carbon-limiting conditions. Together these results reveal that maize root bacteria - through BxdA - are metabolically adapted to the benzoxazinoids of their host. We propose that metabolic adaptation to plant-specialised compounds shapes root bacterial communities across the plant kingdom.

Publisher

Cold Spring Harbor Laboratory

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