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

Lisa Thoenen, Marco Kreuzer, Christine Pestalozzi, Matilde Florean, Pierre Mateo, Tobias Züst, Anlun Wei, Caitlin Giroud, Liza Rouyer, Valentin Gfeller, Matheus D. Notter, Eva Knoch, Siegfried Hapfelmeier, Claude Becker, Niklas Schandry, Christelle A. M. Robert, Tobias G. Köllner, Rémy Bruggmann, Matthias Erb () and Klaus Schlaeppi ()
Additional contact information
Lisa Thoenen: University of Bern
Marco Kreuzer: University of Bern
Christine Pestalozzi: University of Basel
Matilde Florean: Max Planck Institute for Chemical Ecology
Pierre Mateo: University of Bern
Tobias Züst: University of Bern
Anlun Wei: University of Basel
Caitlin Giroud: University of Basel
Liza Rouyer: Ludwig-Maximilians-University Munich
Valentin Gfeller: University of Bern
Matheus D. Notter: University of Bern
Eva Knoch: Ludwig-Maximilians-University Munich
Siegfried Hapfelmeier: University of Bern
Claude Becker: Ludwig-Maximilians-University Munich
Niklas Schandry: Ludwig-Maximilians-University Munich
Christelle A. M. Robert: University of Bern
Tobias G. Köllner: Max Planck Institute for Chemical Ecology
Rémy Bruggmann: University of Bern
Matthias Erb: University of Bern
Klaus Schlaeppi: University of Bern

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Root exudates contain specialised metabolites that shape the plant’s root microbiome. How host-specific microbes cope with these bioactive compounds, and how this ability affects root microbiomes, remains largely unknown. We investigated how maize root bacteria metabolise benzoxazinoids, the main specialised metabolites of maize. Diverse and abundant bacteria metabolised the major compound in the maize rhizosphere MBOA (6-methoxybenzoxazolin-2(3H)-one) and formed AMPO (2-amino-7-methoxy-phenoxazin-3-one). AMPO forming bacteria were enriched in the rhizosphere of benzoxazinoid-producing maize and could use MBOA as carbon source. We identified a gene cluster associated with AMPO formation in microbacteria. The first gene in this cluster, bxdA encodes a lactonase that converts MBOA to AMPO in vitro. A deletion mutant of the homologous bxdA genes in the genus Sphingobium, did not form AMPO nor was it able to use MBOA as a carbon source. BxdA was identified in different genera of maize root bacteria. Here we show that plant-specialised metabolites select for metabolisation-competent root bacteria. BxdA represents a benzoxazinoid metabolisation gene whose carriers successfully colonize the maize rhizosphere and thereby shape the plant’s chemical environmental footprint.

Date: 2024
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DOI: 10.1038/s41467-024-49643-w

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