title: Coprinopsis cinerea intracellular lactonases hydrolyze quorum sensing molecules of Gram-negative bacteria.
abstract: Biofilm formation on fungal hyphae and production of antifungal molecules are strategies of bacteria in their competition with fungi for nutrients. Since these strategies are often coordinated and under control of quorum sensing by the bacteria, interference with this bacterial communication system can be used as a counter-strategy by the fungi in this competition. Hydrolysis of N-acyl-homoserine lactones (HSL), a quorum sensing molecule used by Gram-negative bacteria, by fungal cultures has been demonstrated. However, the enzymes that are responsible for this activity, have not been identified. In this study, we identified and characterized two paralogous HSL hydrolyzing enzymes from the coprophilous fungus Coprinopsis cinerea. The C. cinerea HSL lactonases belong to the metallo-β-lactamase family and show sequence homology to and a similar biochemical activity as the well characterized lactonase AiiA from Bacillus thuringiensis. We show that the fungal lactonases, similar to the bacterial enzymes, are kept intracellularly and act as a sink for the bacterial quorum sensing signals both in C. cinerea and in Saccharomyces cerevisiae expressing C. cinerea lactonases, due to the ability of these signal molecules to diffuse over the fungal cell wall and plasma membrane. The two isogenes coding for the C. cinerea HSL lactonases are arranged in the genome as a tandem repeat and expressed preferentially in vegetative mycelium. The occurrence of orthologous genes in genomes of other basidiomycetes appears to correlate with a saprotrophic lifestyle.
authors.affiliation: Institute of Microbiology, Department of Biology, ETH Zurich, Vladimir-Prelog-Weg 1-5/10, 8093 Zürich, Switzerland. Electronic address: smartina@ethz.ch.
authors.forename: Martina
authors.initials: M
authors.lastname: Stöckli
authors.affiliation: Institute of Microbiology, Department of Biology, ETH Zurich, Vladimir-Prelog-Weg 1-5/10, 8093 Zürich, Switzerland. Electronic address: linc@ethz.ch.
authors.forename: Chia-Wei
authors.initials: CW
authors.lastname: Lin
authors.affiliation: Institute of Microbiology, Department of Biology, ETH Zurich, Vladimir-Prelog-Weg 1-5/10, 8093 Zürich, Switzerland. Electronic address: ramsiebe@ethz.ch.
authors.forename: Ramon
authors.initials: R
authors.lastname: Sieber
authors.affiliation: Institute of Microbiology, Department of Biology, ETH Zurich, Vladimir-Prelog-Weg 1-5/10, 8093 Zürich, Switzerland. Electronic address: davidplaza@fas.harvard.edu.
authors.forename: David F
authors.initials: DF
authors.lastname: Plaza
authors.affiliation: Microbiology, Faculty of Science, Utrecht University, Padualaan 8, 3584 Utrecht, The Netherlands. Electronic address: r.a.ohm@uu.nl.
authors.forename: Robin A
authors.initials: RA
authors.lastname: Ohm
authors.affiliation: Institute of Microbiology, Department of Biology, ETH Zurich, Vladimir-Prelog-Weg 1-5/10, 8093 Zürich, Switzerland. Electronic address: mkuenzle@ethz.ch.
authors.forename: Markus
authors.initials: M
authors.lastname: Künzler
mesh_terms: D002265:Carboxylic Ester Hydrolases / Q000235:genetics / Q000378:metabolism*; D003302:Coprinus / Q000145:classification / Q000201:enzymology* / Q000235:genetics / Q000378:metabolism*; D006090:Gram-Negative Bacteria / Q000235:genetics / Q000378:metabolism*; D006868:Hydrolysis; D010802:Phylogeny; D053038:Quorum Sensing; D012689:Sequence Homology, Nucleic Acid
chemical_list: D002265:Carboxylic Ester Hydrolases; C020579:gluconolactonase
keywords: Bacterial-fungal interaction; HSL lactonase; Phylogenetic distribution; Quorum quenching; Saprotrophic fungi