Quorum sensing disruption regulates hydrolytic enzyme and biofilm production in estuarine bacteria

Type Article
Date 2021-11
Language English
Author(s) Urvoy MarionORCID1, 2, Lami RaphaelORCID3, Dreanno CatherineORCID5, Daudé DavidORCID4, Rodrigues Alice M S3, Gourmelon MicheleORCID1, L'Helguen StephaneORCID2, Labry ClaireORCID1
Affiliation(s) 1 : Ifremer, DYNECO, F-29280 Plouzané, France
2 : Université de Bretagne Occidentale, CNRS, IRD, Ifremer, UMR 6539, Laboratoire des Sciences de l’Environnement Marin (LEMAR), F-29280 Plouzané, France
3 : Sorbonne Université, CNRS, Laboratoire de Biodiversité et Biotechnologies Microbiennes (LBBM), 66650 Banyuls-sur-Mer, France
4 : Gene&GreenTK, 19-21 Boulevard Jean Moulin, 13005 Marseille, France
5 : Ifremer, RDT, F-29280 Plouzané, France
Source Environmental Microbiology (1462-2912) (Wiley / Blackwell), 2021-11 , Vol. 23 , N. 11 , P. 7183-7200
DOI 10.1111/1462-2920.15775
WOS© Times Cited 3
Abstract

Biofilms of heterotrophic bacteria cover organic matter aggregates and constitute hotspots of mineralization, primarily acting through extracellular hydrolytic enzyme production. Nevertheless, regulation of both biofilm and hydrolytic enzyme synthesis remains poorly investigated, especially in estuarine ecosystems. In this study, various bioassays, mass spectrometry and genomics approaches were combined to test the possible involvement of quorum sensing (QS) in these mechanisms. QS is a bacterial cell-cell communication system that relies notably on the emission of N-acylhomoserine lactones (AHLs). In our estuarine bacterial collection, we found that 28 strains (9%), mainly Vibrio, Pseudomonas and Acinetobacter isolates, produced at least 14 different types of AHLs encoded by various luxI genes. We then inhibited the AHL QS circuits of those 28 strains using a broad-spectrum lactonase preparation and tested whether biofilm production as well as β-glucosidase and leucineaminopeptidase activities were impacted. Interestingly, we recorded contrasted responses, as biofilm production, dissolved and cell-bound β-glucosidase and leucine-aminopeptidase activities significantly increased in 4%-68% of strains but decreased in 0%-21% of strains. These findings highlight the key role of AHL-based QS in estuarine bacterial physiology and ultimately on biogeochemical cycles. They also point out the complexity of QS regulations within natural microbial assemblages.

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Urvoy Marion, Lami Raphael, Dreanno Catherine, Daudé David, Rodrigues Alice M S, Gourmelon Michele, L'Helguen Stephane, Labry Claire (2021). Quorum sensing disruption regulates hydrolytic enzyme and biofilm production in estuarine bacteria. Environmental Microbiology, 23(11), 7183-7200. Publisher's official version : https://doi.org/10.1111/1462-2920.15775 , Open Access version : https://archimer.ifremer.fr/doc/00723/83499/