Disrupting quorum sensing alters social interactions in Chromobacterium violaceum

Sonia Mion,Gérald Culioli,Julien Lopez,David Daudé,Eric Chabrière,Annick Ortalo-Magné,Laure Plener,Nathan Carriot

doi:10.1038/s41522-021-00211-w

Abstract

Quorum sensing (QS) is a communication system used by bacteria to coordinate a wide panel of biological functions in a cell density-dependent manner. The Gram-negative Chromobacterium violaceum has previously been shown to use an acyl-homoserine lactone (AHL)-based QS to regulate various behaviors, including the production of proteases, hydrogen cyanide, or antimicrobial compounds such as violacein. By using combined metabolomic and proteomic approaches, we demonstrated that QS modulates the production of antimicrobial and toxic compounds in C. violaceum ATCC 12472. We provided the first evidence of anisomycin antibiotic production by this strain as well as evidence of its regulation by QS and identified new AHLs produced by C. violaceum ATCC 12472. Furthermore, we demonstrated that targeting AHLs with lactonase leads to major QS disruption yielding significant molecular and phenotypic changes. These modifications resulted in drastic changes in social interactions between C. violaceum and a Gram-positive bacterium (Bacillus cereus), a yeast (Saccharomyces cerevisiae), immune cells (murine macrophages), and an animal model (planarian Schmidtea mediterranea). These results underscored that AHL-based QS plays a key role in the capacity of C. violaceum to interact with micro- and macroorganisms and that quorum quenching can affect microbial population dynamics beyond AHL-producing bacteria and Gram-negative bacteria.

Highlights

Many proteobacteria use acyl-homoserine lactones (AHLs) to orchestrate their behavior in a cell density-dependent manner[1].This communication system, referred to as quorum sensing (QS), plays a key role in bacterial adaptation to the environment
We considered the use of the lactonase SsoPox W263I, a quorum-quenching enzymes (QQE) able to degrade a wide spectrum of AHLs and to affect microbial communities from soil and freshwater ecosystems, to decipher how QQ can modulate molecular mechanisms involved in social interactions[18] in a single proteobacteria species representative from these ecosystems
We further provided a series of experiments suggesting that SsoPox W263I alters the ability of C. violaceum to produce QS-regulated antimicrobials and to compete with prokaryotic and eukaryotic

Summary

INTRODUCTION

Many proteobacteria use acyl-homoserine lactones (AHLs) to orchestrate their behavior in a cell density-dependent manner[1] This communication system, referred to as quorum sensing (QS), plays a key role in bacterial adaptation to the environment. Disrupting QS has appeared as a promising way to counteract bacterial behavior in fields of application useful for human healthcare and agriculture[8] To this end, many strategies have been considered, including inhibition of QS signals using chemical inhibitors (QSI), their sequestration by antibodies, or the use of quorum-quenching enzymes (QQE). We considered the use of the lactonase SsoPox W263I, a QQE able to degrade a wide spectrum of AHLs and to affect microbial communities from soil and freshwater ecosystems, to decipher how QQ can modulate molecular mechanisms involved in social interactions[18] in a single proteobacteria species representative from these ecosystems. These results indicate that disrupting QS may broadly impact interspecies interactions and microbial population dynamics

RESULTS

DISCUSSION

METHODS

CODE AVAILABILITY