Cryptic, solo acylhomoserine lactone synthase from predatory myxobacterium suggests beneficial contribution to prey quorum signaling

Abstract

AbstractConsidered a key taxon in microbial communities, myxobacteria exist as coordinated swarms that utilize an excreted combination of lytic enzymes and specialized metabolites to facilitate predation of numerous microbial phyla. This capacity to produce biologically active metabolites and the associated abundance of natural product biosynthetic pathways contained within their genomes have motivated continued drug discovery efforts from myxobacteria. Of all the biosynthetic gene clusters associated with myxobacteria deposited in the antiSMASH database (∼1,000 total), only one putative acylhomoserine lactone synthase, agpI, was observed in genome data from the myxobacterium Archangium gephyra. Without an acylhomoserine lactone (AHL) receptor also apparent in the genome of A. gephyra, we sought to determine if AgpI was the first example of an orphaned AHL synthase. Herein we report the bioinformatic assessment of AgpI and discovery of a second myxobacterial AHL synthase from Vitiosangium sp. strain GDMCC 1.1324. During axenic cultivation conditions, no detectible AHL metabolites were observed in A. gephyra extracts. However, heterologous expression of each synthase in Escherichia coli provided detectible quantities of 3 AHL signals including 2 known AHLs, C8-AHL and C9-AHL. These results suggest that A. gephyra AHL production is dormant during axenic cultivation conditions and requires an unknown external cue for activation. The orphaned AHL synthase, AgpI, is the first to be reported from a predatory myxobacterium, and predator production of prey quorum signals provides unique insight into interspecies crosstalk within polymicrobial communities.ImportanceThe presence of orphaned quorum signal receptors and associated recognition and response to exogenous acylhomoserine lactone quorum signals observed in microbial communities provides evidence for small molecule-mediated interspecies interactions. While the high occurrence of orphaned AHL receptors from bacteria that do not produce cognate AHL signals suggests the involvement of AHL signals as a shared chemical resource in polymicrobial communities, no orphaned AHL synthases have been determined to be functional in a species without an associated AHL receptor. An orphan signal synthase from a predatory myxobacterium provides an alternative perspective on the evolution and benefits of quorum signaling systems within these communities.