A widespread methylotroph acyl-homoserine lactone synthase produces a new quorum sensing signal that regulates swarming in Methylobacterium fujisawaense

Abstract

ABSTRACT Pink-pigmented facultative methylotrophs of the genera Methylorubrum and Methylobacterium are metabolically versatile bacteria that colonize many diverse environments on earth. Despite their widespread occurrence, the molecular details of how these organisms interact with each other and their environment remain understudied. We analyzed genes encoding N -acylhomoserine lactone (acyl-HSL) quorum sensing signal synthases in the published genomes of these bacteria and determined that the product of the largest family of signal synthases had not been characterized. We identified 3 R -OH-5 Z -C 12:1 -HSL as a novel signal produced by these synthases using inverse stable isotopic labeling and structural characterization by mass spectrometry, nuclear magnetic resonance spectroscopy, and chemical synthesis. We show that in the methylotroph Methylobacterium fujisawaense DSM5686, this signal activates its cognate LuxR-family transcription factor and is produced in a positive feedback loop. We also discover that in this strain, quorum sensing negatively regulates swarming motility by activating the expression of a small protein that binds a predicted transcription factor. These results characterize a previously undescribed, yet widespread quorum sensing system used by pink-pigmented facultative methylotrophs, which helps us understand the chemical ecology of these important bacteria. IMPORTANCE Bacteria known as pink-pigmented facultative methylotrophs colonize many diverse environments on earth, play an important role in the carbon cycle, and in some cases promote plant growth. However, little is known about how these organisms interact with each other and their environment. In this work, we identify one of the chemical signals commonly used by these bacteria and discover that this signal controls swarming motility in the pink-pigmented facultative methylotroph Methylobacterium fujisawaense DSM5686. This work provides new molecular details about interactions between these important bacteria and will help scientists predict these interactions and the group behaviors they regulate from genomic sequencing information.