The V-Shaped Structuring Regulated via the LuxS-Dependent Quorum-Sensing Pathway Is Associated With Lactiplantibacillus plantarum Survivability in Acidic Environments

Abstract

Tolerance to acidic environments is an important adaptive feature of the probiotic bacterium Lactiplantibacillus plantarum for surviving gastrointestinal transit or food processing. Here, we report a previously uncharacterized biological process that enables a highly coordinated adaptation of this bacterium to acidic stress. We provide mechanistic evidence for the role of the V-shaped multicellular structuring, associated with incomplete daughter cell separation, in the survival of L. plantarum cells in acidic environments. We also show that this process facilitates structured biofilm formation through the LuxS-dependent quorum-sensing pathway associated with autoinducer-2 (AI-2) production. The LuxS knockout results in compromised V-shaped structuring and poor biofilm formation under acidic conditions, whereas exogenous supplementation of 4,5-dihydroxy-pentanedione (DPD), the precursor of AI-2, to the LuxS knockout strain, restores V-shaped structuring and biofilm formation in an acidic environment. Furthermore, we show that LuxS-dependent V-shaped structuring provides an extraordinary protection mode for cellular survivability in extremely acidic conditions. Consequently, we propose that the self-generated V-shaped structuring, regulated by LuxS, is associated with protective and coordinated multicellular behavior during adaptation to acidic stress. It is believed that this study paves the way for developing a promising platform for preserving and delivering probiotic cells to mammalian hosts by utilizing persistent geometrical structuring.