Polyethylene terephthalate (PET) primary degradation products affect c-di-GMP-, cAMP-signaling, and quorum sensing (QS) in Vibrio gazogenes DSM 21264

Global plastic pollution in oceans and estuaries is increasing rapidly, and it is well known that bacteria colonize plastic particles of all sizes. Vibri o spp. are frequently found as part of the plastisphere. We recently showed that Vibrio gazogenes DSM 21264 harbors a promiscuous esterase designated PET6. We now provide evidence that the pet6 gene is expressed under a wide range of environmental conditions in its native host. However, in PET- and PE-grown biofilms, the pet6 gene expression was not affected by the type of surface. The pet6 transcription was sufficient to allow enzyme production and release of µM amounts of mono-(2-hydroxyethyl) terephthalate (MHET) and terephthalic acid (TPA) already after 24 hours of incubation on the PET foil. Notably, the highest pet6 gene transcription was observed in planktonic lifestyle in the presence of bis(2-hydroxyethyl) terephthalate (BHET), one of the primary degradation products of PET. BHET was further hydrolyzed by PET6 and UlaG, a lactonase that had not been known to be involved in BHET degradation. Elevated concentrations of BHET affected the major signaling circuits involved in bacterial quorum sensing (QS), c-di-GMP, and cAMP-CRP signaling. This resulted in failure to form biofilms, synthesis of the red pigment prodigiosin, and altered colony morphologies. While BHET had a very wide impact, TPA interfered mainly with the bacterial QS by attenuating the expression of the CAI-I autoinducer synthase gene. These observations imply a potential role of BHET and TPA as nutritional signals in Vibrio gazogenes and that may affect its growth and survival in the plastisphere. IMPORTANCE This study provides the first evidence that Vibrio gazogenes DSM 21264 secretes an active polyethylene terephthalate (PET) hydrolase and degrades the polymer using PET6 when growing in biofilms on foils and microplastic particles. The study further provides evidence that the primary PET degradation products bis(2-hydroxyethyl) terephthalate (BHET) and terephthalic acid (TPA) may have a profound impact on the global QS, c-di-GMP, and cAMP-CRP signaling of V. gazogenes and its capability to colonize plastic particles in the marine environment.