Quorum Sensing Regulates Bacterial Processes That Play a Major Role in Marine Biogeochemical Cycles

Abstract

Bacteria play a crucial role in marine biogeochemistry by releasing, consuming and transforming organic matter. Far from being isolated entities, bacteria are involved in numerous cell–cell interactions. Among such interactions, quorum sensing (QS) allows bacteria to operate in unison, synchronizing their actions through chemical communication. This review aims to explore and synthesize our current knowledge of the involvement of QS in the regulation of bacterial processes that ultimately impact marine biogeochemical cycles. We first describe the principles of QS communication and the renewed interest in its study in marine environments. Second, we highlight that the microniches where QS is most likely to occur due to their high bacterial densities are also hotspots of bacterially mediated biogeochemical transformations. Many bacterial groups colonizing these microniches harbor various QS systems. Thereafter, we review relevant QS-regulated bacterial processes in marine environments, building on research performed in both complex marine assemblages and isolated marine bacteria. QS pathways have been shown to directly regulate organic matter degradation, carbon allocation and nutrient acquisition but also to structure the community composition by mediating colonization processes and microbial interactions. Finally, we discuss current limitations and future perspectives to better characterize the link between QS expression and the bacterial mediation of biogeochemical cycles. The picture drawn by this review highlights QS as one of the pivotal mechanisms impacting microbial composition and functions in the oceans, paving the way for future research to better constrain its impact on marine biogeochemical cycles.

Diversity of Bacteria with Quorum Sensing and Quenching Activities from Hydrothermal Vents in the Okinawa Trough

“…Actinobacteria are widespread in marine environments and reached high abundance in deep-sea sediments, organic aggregates and macroalgae [ 54 ]. In terms of QS, several bacteria belonging to Actinobacteria , which were isolated from marine snow [ 3 ] and microbial mats in Shark Bay Australia [ 16 ] or reef macroalgae [ 55 ], have been identified to show AHL-producing activities.…”

“…The QS pathways presented among marine bacteria may directly or indirectly influence biogeochemical cycles through the regulation of genes and EE activities, and the degradation of marine particles and marine snows [ 54 ]. Hmelo et al [ 46 ] demonstrated that the addition of 3OC 6 -HSL or 3OC 8 -HSL improved the extracellular aminopeptidase and phosphatase activities of bacterial communities colonizing marine snow.…”

Metabolic activities of marine ammonia-oxidizing archaea orchestrated by quorum sensing

“…To further advance our knowledge, additional studies are necessary to experimentally validate the complete mechanism. Techniques using biosensor reporter strains [78,79] and analytical methods like liquid chromatography and mass spectrometry [18,80]…”

“…Detecting QS/QQ systems in environmental samples can be challenging due to the diversity of gene sequences encoding these systems [18]. Advanced approaches, such as combining comprehensive environmental databases and large-scale metagenomics data, can increase our ability to identify organisms that have the potential to perform QS/QQ functions [17,18]. Ammonia-oxidizing archaea (AOA) are among the most abundant planktonic archaea in the ocean [19].…”

Impact of Quorum Sensing and Tropodithietic Acid Production on the Exometabolome of Phaeobacter inhibens

“…QS regulation of pathways for organic matter degradation, nutrient acquisition, colonization processes and microbial interactions has been studied extensively in marine bacteria ( Urvoy et al, 2022 ). Previous studies have also discussed the influence of QS in regulating production, release and/or uptake of specific metabolites ( An et al, 2014 ; Johnson et al, 2016 ; Landa et al, 2017 ; McRose et al, 2018 ).…”