Quorum Sensing Regulates the Hydrolytic Enzyme Production and Community Composition of Heterotrophic Bacteria in Coastal Waters

Abstract

Heterotrophic microbial communities play a central role in biogeochemical cycles in the ocean by degrading organic matter through the synthesis of extracellular hydrolytic enzymes. Their hydrolysis rates result from the community’s genomic potential and the differential expression of this genomic potential. Cell-cell communication pathways such as quorum sensing (QS) could impact both aspects and, consequently, structure marine ecosystem functioning. However, the role of QS communications in complex natural assemblages remains largely unknown. In this study, we investigated whether N-acylhomoserine lactones (AHLs), a type of QS signal, could regulate both hydrolytic activities and the bacterial community composition (BCC) of marine planktonic assemblages. To this extent, we carried out two microcosm experiments, adding five different AHLs to bacterial communities sampled in coastal waters (during early and peak bloom) and monitoring their impact on enzymatic activities and diversity over 48 h. Several specific enzymatic activities were impacted during both experiments, as early as 6 h after the AHL amendments. The BCC was also significantly impacted by the treatments after 48 h, and correlated with the expression of the hydrolytic activities, suggesting that changes in hydrolytic intensities may drive changes in BCC. Overall, our results suggest that QS communication could participate in structuring both the function and diversity of marine bacterial communities.

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

“…Van Mooy et al (2012) made similar observations in epibiontic bacteria colonizing Trichodesmium colonies, demonstrating that the addition of C8-, 3-oxo-C8-HSL and long-chain AHLs (a cocktail of C10-, C12-and C14-HSL) induced a doubling of extracellular alkaline phosphatase activity (total activity). Finally, Urvoy et al (2021b) showed that the addition of low concentrations of C4-, C6-, 3-oxo-C8-, C12-or C16-HSL to coastal bacterioplankton communities sampled in two contrasting stages of the spring phytoplankton bloom differently modified their extracellular leucine aminopeptidase, N-acetyl glucosaminidase, lipase and β-glucuronidase activities (total activity), further highlighting the complexity of QS regulation.…”

“…The possible role of QS in synchronizing hydrolase expression in bacteria would impact C, P, and N cycles through the degradation of various polymers. Several studies have examined the implications of QS in hydrolase expression in either isolated strains (Jatt et al, 2015;Su et al, 2019;Urvoy et al, 2021a) or natural bacterial communities from various environments (Hmelo et al, 2011;Van Mooy et al, 2012;Krupke et al, 2016;Su et al, 2019;Urvoy et al, 2021b; Supplementary Table 4). These studies, mainly performed in the context of AHL-based QS, have largely demonstrated the complexity of QS regulation, as no clear pattern has emerged.…”

“…Once bacterial cells settle into relevant microniches, QS regulates a myriad of phenotypes that could further alter the BCC. Thus far, four studies have demonstrated a direct influence of AI amendment on the composition of marine planktonic communities (Whalen et al, 2019;Urvoy et al, 2021b) and established marine and lacustrine biofilm communities (Wang et al, 2020;Xu et al, 2021). Whalen et al (2019) showed that HHQ addition to microbial communities sampled along a simulated phytoplanktonic bloom altered the BCC of both PA and FL heterotrophic bacteria, with highly variable effects depending on the bloom stage.…”

“…Whalen et al (2019) also found that HHQ exposure reduced the growth of eukaryotes (especially nanoeukaryotes) without altering their composition. Urvoy et al (2021b) showed that amendment with low concentrations of different AHLs (50 nM, C4-to C16-HSL) altered the composition of planktonic bacterial communities sampled at two stages of coastal phytoplanktonic spring bloom as well as their hydrolytic activities. Similar to Whalen et al (2019), the AHL effect widely differed depending on the bloom stage.…”

“…QS is known to regulate the production of a number of public goods (Whiteley et al, 2017;Mukherjee and Bassler, 2019). In the highlighted articles, QS altered hydrolytic enzymes (Urvoy et al, 2021b) and polysaccharide production (Xu et al, 2021), which could drive changes in the BCC. In the study by Urvoy et al (2021b), the changes in hydrolytic enzymes and bacterial diversity were correlated, supporting this hypothesis.…”