Bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean

Abstract

Background Marine bacteria form complex relationships with eukaryotic hosts, from obligate symbioses to pathogenic interactions. These interactions can be tightly regulated by bioactive molecules, creating a complex system of chemical interactions through which these species chemically communicate thereby directly altering the host’s physiology and community composition. Quorum sensing (QS) signals were first described in a marine bacterium four decades ago, and since then, we have come to discover that QS mediates processes within the marine carbon cycle, affects the health of coral reef ecosystems, and shapes microbial diversity and bacteria-eukaryotic host relationships. Yet, only recently have alkylquinolone signals been recognized for their role in cell-to-cell communication and the orchestration of virulence in biomedically relevant pathogens. The alkylquinolone, 2-heptyl-4-quinolone (HHQ), was recently found to arrest cell growth without inducing cell mortality in selected phytoplankton species at nanomolar concentrations, suggesting QS molecules like HHQ can influence algal physiology, playing pivotal roles in structuring larger ecological frameworks. Results To understand how natural communities of phytoplankton and bacteria respond to HHQ, field-based incubation experiments with ecologically relevant concentrations of HHQ were conducted over the course of a stimulated phytoplankton bloom. Bulk flow cytometry measurements indicated that, in general, exposure to HHQ caused nanoplankton and prokaryotic cell abundances to decrease. Amplicon sequencing revealed HHQ exposure altered the composition of particle-associated and free-living microbiota, favoring the relative expansion of both gamma- and alpha-proteobacteria, and a concurrent decrease in Bacteroidetes. Specifically, Pseudoalteromonas spp., known to produce HHQ, increased in relative abundance following HHQ exposure. A search of representative bacterial genomes from genera that increased in relative abundance when exposed to HHQ revealed that they all have the genetic potential to bind HHQ. Conclusions This work demonstrates HHQ has the capacity to influence microbial community organization, suggesting alkylquinolones have functions beyond bacterial communication and are pivotal in driving microbial community structure and phytoplankton growth. Knowledge of how bacterial signals alter marine communities will serve to deepen our understanding of the impact these chemical interactions have on a global scale. Electronic supplementary material The online version of this article (10.1186/s40168-019-0711-9) contains supplementary material, which is available to authorized users.

Opportunistic bacteria use quorum sensing to disturb coral symbiotic communities and mediate the occurrence of coral bleaching

“…Taking Vibrio as an example, its relative abundance was increased more than fivefold that of the control (Fig. ), a response that could be linked to Vibrio being capable of listening in and interpreting information from exogenous chemical signals in complex microbial communities (Whalen et al ., ). In fact, the QS system is well characterized in this genus, including that for V. cholerae , V. fischeri , and V. harveyi ; the last species, in particular, is closely related to a number of suspected and established marine pathogens from the Vibrio genus (Rosenberg and Falkovitz, ; Golberg et al ., ).…”

“…Recently, Whalen et al . () demonstrated alkylquinolones have the capacity to influence the phycosphere's microbial community organization, in which Pseudoalteromonas spp. was the strongest responder.…”

“…For former, Whalen et al . () pointed out that it reflects certain bacteria have the capability to sensing information from exogenous AHL signals in surrounding environment. In this case, some bacteria can increase their cell‐density under signals' regulation, just like the Vibrio (Fig.…”

Bacterial quorum sensing signal arrests phytoplankton cell division and protects against virus-induced mortality

“…and Pseudoalteromonas sp.) where it was observed to cause significant shifts in both natural phytoplankton and microbial communities 14 and induce species-specific decreases in phytoplankton growth at nanomolar concentrations 15 . However, the underlying molecular mechanism(s) by which HHQ influences phytoplankton fitness remains unknown.…”

Functional traits of particle-associated microbial assemblages in the low-latitude Pacific Ocean

“…Accordingly, it is important to elucidate the differences not only in microbial community structures but also in functional traits between PA and FL environmental sample fractions to reach a better understanding of marine microbial ecosystems. Although most bacterial community structure studies do not distinguish between PA and FL assemblages, several studies have compared microbial diversity between PA and FL fractions at individual marine sites [17,[20][21][22][23].…”