Quorum sensing: an invisible hand driving microbial cooperation in the oligotrophic ocean

Ammonia-oxidizing archaea (AOA) are crucial contributors to marine carbon and nitrogen cycles. They play a vital role by fixing inorganic carbon and performing the initial step of nitrification, which converts ammonia into nitrite—an essential process for nutrient cycling in oceans. Interestingly, while AOA do not fix organic carbon, they produce and release it into the environment, where it serves as a fuel source for the surrounding heterotrophic community. However, the regulatory mechanisms governing these processes remain largely unknown. Recent research indicates that quorum sensing (QS), a communication mechanism primarily studied in bacterial biofilms, may also function as a universal regulatory system among prokaryotes, including archaea. Despite this potential, the concept has not been thoroughly explored in marine planktonic archaea. To address this knowledge gap, we employed a combination of gene markers that encompass AOA metabolic activities and prokaryotic quorum sensing. Specifically, we analyzed transcripts from over 300 metatranscriptomic samples published by the Tara Ocean consortium. After validating the various markers, our co-transcription studies revealed that QS molecules significantly influence AOA's carbon, nitrogen, and lipid metabolism under different environmental conditions. Notably, we discovered that specific AOA ecotypes prefer distinct QS systems and exhibit unique QS circuits involving different populations. Overall, our findings underscore the critical role of QS in coordinating metabolic processes, including nitrogen and carbon metabolism. This coordination optimizes energy consumption during the exchange of organic metabolites between AOA and neighboring heterotrophic bacteria—a dynamic previously overlooked in marine AOA research. This discovery enhances our understanding of microbial interactions within marine ecosystems and their implications for nutrient cycling, suggesting that further exploration of QS mechanisms in AOA could provide significant insights into the complexities of marine biogeochemical processes.