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

Olivier Pereira , Wei Qin , Pierre E. Galand , Didier Debroas , Raphael Lami , Corentin Hochart , Yangkai Zhou , Jin Zhou , Chuanlun Zhang

mLife ›› 2024, Vol. 3 ›› Issue (3) : 417 -429.

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mLife ›› 2024, Vol. 3 ›› Issue (3) : 417 -429. DOI: 10.1002/mlf2.12144
ORIGINAL RESEARCH

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

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Abstract

Ammonia-oxidizing archaea (AOA) play crucial roles in marine carbon and nitrogen cycles by fixing inorganic carbon and performing the initial step of nitrification. Evaluation of carbon and nitrogen metabolism popularly relies on functional genes such as amoA and accA. Increasing studies suggest that quorum sensing (QS) mainly studied in biofilms for bacteria may serve as a universal communication and regulatory mechanism among prokaryotes; however, this has yet to be demonstrated in marine planktonic archaea. To bridge this knowledge gap, we employed a combination of metabolic activity markers (amoA, accA, and grs) to elucidate the regulation of AOA-mediated nitrogen, carbon processes, and their interactions with the surrounding heterotrophic population. Through co-transcription investigations linking metabolic markers to potential key QS genes, we discovered that QS molecules could regulate AOA’s carbon, nitrogen, and lipid metabolisms under different conditions. Interestingly, specific AOA ecotypes showed a preference for employing distinct QS systems and a distinct QS circuit involving a typical population. Overall, our data demonstrate that QS orchestrates nitrogen and carbon metabolism, including the exchange of organic metabolites between AOA and surrounding heterotrophic bacteria, which has been previously overlooked in marine AOA research.

Keywords

AOA functional genes / marine ammonia-oxidizing archaea / networking / quorum sensing / Tara Oceans

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Olivier Pereira, Wei Qin, Pierre E. Galand, Didier Debroas, Raphael Lami, Corentin Hochart, Yangkai Zhou, Jin Zhou, Chuanlun Zhang. Metabolic activities of marine ammonia-oxidizing archaea orchestrated by quorum sensing. mLife, 2024, 3(3): 417-429 DOI:10.1002/mlf2.12144

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2024 The Author(s). mLife published by John Wiley & Sons Australia, Ltd on behalf of Institute of Microbiology, Chinese Academy of Sciences.

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