Microbiome manipulation by corals and other Cnidaria via quorum quenching

Mason, Benjamin, Hayward, David C., Moya, Aurelie, Cooke, Ira, Sorenson, Alanna, Brunner, Ramona, Andrade Rodriguez, Natalia, Huerlimann, Roger, Bourne, David G., Schaeffer, Patrick, Grinblat, Mila, Ravasi, Timothy, Ueda, Nobuo, Tang, Sen-Lin, Ball, Eldon E., and Miller, David J. (2024) Microbiome manipulation by corals and other Cnidaria via quorum quenching. Current Biology, 34. pp. 3226-3232.

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Abstract

A dynamic mucous layer containing numerous micro-organisms covers the surface of corals and has multiple functions including both removal of sediment and ‘‘food gathering.’’1 It is likely to also act as the primary barrier to infection; various proteins and compounds with antimicrobial activity have been identified in coral mucus, though these are thought to be largely or exclusively of microbial origin. As in Hydra,2 anti-microbial peptides (AMPs) are likely to play major roles in regulating the microbiomes of corals.3,4 Some eukaryotes employ a complementary but less obvious approach to manipulate their associated microbiome by interfering with quorum signaling, effectively preventing bacteria from coordinating gene expression across a population. Our investigation of immunity in the reef-building coral Acropora millepora,5 however, led to the discovery of a coral gene referred to here as AmNtNH1 that can inactivate a range of acyl homoserine lactones (AHLs), common bacterial quorum signaling molecules, and is induced on immune challenge of adult corals and expressed during the larval settlement process. Closely related proteins are widely distributed within the Scleractinia (hard corals) and some other cnidarians, with multiple paralogs in Acropora, but their closest relatives are bacterial, implying that these are products of one or more lateral gene transfer events post-dating the cnidarian-bilaterian divergence. The deployment by corals of genes used by bacteria to compete with other bacteria reflects a mechanism of microbiome manipulation previously unknown in Metazoa but that may apply more generally.

Item ID: 83410
Item Type: Article (Research - C1)
ISSN: 1879-0445
Keywords: acyl homoserine lactone,Cnidaria,coral microbiome,lateral gene transfer,NtN-hydrolase,quorum quenching,symbiosis
Copyright Information: Crown Copyright © 2024 Published by Elsevier Inc. All rights are reserved, including those for text and data mining, AI training, and similar technologies.
Additional Information:

Codes added. WB 09.08.24

Funders: Australian Research Council (ARC)
Projects and Grants: ARC Discovery Grant DP170104734, ARC Centres of Excellence Grant CE14100020
Date Deposited: 13 Aug 2024 02:43
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