Gill-associated bacteria are homogeneously selected in amphibious mangrove crabs to sustain host intertidal adaptation

Fusi, Marco; Ngugi, David K.; Marasco, Ramona; Booth, Jenny Marie; Cardinale, Massimiliano; Sacchi, Luciano; Clementi, Emanuela; Yang, Xinyuan; Garuglieri, Elisa; Fodelianakis, Stilianos; Michoud, Grégoire; Daffonchio, Daniele

Abstract

Background: The transition from water to air is a key event in the evolution of many marine organisms to access new food sources, escape water hypoxia, and exploit the higher and temperature-independent oxygen concentration of air. Despite the importance of microorganisms in host adaptation, their contribution to overcoming the challenges posed by the lifestyle changes from water to land is not well understood. To address this, we examined how microbial association with a key multifunctional organ, the gill, is involved in the intertidal adaptation of fiddler crabs, a dual-breathing organism. Results: Electron microscopy revealed a rod-shaped bacterial layer tightly connected to the gill lamellae of the five crab species sampled across a latitudinal gradient from the central Red Sea to the southern Indian Ocean. The gill bacterial community diversity assessed with 16S rRNA gene amplicon sequencing was consistently low across crab species, and the same actinobacterial group, namely Ilumatobacter, was dominant regardless of the geographic location of the host. Using metagenomics and metatranscriptomics, we detected that these members of actinobacteria are potentially able to convert ammonia to amino acids and may help eliminate toxic sulphur compounds and carbon monoxide to which crabs are constantly exposed. Conclusions: These results indicate that bacteria selected on gills can play a role in the adaptation of animals in dynamic intertidal ecosystems. Hence, this relationship is likely to be important in the ecological and evolutionary processes of the transition from water to air and deserves further attention, including the ontogenetic onset of this association.

Citation

Fusi, M., Ngugi, D. K., Marasco, R., Booth, J. M., Cardinale, M., Sacchi, L., Clementi, E., Yang, X., Garuglieri, E., Fodelianakis, S., Michoud, G., & Daffonchio, D. (2023). Gill-associated bacteria are homogeneously selected in amphibious mangrove crabs to sustain host intertidal adaptation. Microbiome, 11(1), Article 189. https://doi.org/10.1186/s40168-023-01629-4

• Journal Article Type: Article
• Acceptance Date: Jul 20, 2023
• Online Publication Date: Aug 24, 2023
• Publication Date: 2023
• Deposit Date: Aug 28, 2023
• Publicly Available Date: Aug 28, 2023
• Journal: Microbiome
• Publisher: BMC
• Peer Reviewed: Peer Reviewed
• Volume: 11
• Issue: 1
• Article Number: 189
• DOI: https://doi.org/10.1186/s40168-023-01629-4
• Keywords: Microbiome, Gill system, Terrestrialisation, Bimodal breathing, Symbiosis