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

Marco Fusi, David Ngugi, Ramona Marasco, Jenny Marie Booth, Massimiliano Cardinale, Luciano Sacchi, Emanuela Clementi, Xinyuan Yang, Elisa Garuglieri, Stylianos Fodelianakis, Gregoire Michoud, Daniele Daffonchio

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

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. Video Abstract.
Original languageEnglish (US)
JournalMicrobiome
Volume11
Issue number1
DOIs
StatePublished - Aug 24 2023

Bibliographical note

KAUST Repository Item: Exported on 2023-08-31
Acknowledged KAUST grant number(s): CRG-7-3739
Acknowledgements: The study was supported by King Abdullah University of Science and Technology (baseline research funds to DD) and the Competitive Research Grant (CRG-7-3739) to DD “The role of the bacterial symbiome at the gill-water (air) interface in the evolution towards terrestrialisation (Microlanding)”. Thanks to Giulia Liberatori for invaluable help in the laboratory, and to Riccardo Simoni, Simone Babbini, Francesca Porri, Christopher McQuaid, Carmelo La Barba, and Bruce Mostert for fundamental help during Kenyan and South African fieldwork. We also thank the Gazi (Kenya) villagers for their help collecting the animals and Latifa’s family for accommodation. We thank the BLC and Imaging KAUST Core Lab Facilities for their invaluable support in producing sequencing and imaging data for this paper.

ASJC Scopus subject areas

  • Microbiology (medical)
  • Microbiology

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