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Important role of endogenous microbial symbionts of fish gills in the challenging but highly biodiverse Amazonian blackwaters

Author

Listed:
  • Sylvain François-Étienne

    (Université Laval
    Gulf Fisheries Center)

  • Leroux Nicolas

    (Université Laval)

  • Normandeau Eric

    (Université Laval)

  • Custodio Jaqueline

    (Laboratório de Ecofisiologia e Evolução Molecular)

  • Mercier Pierre-Luc

    (Université Laval)

  • Bouslama Sidki

    (Université Laval)

  • Holland Aleicia

    (Albury/Wodonga Campus)

  • Barroso Danilo

    (Laboratório de Ecofisiologia e Evolução Molecular)

  • Val Adalberto Luis

    (Laboratório de Ecofisiologia e Evolução Molecular)

  • Derome Nicolas

    (Université Laval)

Abstract

Amazonian blackwaters are extremely biodiverse systems containing some of Earth’s most naturally acidic, dissolved organic carbon -rich and ion‐poor waters. Physiological adaptations of fish facing these ionoregulatory challenges are unresolved but could involve microbially-mediated processes. Here, we characterize the physiological response of 964 fish-microbe systems from four blackwater Teleost species along a natural hydrochemical gradient, using dual RNA-Seq and 16 S rRNA of gill samples. We find that host transcriptional responses to blackwaters are species-specific, but occasionally include the overexpression of Toll-receptors and integrins associated to interkingdom communication. Blackwater gill microbiomes are characterized by a transcriptionally-active betaproteobacterial cluster potentially interfering with epithelial permeability. We explore further blackwater fish-microbe interactions by analyzing transcriptomes of axenic zebrafish larvae exposed to sterile, non-sterile and inverted (non-native bacterioplankton) blackwater. We find that axenic zebrafish survive poorly when exposed to sterile/inverted blackwater. Overall, our results suggest a critical role for endogenous symbionts in blackwater fish physiology.

Suggested Citation

  • Sylvain François-Étienne & Leroux Nicolas & Normandeau Eric & Custodio Jaqueline & Mercier Pierre-Luc & Bouslama Sidki & Holland Aleicia & Barroso Danilo & Val Adalberto Luis & Derome Nicolas, 2023. "Important role of endogenous microbial symbionts of fish gills in the challenging but highly biodiverse Amazonian blackwaters," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39461-x
    DOI: 10.1038/s41467-023-39461-x
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    1. Daniel H Huson & Sina Beier & Isabell Flade & Anna Górska & Mohamed El-Hadidi & Suparna Mitra & Hans-Joachim Ruscheweyh & Rewati Tappu, 2016. "MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data," PLOS Computational Biology, Public Library of Science, vol. 12(6), pages 1-12, June.
    2. Yuuki Obata & Álvaro Castaño & Stefan Boeing & Ana Carina Bon-Frauches & Candice Fung & Todd Fallesen & Mercedes Gomez Agüero & Bahtiyar Yilmaz & Rita Lopes & Almaz Huseynova & Stuart Horswell & Mural, 2020. "Neuronal programming by microbiota regulates intestinal physiology," Nature, Nature, vol. 578(7794), pages 284-289, February.
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