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

Sylvain François-Étienne (), Leroux Nicolas, Normandeau Eric, Custodio Jaqueline, Mercier Pierre-Luc, Bouslama Sidki, Holland Aleicia, Barroso Danilo, Val Adalberto Luis and Derome Nicolas
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Sylvain François-Étienne: Université Laval
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

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-39461-x

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