Dual RNAseq highlights the kinetics of skin microbiome and fish host responsiveness to bacterial infection

Type Article
Date 2021-12
Language English
Author(s) Le Luyer JeremyORCID1, Schull Quentin1, 2, Auffret Pauline1, Lopez Pierre1, 3, Crusot Margaux1, 4, Belliard Corinne1, Basset Caline1, Carradec Q.5, Poulain J.5, Planes S.6, Saulnier Denis1
Affiliation(s) 1 : Ifremer, IRD, Institut Louis-Malardé, Univ Polynésie Française, EIO, F-98719 Taravao, Tahiti, Polynésie Française
2 : MARBEC, Univ. Montpellier, Ifremer, IRD, CNRS, F-34200, Sète, France
3 : Virologie et Immunologie Moléculaires, Institut National de la Recherche Agronomique, Université Paris-Saclay, Jouy-en-Josas, France
4 : Univ Polynésie française, Ifremer, IRD, Institut Louis-Malardé, EIO, F-98702 Fa, ’a, Tahiti, Polynésie Française
5 : Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057, Evry, France
6 : PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Moorea, Polynésie Française
Source Animal Microbiome (2524-4671) (Springer Science and Business Media LLC), 2021-12 , Vol. 3 , N. 1 , P. 35 (15p.)
DOI 10.1186/s42523-021-00097-1
Keyword(s) Microbiome, Gene expression, 16S rRNA, Nanopore, Tenacibaculum maritimum, Co-infection
Abstract

Background

Tenacibaculum maritimum is a fish pathogen known for causing serious damage to a broad range of wild and farmed marine fish populations worldwide. The recently sequenced genome of T. maritimum strain NCIMB 2154T provided unprecedented information on the possible molecular mechanisms involved in the virulence of this species. However, little is known about the dynamic of infection in vivo, and information is lacking on both the intrinsic host response (gene expression) and its associated microbiota. Here, we applied complementary omic approaches, including dual RNAseq and 16S rRNA gene metabarcoding sequencing using Nanopore and short-read Illumina technologies to unravel the host–pathogen interplay in an experimental infection system using the tropical fish Platax orbicularis as model.

Results

We showed that the infection of the host is characterised by an enhancement of functions associated with antibiotic and glucans catabolism functions but a reduction of sulfate assimilation process in T. maritimum. The fish host concurrently displays a large panel of immune effectors, notably involving innate response and triggering acute inflammatory response. In addition, our results suggest that fish activate an adaptive immune response visible through the stimulation of T-helper cells, Th17, with congruent reduction of Th2 and T-regulatory cells. Fish were, however, largely sensitive to infection, and less than 25% survived after 96 hpi. These surviving fish showed no evidence of stress (cortisol levels) or significant difference in microbiome diversity compared with controls at the same sampling time. The presence of T. maritimum in resistant fish skin and the total absence of any skin lesions suggest that these fish did not escape contact with the pathogen, but rather that some mechanisms prevented pathogens entry. In resistant individuals, we detected up-regulation of specific immune-related genes differentiating resistant individuals from controls at 96 hpi, which suggests a possible genomic basis of resistance, although no genetic variation in coding regions was found.

Conclusion

Here we focus in detail on the interplay between common fish pathogens and host immune response during experimental infection. We further highlight key actors of defence response, pathogenicity and possible genomic bases of fish resistance to T. maritimum.

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How to cite 

Le Luyer Jeremy, Schull Quentin, Auffret Pauline, Lopez Pierre, Crusot Margaux, Belliard Corinne, Basset Caline, Carradec Q., Poulain J., Planes S., Saulnier Denis (2021). Dual RNAseq highlights the kinetics of skin microbiome and fish host responsiveness to bacterial infection. Animal Microbiome, 3(1), 35 (15p.). Publisher's official version : https://doi.org/10.1186/s42523-021-00097-1 , Open Access version : https://archimer.ifremer.fr/doc/00697/80883/