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

Abstract

Abstracta)BackgroundTenacibaculum maritimum is a worldwide-distributed fish pathogen known for causing dramatic damages on a broad range of wild and farmed marine fish populations. Recently sequenced genome of T. maritimum strain NCIMB 2154T provided unprecedented information on the possible molecular mechanisms involved in virulence for this species. However, little is known on the dynamic on the infection in vivo, and information are lacking on both the intrinsic host response (gene expression) and its associated microbiome community. Here, we applied complementary omic approaches, including dual RNAseq and 16S rRNA gene metabarcoding sequencing using Nanopore and short-reads Illumina technologies to unravel the host-pathogens interplay in experimental infection system using the tropical fish Platax orbicularis as model.b)ResultsWe show that T. maritimum transcriptomic landscape during infection is characterized by an enhancement of antibiotic catalytic and glucan catalytic functions while decreasing specific sulphate assimilation process, compared to in vitro cultures. Simultaneously, fish host display a large palette of immune effectors, notably involving innate response and triggering acute inflammatory response. In addition, results suggest that fish activate adaptive immune response visible through 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% of them survived after 96hpi. These surviving fish showed no evidence of stress (cortisol levels) as well as no significant difference in microbiome diversity compared to control at the same sampling time. The presence of Tenacibaculum in resistant fish skin and the total absence of any skin lesion suggest that these fish did not escape contact with the pathogen but rather prevent the pathogen entry. In these individuals we detected the up-regulation of specific immune-related genes differentiating resistant from control at 96hpi, which suggests a possible genomic basis of resistance while no genetic variations in coding regions was reported.c)ConclusionHere we refine the interplay between common fish pathogens and host immune response during experimental infection. We further highlight key actors of defense response, pathogenicity and possible genomic bases of resistance to T. maritimum.