Abstract

The family Flavobacteriaceae (phylum Bacteroidetes) is a major component of soil, marine and freshwater ecosystems. In this understudied family, Flavobacterium psychrophilum is a freshwater pathogen that infects salmonid fish worldwide, with critical environmental and economic impact. Here, we report an extensive transcriptome analysis that established the genome map of transcription start sites and transcribed regions, predicted alternative sigma factor regulons and regulatory RNAs, and documented gene expression profiles across 32 biological conditions mimicking the pathogen life cycle. The results link genes to environmental conditions and phenotypic traits and provide insights into gene regulation, highlighting similarities with better known bacteria and original characteristics linked to the phylogenetic position and the ecological niche of the bacterium. In particular, osmolarity appears as a signal for transition between free-living and within-host programs and expression patterns of secreted proteins shed light on probable virulence factors. Further investigations showed that a newly discovered sRNA widely conserved in the genus, Rfp18, is required for precise expression of proteases. By pointing proteins and regulatory elements probably involved in host–pathogen interactions, metabolic pathways, and molecular machineries, the results suggest many directions for future research; a website is made available to facilitate their use to fill knowledge gaps on flavobacteria.

Highlights

  • Aquaculture is the fastest growing food-producing sector and accounts for half of the human fish consumption in the world [1]

  • By pointing proteins and regulatory elements probably involved in host–pathogen interactions, metabolic pathways, and molecular machineries, the results suggest many directions for future research; a website is made available to facilitate their use to fill knowledge gaps on flavobacteria

  • These results document how F. psychrophilum adapts its pool of secreted degradative enzymes and allow to formulate hypotheses on their respective importance at particular life stages. Expression of this large variety of degradative enzymes and their refined regulation at environmental transitions highlight sophisticated adaptations to a pathogenic lifestyle. Due to their diverse ecological niches and their important contribution to aquatic ecosystems, there is a great interest in flavobacteria [2]

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Summary

Introduction

Aquaculture is the fastest growing food-producing sector and accounts for half of the human fish consumption in the world [1]. A primary concern of this expending sector is the control of infectious diseases, such as those caused by bacteria of the family Flavobacteriaceae. The conditions, known as rainbow trout fry syndrome and bacterial cold-water disease, are major sanitary issues for the fish farming activity worldwide. Infected fish present signs of tissue erosion, skin ulcerations, necrotic lesions and splenic hypertrophy. The bacterium is mainly found in skin lesions, dermal ulcers extending deeply into muscular tissues, and in lymphoid organs [7]. The disease often occurs as a septicemic form and mortality reaches 70% [5]

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