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Genome analysis provides insights into the epidemiology of infection with Flavobacterium psychrophilum among farmed salmonid fish in Sweden.

ABSTRACT: The pathogen Flavobacterium psychrophilum is a major problem for the expanding salmonid fish farming industry in Sweden as well as worldwide. A better understanding of the phylogeography and infection routes of F. psychrophilum outbreaks could help to improve aquaculture profitability and the welfare of farmed fish while reducing the need for antibiotics. In the present study, high-throughput genome sequencing was applied to a collection of F. psychrophilum isolates (n=38) from outbreaks on fish farms in different regions of Sweden between 1988 and 2016. Antibiotic susceptibility tests were applied to a subset of the isolates and the results correlated to the presence of genetic resistance markers. We show that F. psychrophilum clones are not regionally biased and that new clones with a higher degree of antibiotic resistance have emerged nationwide during the study period. This supports previous theories of the importance of live fish and egg trade as a route of infection. Continuous monitoring of recovered isolates by high-throughput sequencing techniques in the future could facilitate tracing of clones within and between countries, as well as the detection of emergent virulent or antibiotic-resistant clones. This article contains data hosted by Microreact.

SUBMITTER: Soderlund R

PROVIDER: S-EPMC6412038 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Genome analysis provides insights into the epidemiology of infection with Flavobacterium psychrophilum among farmed salmonid fish in Sweden.

Söderlund Robert R Hakhverdyan Mikhayil M Aspán Anna A Jansson Eva E

Microbial genomics 20181213 12

The pathogen Flavobacterium psychrophilum is a major problem for the expanding salmonid fish farming industry in Sweden as well as worldwide. A better understanding of the phylogeography and infection routes of F. psychrophilum outbreaks could help to improve aquaculture profitability and the welfare of farmed fish while reducing the need for antibiotics. In the present study, high-throughput genome sequencing was applied to a collection of F. psychrophilum isolates (n=38) from outbreaks on fish ...[more]

PMID: 30543323

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Project description:Flavobacterium psychrophilum is a fish pathogen in salmonid aquaculture worldwide that causes cold water disease (CWD) and rainbow trout fry syndrome (RTFS). Comparative genome analyses of 11 F. psychrophilum isolates representing temporally and geographically distant populations were used to describe the F. psychrophilum pan-genome and to examine virulence factors, prophages, CRISPR arrays, and genomic islands present in the genomes. Analysis of the genomic DNA sequences were complemented with selected phenotypic characteristics of the strains. The pan genome analysis showed that F. psychrophilum could hold at least 3373 genes, while the core genome contained 1743 genes. On average, 67 new genes were detected for every new genome added to the analysis, indicating that F. psychrophilum possesses an open pan genome. The putative virulence factors were equally distributed among isolates, independent of geographic location, year of isolation and source of isolates. Only one prophage-related sequence was found which corresponded to the previously described prophage 6H, and appeared in 5 out of 11 isolates. CRISPR array analysis revealed two different loci with dissimilar spacer content, which only matched one sequence in the database, the temperate bacteriophage 6H. Genomic Islands (GIs) were identified in F. psychrophilum isolates 950106-1/1 and CSF 259-93, associated with toxins and antibiotic resistance. Finally, phenotypic characterization revealed a high degree of similarity among the strains with respect to biofilm formation and secretion of extracellular enzymes. Global scale dispersion of virulence factors in the genomes and the abilities for biofilm formation, hemolytic activity and secretion of extracellular enzymes among the strains suggested that F. psychrophilum isolates have a similar mode of action on adhesion, colonization and destruction of fish tissues across large spatial and temporal scales of occurrence. Overall, the genomic characterization and phenotypic properties may provide new insights to the mechanisms of pathogenicity in F. psychrophilum.

Project description:Flavobacterium psychrophilum, the etiological agent of rainbow trout fry syndrome and bacterial cold-water disease in salmonid fish, is currently one of the main bacterial pathogens hampering the productivity of salmonid farming worldwide. In this study, the genomic diversity of the F. psychrophilum species is analyzed using a set of 41 genomes, including 30 newly sequenced isolates. These were selected on the basis of available MLST data with the two-fold objective of maximizing the coverage of the species diversity and of allowing a focus on the main clonal complex (CC-ST10) infecting farmed rainbow trout (Oncorhynchus mykiss) worldwide. The results reveal a bacterial species harboring a limited genomic diversity both in terms of nucleotide diversity, with ~0.3% nucleotide divergence inside CDSs in pairwise genome comparisons, and in terms of gene repertoire, with the core genome accounting for ~80% of the genes in each genome. The pan-genome seems nevertheless "open" according to the scaling exponent of a power-law fitted on the rate of new gene discovery when genomes are added one-by-one. Recombination is a key component of the evolutionary process of the species as seen in the high level of apparent homoplasy in the core genome. Using a Hidden Markov Model to delineate recombination tracts in pairs of closely related genomes, the average recombination tract length was estimated to ~4.0 Kbp and the typical ratio of the contributions of recombination and mutations to nucleotide-level differentiation (r/m) was estimated to ~13. Within CC-ST10, evolutionary distances computed on non-recombined regions and comparisons between 22 isolates sampled up to 27 years apart suggest a most recent common ancestor in the second half of the nineteenth century in North America with subsequent diversification and transmission of this clonal complex coinciding with the worldwide expansion of rainbow trout farming. With the goal to promote the development of tools for the genetic manipulation of F. psychrophilum, a particular attention was also paid to plasmids. Their extraction and sequencing to completion revealed plasmid diversity that remained hidden to classical plasmid profiling due to size similarities.

Project description:Hydrolytic extracellular enzymes degrading host tissues potentially play a role in bacterial pathogenesis. Flavobacterium psychrophilum is an important bacterial pathogen of salmonid fish reared in freshwater throughout the world. Diversity among isolates has been described at the phenotypic, serological, and genomic levels, but the links between these various traits remain poorly understood. Using a genome-wide association study, we identified a gene encoding a novel elastinolytic enzyme in F. psychrophilum To formally demonstrate enzymatic activity, this gene (FP0506 from strain JIP 02/86) was expressed in the elastinolysis-deficient strain OSU THCO2-90, resulting in proficient elastin-degrading cells. The encoded protein is predicted to be a cell-surface-exposed lipoprotein with no homology to previously reported elastases. FP0506 might belong to the zincin tribe and gluzincin clan of metalloproteases, and this new elastase-encoding gene seems to be present only in some members of the family Flavobacteriaceae IMPORTANCE Elastin is an important proteinaceous component of vertebrate connective tissues (e.g., blood vessels, lung, and skin), to which it confers elasticity. Elastases have been identified in a number of pathogenic bacteria. They are thought to be required for tissue penetration and dissemination, acting as "spreading factors." Flavobacterium psychrophilum is a devastating bacterial pathogen of salmonid fish (salmon and trout) that is responsible for severe economic losses worldwide. This pathogen displays strong proteolytic activities. Using a variety of techniques, including genome comparisons, we identified a gene encoding a novel elastase in F. psychrophilum The encoded protein is predicted to be a cell-surface-exposed lipoprotein with no homology to previously reported elastases. In addition, this elastase likely belongs to a new family of proteases that seems to be present only in some members of this important group of bacteria.

Dataset Information

Genome analysis provides insights into the epidemiology of infection with Flavobacterium psychrophilum among farmed salmonid fish in Sweden.

Publications

Genome analysis provides insights into the epidemiology of infection with Flavobacterium psychrophilum among farmed salmonid fish in Sweden.

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