Microevolution of Renibacterium salmoninarum: evidence for intercontinental dissemination associated with fish movements

Abstract

Renibacterium salmoninarum is the causative agent of bacterial kidney disease, a major pathogen of salmonid fish species worldwide. Very low levels of intra-species genetic diversity have hampered efforts to understand the transmission dynamics and recent evolutionary history of this Gram-positive bacterium. We exploited recent advances in the next-generation sequencing technology to generate genome-wide single-nucleotide polymorphism (SNP) data from 68 diverse R. salmoninarum isolates representing broad geographical and temporal ranges and different host species. Phylogenetic analysis robustly delineated two lineages (lineage 1 and lineage 2); futhermore, dating analysis estimated that the time to the most recent ancestor of all the isolates is 1239 years ago (95% credible interval (CI) 444–2720 years ago). Our data reveal the intercontinental spread of lineage 1 over the last century, concurrent with anthropogenic movement of live fish, feed and ova for aquaculture purposes and stocking of recreational fisheries, whilst lineage 2 appears to have been endemic in wild Eastern Atlantic salmonid stocks before commercial activity. The high resolution of the SNP-based analyses allowed us to separate closely related isolates linked to neighboring fish farms, indicating that they formed part of single outbreaks. We were able to demonstrate that the main lineage 1 subgroup of R. salmoninarum isolated from Norway and the UK likely represent an introduction to these areas ∼40 years ago. This study demonstrates the promise of this technology for analysis of micro and medium scale evolutionary relationships in veterinary and environmental microorganisms, as well as human pathogens.

Multilocus Sequence Analysis of the Marine Bacterial Genus Tenacibaculum Suggests Parallel Evolution of Fish Pathogenicity and Endemic Colonization of Aquaculture Systems

“…This situation is in sharp contrast to that in F. psychrophilum (59,62,63), R. salmoninarium (61), and Y. ruckeri (60), for which the sequence data unambiguously revealed transcontinental dissemination linked to the international trade of broodfish and eggs. Furthermore, as a result of preferential dissemination routes or of adaptive niche specificity, the large clonal complexes detected in F. psychrophilum tended to be strongly associated with particular host fish species (59,62,64).…”

“…In terms of per-nucleotide r/m ratio, the rate of recombination in T. maritimum may be slightly lower than that in Y. ruckeri (ϳ7:1) and is clearly lower than that in the highly recombinogenic bacterium F. psychrophilum (ϳ26:1) (see references 58 and 59 for even higher estimates). In contrast, a near absence of recombination was reported for R. salmoninarum (61).…”

Addressing viral and bacterial threats to salmon farming in Chile: historical contexts and perspectives for management and control

“…Recently, Wiens and other researchers from the United Kingdom, the United States and Norway, where R. salmoninarum is also a problem, sequenced 68 R. salmoninarum isolates from broad geographical and temperature ranges, and different host species were drafted for single nucleotide polymorphisms (Brynildsrud et al . ). One interesting finding from this collaborative project was that there were two major lineages of R. salmoninarum that split allopatrically approximately 944 years ago.…”

Effects of temperature on Renibacterium salmoninarum infection and transmission potential in Chinook salmon, Oncorhynchus tshawytscha (Walbaum)

“…Renibacterium salmoninarum is a globally significant pathogen of salmonid fishes and the causative agent of bacterial kidney disease (BKD; Brynildsrud et al 2014). Renibacterium salmoninarum infects a number of fish host species, and chronic BKD is associated with granulomatous lesions in internal organs such as the kidney (Bruno 1986).…”