Independent Emergence of Yersinia ruckeri Biotype 2 in the United States and Europe

Abstract

Biotype 2 (BT2) variants of the bacterium Yersinia ruckeri are an increasing disease problem in U.S. and European aquaculture and have been characterized as serovar 1 isolates that lack both peritrichous flagella and secreted phospholipase activity. The emergence of this biotype has been associated with an increased frequency of enteric redmouth disease (ERM) outbreaks in previously vaccinated salmonid fish. In this study, four independent specific natural mutations that cause the loss of both motility and secreted lipase activity were identified in BT2 strains from the United States, United Kingdom, and mainland Europe. Each of these was a unique mutation in either fliR, flhA, or flhB, all of which are genes predicted to encode essential components of the flagellar secretion apparatus. Our results demonstrate the existence of independent mutations leading to the BT2 phenotype; thus, this phenotype has emerged separately at least four times. In addition, BT2 strains from the United Kingdom were shown to have the same mutant allele found in U.S. BT2 strains, suggesting a common origin of this BT2 lineage. This differentiation of distinct BT2 lineages is of critical importance for the development and validation of alternative vaccines or other treatment strategies intended for the control of BT2 strains.

Yersinia ruckeri Isolates Recovered from Diseased Atlantic Salmon (Salmo salar) in Scotland Are More Diverse than Those from Rainbow Trout (Oncorhynchus mykiss) and Represent Distinct Subpopulations

“…However, it is also notable that Y. ruckeri strains isolated from Atlantic salmon in Australia and Chile are also members of biotype 1 and not biotype 2 (7,9). It has been postulated that vaccination may be providing the selective pressure that is driving the loss of flagellar motility in Y. ruckeri (20,42). If this is the case, it is surprising that biotype 2 has emerged in rainbow trout but not in Atlantic salmon because Atlantic salmon are generally vaccinated with the same serotype O1-based vaccines as those used for rainbow trout (9).…”

“…A second explanation to account for the presence of distinct subpopulations of Y. ruckeri in Atlantic salmon and rainbow trout is that different strains are specifically adapted to one host species or the other. It has long been recognized that serotype O1 isolates of Y. ruckeri have far greater prevalence in, and are more pathogenic toward, rainbow trout than are other serotypes; as pointed out above, it has been proposed that the epidemic expansion and dissemination of serotype O1 Y. ruckeri occurred when the pathogen found an alternative niche in intensively cultured rainbow trout (42). Conversely, non-O1 serotypes are usually associated with nonsalmonid species or with the environment, leading to the suggestion that different Y. ruckeri isolates exhibit various degrees of host specificity and virulence or adaptation for survival in the environment (16,31,63).…”

“…This observation suggests that the biotype 2 phenotype has not yet emerged in Scottish Atlantic salmon isolates as it has in European and North American rainbow trout isolates (16,17,(22)(23)(24)(25)(26)(27); however, it should be noted that the biotype 2 phenotype was previously described in a small number of older Atlantic salmon isolates originating from Norway (18) and the United Kingdom (24). The biotype 2 phenotype has arisen independently on at least four occasions within serotype O1 rainbow trout isolates in Europe and the United States by specific mutations in the genes (fliR, flhA, and flhB) involved in flagellar secretion; its distribution in Europe is not due simply to the expansion and distribution of a single clone (24,42). Possible explanations for the loss of flagellar motility in Y. ruckeri isolates from rainbow trout have been discussed by Welch et al (42), but it is intriguing that, in the present study, the biotype 2 phenotype was not identified in a single Atlantic salmon isolate.…”

“…The biotype 2 phenotype has arisen independently on at least four occasions within serotype O1 rainbow trout isolates in Europe and the United States by specific mutations in the genes (fliR, flhA, and flhB) involved in flagellar secretion; its distribution in Europe is not due simply to the expansion and distribution of a single clone (24,42). Possible explanations for the loss of flagellar motility in Y. ruckeri isolates from rainbow trout have been discussed by Welch et al (42), but it is intriguing that, in the present study, the biotype 2 phenotype was not identified in a single Atlantic salmon isolate. The complete absence of biotype 2, serotype O1 isolates in Atlantic salmon over the 14-year period is striking because these strains continue to be the predominant cause of disease in rainbow trout in Scotland since they were first identified in the 1980s (22).…”

“…Historically, the majority of disease in rainbow trout in Europe and North America has been caused by serotype O1 strains of biotype 1 (the Hagerman strain) or, more recently, by biotype 2 variants (42). The association of a limited number of clones with a large proportion of disease in rainbow trout fits with the epidemic population structure model proposed for Y. ruckeri (34,57) and is consistent with the belief that Y. ruckeri is a recently emerged pathogen that was originally geographically isolated but quickly became widely disseminated (3,42). These strains presumably represent hypervirulent clones (58) that have adapted to a new niche (intensively cultured rainbow trout) (42) and consequently "exploded" in number and become widely distributed by extensive fish movements (34,57).…”