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Title: Novel, host-restricted genotypes of Bordetella bronchiseptica associated with phocine respiratory tract isolates

Author
item Register, Karen
item IVANOV, YURI - Pennsylvania State University
item HARVILL, ERIC - Pennsylvania State University
item DAVISON, NICK - Sruc-Scotland'S Rural College
item GEOFFRY, FOSTER - Sruc-Scotland'S Rural College

Submitted to: Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/9/2015
Publication Date: 3/1/2015
Publication URL: http://handle.nal.usda.gov/10113/61362
Citation: Register, K.B., Ivanov, Y., Harvill, E., Davison, N., Geoffry, F. 2015. Novel, host-restricted genotypes of Bordetella bronchiseptica associated with phocine respiratory tract isolates. Microbiology. 161(3):580-592. DOI: 10.1099/mic.0.000035.

Interpretive Summary: Bordetella bronchiseptica is a widespread respiratory pathogen in a variety of wild and domesticated animals. During a succession of phocine morbillivirus outbreaks occurring over the past 25 years, it was identified as a frequent secondary invader, often believed to be the cause of death. Prior analysis of isolates from seals in the North Sea acquired during the 1988 phocine distemper epidemic suggests a single, unique clone of the bacterium was circulating among affected seals. The goal of this study was to more fully evaluate the genetic diversity among seal isolates of B. bronchiseptica representing multiple outbreaks over the past 25 years in both the North Sea and Caspian Sea. We used two different molecular typing methods that target genes encoding basic metabolic functions, multilocus sequence typing (MLST) and Pvu II ribotyping, to evaluate 55 isolates from the North Sea, collected between 1998 and 2009. All isolates have the same genotype that has not otherwise been found in any other host species. A single, novel genotype, unique from that of the North Sea isolates, was also found in four isolates from a 2000 outbreak in the Caspian Sea. Further analysis suggested that the two distinct genotypes found in seals are only distantly related and are likely to have evolved independently of one another. In contrast, virulence genes from the seal isolates are more similar to one another than to virulence genes from strains to which they are more closely related that were acquired from different hosts. This suggests a possible host-specific fine-tuning of virulence genes in B. bronchiseptica that facilitates optimal function of the proteins they encode. These data indicate disease-causing seal isolates of B. bronchiseptica comprise unique, host-adapted and highly clonal populations.

Technical Abstract: Bordetella bronchiseptica is a widespread respiratory pathogen in a variety of wild and domesticated animals. During a succession of phocine morbillivirus outbreaks occurring over the past 25 years, it was identified as a frequent secondary invader, often believed to be the cause of death. Prior analysis of isolates from seals in the North Sea acquired during the 1988 phocine distemper epidemic suggests a single, unique clone of the bacterium was circulating among affected seals. The goal of this study was to more fully evaluate the genetic diversity among seal isolates of B. bronchiseptica representing multiple outbreaks over the past 25 years in both the North Sea and Caspian Sea. Multilocus sequence typing (MLST) and Pvu II ribotyping of 55 isolates from the North Sea, collected between 1998 and 2009, revealed a single genotype not found in any other host species. A single, novel genotype, unique from that of the North Sea isolates, was found in four isolates from a 2000 outbreak in the Caspian Sea. Phylogenetic analysis of all B. bronchiseptica isolates for which information is available, based either on MLST sequence, ribotype patterns or genome-wide single-nucleotide polymorphisms (SNPs), consistently placed both seal-specific genotypes within the same major clade but also indicates a distinct evolutionary history for each. To investigate the possible basis for host specificity, DNA and predicted protein sequences of virulence genes that mediate host interactions were used in comparisons between a North Sea isolate, a Caspian Sea isolate and each of their closest relatives as inferred from genome-wide SNP analysis. Despite their phylogenetic divergence, fewer nucleotide and amino acid substitutions were found in comparisons of the two seal isolates than in comparisons with closely related strains. These data indicate disease-causing seal isolates of B. bronchiseptica comprise unique, host-adapted and highly clonal populations.