Genome-Wide Diversity and Phylogeography of Mycobacterium avium subsp. paratuberculosis in Canadian Dairy Cattle

Mycobacterium avium subsp. paratuberculosis (MAP) is the causative bacterium of Johne’s disease (JD) in ruminants. The control of JD in the dairy industry is challenging, but can be improved with a better understanding of the diversity and distribution of MAP subtypes. Previously established molecular typing techniques used to differentiate MAP have not been sufficiently discriminatory and/or reliable to accurately assess the population structure. In this study, the genetic diversity of 182 MAP isolates representing all Canadian provinces was compared to the known global diversity, using single nucleotide polymorphisms identified through whole genome sequencing. MAP isolates from Canada represented a subset of the known global diversity, as there were global isolates intermingled with Canadian isolates, as well as multiple global subtypes that were not found in Canada. One Type III and six “Bison type” isolates were found in Canada as well as one Type II subtype that represented 86% of all Canadian isolates. Rarefaction estimated larger subtype richness in Québec than in other Canadian provinces using a strict definition of MAP subtypes and lower subtype richness in the Atlantic region using a relaxed definition. Significant phylogeographic clustering was observed at the inter-provincial but not at the intra-provincial level, although most major clades were found in all provinces. The large number of shared subtypes among provinces suggests that cattle movement is a major driver of MAP transmission at the herd level, which is further supported by the lack of spatial clustering on an intra-provincial scale.

[1]  D. Kelton,et al.  Limitations of variable number of tandem repeat typing identified through whole genome sequencing of Mycobacterium avium subsp. paratuberculosis on a national and herd level , 2015, BMC Genomics.

[2]  H. Barkema,et al.  High herd-level prevalence of Mycobacterium avium subspecies paratuberculosis in Western Canadian dairy farms, based on environmental sampling. , 2014, Journal of dairy science.

[3]  J. Arsenault,et al.  Genetic Structure of Mycobacterium avium subsp. paratuberculosis Population in Cattle Herds in Quebec as Revealed by Using a Combination of Multilocus Genomic Analyses , 2014, Journal of Clinical Microbiology.

[4]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[5]  H. Barkema,et al.  Evaluation of milk ELISA for detection of Mycobacterium avium subspecies paratuberculosis in dairy herds and association with within-herd prevalence. , 2014, Journal of dairy science.

[6]  H. Barkema,et al.  Improved Short-Sequence-Repeat Genotyping of Mycobacterium avium subsp. paratuberculosis by Using Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry , 2013, Applied and Environmental Microbiology.

[7]  H. Barkema,et al.  Evaluation of environmental fecal culture for Mycobacterium avium subspecies paratuberculosis detection in dairy herds and association with apparent within-herd prevalence. , 2013, The Canadian veterinary journal = La revue veterinaire canadienne.

[8]  Christl A. Donnelly,et al.  The Contribution of Badgers to Confirmed Tuberculosis in Cattle in High-Incidence Areas in England , 2013, PLoS currents.

[9]  R. Kao,et al.  Whole Genome Sequencing Reveals Local Transmission Patterns of Mycobacterium bovis in Sympatric Cattle and Badger Populations , 2012, PLoS pathogens.

[10]  Ramón Doallo,et al.  CircadiOmics: integrating circadian genomics, transcriptomics, proteomics and metabolomics , 2012, Nature Methods.

[11]  M. Suchard,et al.  Bayesian Phylogenetics with BEAUti and the BEAST 1.7 , 2012, Molecular biology and evolution.

[12]  H. Köhler,et al.  Divergent cytokine responses of macrophages to Mycobacterium avium subsp. paratuberculosis strains of Types II and III in a standardized in vitro model. , 2011, Veterinary microbiology.

[13]  Peer Bork,et al.  Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy , 2011, Nucleic Acids Res..

[14]  Steven J. M. Jones,et al.  Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. , 2011, The New England journal of medicine.

[15]  W. Michalski,et al.  Resequencing the Mycobacterium avium subsp. paratuberculosis K10 Genome: Improved Annotation and Revised Genome Sequence , 2010, Journal of bacteriology.

[16]  M. Behr The path to Crohn's disease: is mucosal pathology a secondary event? , 2010, Inflammatory bowel diseases.

[17]  S. Gagneux,et al.  Does M. tuberculosis genomic diversity explain disease diversity? , 2010, Drug discovery today. Disease mechanisms.

[18]  M. Behr,et al.  Strain characterization of Mycobacterium avium subsp. paratuberculosis. , 2010 .

[19]  M. Behr,et al.  Paratuberculosis: organism, disease, control , 2010 .

[20]  M. Behr,et al.  Global prevalence and economics of infection with Mycobacterium avium subsp. paratuberculosis in ruminants. , 2010 .

[21]  D. Krause,et al.  Zoonotic pathogens in the food chain. , 2010 .

[22]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[23]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[24]  M. Behr,et al.  Insertion and Deletion Events That Define the Pathogen Mycobacterium avium subsp. paratuberculosis , 2008, Journal of bacteriology.

[25]  C Dubé,et al.  Comparing network analysis measures to determine potential epidemic size of highly contagious exotic diseases in fragmented monthly networks of dairy cattle movements in Ontario, Canada. , 2008, Transboundary and emerging diseases.

[26]  S. Sreevatsan,et al.  Transcriptional analysis of diverse strains Mycobacterium avium subspecies paratuberculosis in primary bovine monocyte derived macrophages. , 2008, Microbes and infection.

[27]  O. Pybus,et al.  Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. , 2008, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[28]  I. Kiss,et al.  Estimates for local and movement-based transmission of bovine tuberculosis in British cattle , 2008, Proceedings of the Royal Society B: Biological Sciences.

[29]  S. Sreevatsan,et al.  Survival of Mycobacterium avium subsp. paratuberculosis in bovine monocyte-derived macrophages is not affected by host infection status but depends on the infecting bacterial genotype. , 2007, Veterinary immunology and immunopathology.

[30]  P. Supply,et al.  New Variable-Number Tandem-Repeat Markers for Typing Mycobacterium avium subsp. paratuberculosis and M. avium Strains: Comparison with IS900 and IS1245 Restriction Fragment Length Polymorphism Typing , 2007, Journal of Clinical Microbiology.

[31]  H. Barkema,et al.  Johne's disease in Canada part II: disease impacts, risk factors, and control programs for dairy producers. , 2006, The Canadian veterinary journal = La revue veterinaire canadienne.

[32]  S. Sreevatsan,et al.  Comparative Transcriptional Analysis of Human Macrophages Exposed to Animal and Human Isolates of Mycobacterium avium Subspecies paratuberculosis with Diverse Genotypes , 2006, Infection and Immunity.

[33]  D. Bryant,et al.  A Simple and Robust Statistical Test for Detecting the Presence of Recombination , 2006, Genetics.

[34]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.

[35]  S. Sreevatsan,et al.  Cytokine responses of bovine macrophages to diverse clinical Mycobacterium avium subspecies paratuberculosis strains , 2006, BMC Microbiology.

[36]  A. Amonsin,et al.  The complete genome sequence of Mycobacterium avium subspecies paratuberculosis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Paul Keim,et al.  Anthrax molecular epidemiology and forensics: using the appropriate marker for different evolutionary scales. , 2004, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[38]  A. Amonsin,et al.  Multilocus Short Sequence Repeat Sequencing Approach for Differentiating among Mycobacterium avium subsp. paratuberculosis Strains , 2004, Journal of Clinical Microbiology.

[39]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[40]  Martin Vingron,et al.  TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing , 2002, Bioinform..

[41]  R. Whitlock,et al.  Typing of IS 1311 polymorphisms confirms that bison (Bison bison) with paratuberculosis in Montana are infected with a strain of Mycobacterium avium subsp. paratuberculosis distinct from that occurring in cattle and other domesticated livestock. , 2001, Molecular and cellular probes.

[42]  K. Strimmer,et al.  Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[43]  D. Gabrić,et al.  Identification of two groups of Mycobacterium paratuberculosis strains by restriction endonuclease analysis and DNA hybridization , 1990, Journal of clinical microbiology.

[44]  J. McFadden,et al.  Use of highly specific DNA probes and the polymerase chain reaction to detect Mycobacterium paratuberculosis in Johne's disease , 1990, Journal of clinical microbiology.