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Whooping cough (pertussis) is a highly contagious respiratory disease caused by the bacterium  Bordetella pertussis.  Despite high vaccine coverage, pertussis has re-emerged in many countries including Australia and caused two large epidemics in Australia since 2007. Here, we undertook a genomic and phylogeographic study of 385 Australian  B. pertussis  isolates collected from 2008 to 2017. The Australian  B. pertussis  population was found to be composed of mostly  ptxP3  strains carrying different  fim3  alleles, with  ptxP3-fim3A  genotype expanding far more than  ptxP3-fim3B.  Within the former, there were six co-circulating epidemic lineages (EL1 to EL6). The multiple ELs emerged, expanded, and then declined at different time points over the two epidemics. In population genetics terms, both hard and soft selective sweeps through vaccine selection pressures have determined the population dynamics of Australian  B. pertussis.  Relative risk estimation suggests that once a new  B. pertussis  lineage emerged, it was more likely to spread locally within the first 1.5 years. However, after 1.5 years, any new lineage was likely to expand to a wider region. Phylogenetic analysis revealed the expansion of  ptxP3  strains was also associated with replacement of the type III secretion system allele  bscI1  with  bscI3 .  bscI3  is associated with decreased T3SS secretion and may allow  B. pertussis  to reduce immune recognition. This study advanced our understanding of the epidemic population structure and spatial and temporal dynamics of  B. pertussis  in a highly immunized population.

Genomic dissection of the microevolution of Australian epidemic Bordetella pertussis