Host Adaptation of Pigeon Isolates of Salmonella enterica subsp. enterica Serovar Typhimurium Variant Copenhagen Phage Type 99 Is Associated with Enhanced Macrophage Cytotoxicity

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Abstract
Phage type 99 of Salmonella enterica subsp. enterica serovar Typhimurium variant Copenhagen strains isolated from pigeons were examined for the presence of genotypic and phenotypic characteristics. The pulsed-field gel electrophoresis patterns obtained with Xba I and Bln I from 38 pigeon strains were compared with those obtained from 89 porcine, poultry, and human strains of variant Copenhagen. Identical patterns with Xba I and four closely related patterns with Bln I were obtained with the pigeon strains, whereas 16 Xba I patterns were found with the other strains. The Xba I patterns of the pigeon strains showed a low genetic similarity to the patterns of the porcine, poultry, and human strains and invariably showed a low-molecular-weight band that was absent in the majority of the other strains. The virulence genes shdA , spvR , pefA , sopE , and spvB were uniformly present in six pigeon isolates representing the genetic diversity found with Bln I. These six pigeon-derived strains were highly cytotoxic for pigeon macrophages compared to three porcine strains. After experimental infection of pigeons with a pigeon strain, clinical symptoms, fecal shedding, and colonization of internal organs were more pronounced than those after infection with a porcine strain. These data suggest that the phage type 99 strains used in this study are highly adapted to pigeons and should be classified as a host-restricted lineage of the serovar Typhimurium.