A multidrug-resistant Salmonella enterica Typhimurium DT104 complex lineage circulating among humans and cattle in the USA lost the ability to produce pertussis-like toxin ArtAB

Carroll, Laura M.; Piacenza, Nicolo; Cheng, Rachel A.; Wiedmann, Martin; Guldimann, Claudia (2023): A multidrug-resistant Salmonella enterica Typhimurium DT104 complex lineage circulating among humans and cattle in the USA lost the ability to produce pertussis-like toxin ArtAB. Microbial Genomics, 9 (7). ISSN 2057-5858

Abstract

A multidrug-resistant Salmonella enterica Typhimurium DT104 complex lineage circulating among humans and cattle in the USA lost the ability to produce pertussis-like toxin ArtAB Laura M. Carroll Umeå Centre for Microbial Research, Umeå University, Umeå, Sweden Laboratory for Molecular Infection Medicine Sweden (MIMS), Umeå University, Umeå, Sweden Department of Clinical Microbiology, SciLifeLab, Umeå University, Umeå, Sweden Integrated Science Lab, Umeå University, Umeå, Sweden https://orcid.org/0000-0002-3677-0192 Nicolo Piacenza Chair for Food Safety and Analytics, Ludwig-Maximillians-University Munich, Munich, Germany Rachel A. Cheng Department of Food Science and Technology, Virginia Tech, Blacksburg, VA, USA Martin Wiedmann Department of Food Science, Cornell University, Ithaca, NY, USA Claudia Guldimann Chair for Food Safety and Analytics, Ludwig-Maximillians-University Munich, Munich, Germany https://orcid.org/0000-0002-9895-750X

Salmonella enterica subsp. enterica serotype Typhimurium definitive type 104 (DT104) can infect both humans and animals and is often multidrug-resistant (MDR). Previous studies have indicated that, unlike most S . Typhimurium, the overwhelming majority of DT104 strains produce pertussis-like toxin ArtAB via prophage-encoded genes artAB . However, DT104 that lack artAB have been described on occasion. Here, we identify an MDR DT104 complex lineage circulating among humans and cattle in the USA, which lacks artAB (i.e. the ‘U.S. artAB -negative major clade’; n =42 genomes). Unlike most other bovine- and human-associated DT104 complex strains from the USA ( n =230 total genomes), which harbour artAB on prophage Gifsy-1 ( n =177), members of the U.S. artAB -negative major clade lack Gifsy-1, as well as anti-inflammatory effector gogB . The U.S. artAB -negative major clade encompasses human- and cattle-associated strains isolated from ≥11 USA states over a 20-year period. The clade was predicted to have lost artAB , Gifsy-1 and gogB circa 1985–1987 (95 % highest posterior density interval 1979.0–1992.1). When compared to DT104 genomes from other regions of the world ( n =752 total genomes), several additional, sporadic artAB , Gifsy-1 and/or gogB loss events among clades encompassing five or fewer genomes were observed. Using phenotypic assays that simulate conditions encountered during human and/or bovine digestion, members of the U.S. artAB -negative major clade did not differ from closely related Gifsy-1/ artAB / gogB -harbouring U.S. DT104 complex strains (ANOVA raw P >0.05); thus, future research is needed to elucidate the roles that artAB , gogB and Gifsy-1 play in DT104 virulence in humans and animals.
Salmonella enterica subsp. enterica serotype Typhimurium definitive type 104 (DT104) can infect both humans and animals and is often multidrug-resistant (MDR). Previous studies have indicated that, unlike most S. Typhimurium, the overwhelming majority of DT104 strains produce pertussis-like toxin ArtAB via prophage-encoded genes artAB. However, DT104 that lack artAB have been described on occasion. Here, we identify an MDR DT104 complex lineage circulating among humans and cattle in the USA, which lacks artAB (i.e. the ‘U.S. artAB-negative major clade’; n=42 genomes). Unlike most other bovine- and human-associated DT104 complex strains from the USA (n=230 total genomes), which harbour artAB on prophage Gifsy-1 (n=177), members of the U.S. artAB-negative major clade lack Gifsy-1, as well as anti-inflammatory effector gogB. The U.S. artAB-negative major clade encompasses human- and cattle-associated strains isolated from ≥11 USA states over a 20-year period. The clade was predicted to have lost artAB, Gifsy-1 and gogB circa 1985–1987 (95 % highest posterior density interval 1979.0–1992.1). When compared to DT104 genomes from other regions of the world (n=752 total genomes), several additional, sporadic artAB, Gifsy-1 and/or gogB loss events among clades encompassing five or fewer genomes were observed. Using phenotypic assays that simulate conditions encountered during human and/or bovine digestion, members of the U.S. artAB-negative major clade did not differ from closely related Gifsy-1/artAB/gogB-harbouring U.S. DT104 complex strains (ANOVA raw P>0.05); thus, future research is needed to elucidate the roles that artAB, gogB and Gifsy-1 play in DT104 virulence in humans and animals.

• Dokumententyp: Artikel (LMU)
• Organisationseinheit (Fakultäten): 08 Tiermedizin
• DFG-Fachsystematik der Wissenschaftsbereiche: Lebenswissenschaften
• DFG: Gefördert durch die Deutsche Forschungsgemeinschaft (DFG) - 491502892