Antimicrobial resistance and genomic characterization of Salmonella enterica isolates from chicken meat

Khaloud O Alzahrani; Fahad M Al-Reshoodi; Elaf A Alshdokhi; Ashwaq S Alhamed; Meshari A Al Hadlaq; Mohammed I Mujallad; Lenah E Mukhtar; Amani T Alsufyani; Abdullah A Alajlan; Malfi S Al Rashidy; Mashan J Al Dawsari; Saleh I Al-Akeel; Meshari H Al-Harthi; Abdulaziz M Al Manee; Majed F Alghoribi; Suliman M Alajel

doi:10.3389/fmicb.2023.1104164

Antimicrobial resistance and genomic characterization of Salmonella enterica isolates from chicken meat

Front Microbiol. 2023 Mar 30:14:1104164. doi: 10.3389/fmicb.2023.1104164. eCollection 2023.

Authors

Khaloud O Alzahrani¹, Fahad M Al-Reshoodi², Elaf A Alshdokhi¹, Ashwaq S Alhamed¹, Meshari A Al Hadlaq¹, Mohammed I Mujallad¹, Lenah E Mukhtar², Amani T Alsufyani², Abdullah A Alajlan³, Malfi S Al Rashidy³, Mashan J Al Dawsari³, Saleh I Al-Akeel³, Meshari H Al-Harthi⁴, Abdulaziz M Al Manee^{5

6}, Majed F Alghoribi^{7

8}, Suliman M Alajel⁹

Affiliations

¹ Molecular Biology Division, Reference Laboratory for Microbiology, Executive Department of Reference Laboratories, Research and Laboratories Sector, Saudi Food and Drug Authority (SFDA), Riyadh, Saudi Arabia.
² Antimicrobial Resistance Division, Reference Laboratory for Microbiology, Executive Department of Reference Laboratories, Research and Laboratories Sector, Saudi Food and Drug Authority (SFDA), Riyadh, Saudi Arabia.
³ Microbial Identification Division, Reference Laboratory for Microbiology, Executive Department of Reference Laboratories, Research and Laboratories Sector, Saudi Food and Drug Authority (SFDA), Riyadh, Saudi Arabia.
⁴ Microbiology Section, Food Laboratory, Laboratories Executive Department, Saudi Food and Drug Authority (SFDA), Riyadh, Saudi Arabia.
⁵ Microbial Hazards Division, Risk Assessment Department, Executive Department of Monitoring and Risk Assessment, Saudi Food and Drug Authority (SFDA), Riyadh, Saudi Arabia.
⁶ Biology Department, Faculty of Sciences, King Abdulaziz University, Jeddah, Saudi Arabia.
⁷ Infectious Diseases Research Department, King Abdullah International Medical Research Center (KAIMRC), Riyadh, Saudi Arabia.
⁸ Department of Basic Science, College of Science and Health Professions, King Saud Bin Abdulaziz University for Health Sciences (KSAU), Riyadh, Saudi Arabia.
⁹ Reference Laboratory for Microbiology, Executive Department of Reference Laboratories, Research and Laboratories Sector, Saudi Food and Drug Authority (SFDA), Riyadh, Saudi Arabia.

Abstract

This study investigated genotypic and phenotypic antimicrobial resistance profiles, phylogenic relatedness, plasmid and virulence composition of 39 Salmonella enterica strains isolated from chicken meat samples using whole genome sequencing (WGS) technology. Four distinct serotypes were identified; Salmonella Minnesota (16/39, 41%), Salmonella Infantis (13/39, 33.3%), Salmonella Enteritidis (9/39, 23.1%), and one isolate was detected for Salmonella Kentucky (1/39, 2.6%), with sequence types (STs) as followed: ST548, ST32, ST11, and ST198, respectively. Phenotypic resistance to tetracycline (91.2%), ampicillin (82.4%), sulfisoxazole (64.7%), and nalidixic acid (61.6%) was the most observed. Resistome analysis revealed the presence of resistance genes to aminoglycosides, β-lactamase, sulfonamides, trimethoprim, phenicol, lincosamide, macrolides, and tetracyclines. Plasmidome showed the presence of eight incompatibility groups, including IncA/C2, IncFIB(K)_1_Kpn3, Col440I_1, IncR, IncX1, IncI1_1_Alpha, IncFIB(S)/IncFII(S), IncHI2/IncHI2A, IncX2 and ColpVC plasmids across the 39 genomes. Three resistance genes, sul2, tetA and bla_CMY-2, were predicted to be located on IncA/C2 plasmid in S. Minnesota isolates, whereas all S. Infantis isolates were positive to IncFIB(K)_1_Kpn3 plasmid that carries bla _CTX-M-65 gene. Eleven Salmonella pathogenicity islands and up to 131 stress and/or virulence genes were identified in the evaluated genomes. Phylogenetic analysis showed four phylogroups that were consistent with the identified ST profiles with a high level of inter-diversity between isolates. This is the first genomic characterization of Salmonella isolates from retail chicken meat in Saudi Arabia using WGS technology. The availability of Salmonella genomes from multiple geographic locations, including Saudi Arabia, would be highly beneficial in future source-tracking, especially during epidemiological surveillance and outbreak investigations.

Keywords: Salmonella; antimicrobial resistant genes (ARG); molecular epidemiology; molecular typing; phylogenetic analysis; virulence factors; whole genome sequencing.