Prevalence and characterization of Staphylococcus aureus and Staphylococcus argenteus isolated from rice and flour products in Guangdong, China

Dongli Rong; Zhenjie Liu; Jiahui Huang; Feng Zhang; Qingping Wu; Jingsha Dai; Yuanyu Li; Miao Zhao; Qi Li; Jumei Zhang; Shi Wu

doi:10.1016/j.ijfoodmicro.2023.110348

Prevalence and characterization of Staphylococcus aureus and Staphylococcus argenteus isolated from rice and flour products in Guangdong, China

Int J Food Microbiol. 2023 Dec 2:406:110348. doi: 10.1016/j.ijfoodmicro.2023.110348. Epub 2023 Aug 6.

Authors

Dongli Rong¹, Zhenjie Liu¹, Jiahui Huang¹, Feng Zhang¹, Qingping Wu¹, Jingsha Dai¹, Yuanyu Li¹, Miao Zhao¹, Qi Li¹, Jumei Zhang¹, Shi Wu²

Affiliations

¹ Guangdong Provincial Key Laboratory of Microbial Safety and Health, State Key Laboratory of Applied Microbiology Southern China, Key Laboratory of Agricultural Microbiomics and Precision Application, Ministry of Agriculture and Rural Affairs, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou 510070, PR China.
² Guangdong Provincial Key Laboratory of Microbial Safety and Health, State Key Laboratory of Applied Microbiology Southern China, Key Laboratory of Agricultural Microbiomics and Precision Application, Ministry of Agriculture and Rural Affairs, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou 510070, PR China. Electronic address: wushiloveyou@126.com.

PMID: 37573713
DOI: 10.1016/j.ijfoodmicro.2023.110348

Abstract

Staphylococcus aureus and Staphylococcus argenteus have been implicated in food poisoning outbreaks, and have been found in various types of food products according to our previous study. Rice and flour products are popular and widely consumed around the world. However, limited data are available on the microbial safety of S. aureus in rice and flour products, and S. argenteus has never been reported. Thus, this study aimed to investigate the contamination of S. aureus and S. argenteus in 250 fresh rice and flour product samples from five cities in Guangdong, China. According to qualitative and quantitative analyses, 68 (27.2 %) and 11 (4.4 %) samples were positive for S. aureus and S. argenteus, including 9 samples that exceeded 100 MPN/g. For antibiotics susceptibility tests in 16 antibiotics, the S. aureus isolates exhibited higher rates of resistance and multidrug resistance than S. argenteus. The S. aureus and S. argenteus isolates were mainly resistant to penicillin (70.21 %; 79.17 %), tetracycline (20.21 %; 58.33 %) and azithromycin (19.68 %, 8.33 %). However, the other antibiotic resistance rates were <10 %. Furthermore, the genetic background of the isolates was analyzed by whole-genome sequencing (WGS). As a result, the S. aureus isolates were divided into 18 known sequence types (STs) and 4 novel STs (ST7675, ST7679, ST7680 and ST7682), which mainly belonged to ST188 (20.6 %) and ST6 (14.7 %). The S. argenteus isolates mainly belonged to ST2250 (90.9 %), with a novel type (ST7683). In total, 36 and 16 antibiotic resistance genes (ARGs) were found in S. aureus and S. argenteus isolates, respectively. In addition, 91 virulence genes (VFs) were detected in S. aureus isolates as well as 90 % of core VFs were similar to S. argenteus. More than 20 % of the S. aureus isolates carried the classic enterotoxin gene (sea-sec), but chp, cna and map were free in all S. argenteus isolates. Importantly, 33.8 % of S. aureus isolates belonged to the immune evasion cluster (IEC) type B, whereas most of S. argenteus isolates (90.9 %) belong to IEC type E. According to the phylogenetic analysis, the S. aureus and S. argenteus isolates in fresh rice and flour products may indicate loss or acquisition of ARGs and VFs to survive and adapt to the environment. Our study confirmed the presence of S. argenteus in rice and flour products at first and focused on the multi-dimensional systematic comparative analysis of S. aureus and S. argenteus to reveal their ubiquity and similarities or differences, and provide more accurate and effective basic information for follow-up monitoring and tracking.

Keywords: Characterization; Rice and flour product; S. argenteus; S. aureus; WGS.