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

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...

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Veröffentlicht in:International journal of food microbiology 2023-12, Vol.406, p.110348-110348, Article 110348
Hauptverfasser: Rong, Dongli, Liu, Zhenjie, Huang, Jiahui, Zhang, Feng, Wu, Qingping, Dai, Jingsha, Li, Yuanyu, Zhao, Miao, Li, Qi, Zhang, Jumei, Wu, Shi
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container_title International journal of food microbiology
container_volume 406
creator Rong, Dongli
Liu, Zhenjie
Huang, Jiahui
Zhang, Feng
Wu, Qingping
Dai, Jingsha
Li, Yuanyu
Zhao, Miao
Li, Qi
Zhang, Jumei
Wu, Shi
description 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
doi_str_mv 10.1016/j.ijfoodmicro.2023.110348
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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 &lt;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. •The Staphylococcus argenteus was first found in rice and flour products, which are very popular on Chinese dinner tables.•Polysaccharide capsule (PC) mutation, especially Cap8H-K deletion, is more common in ST398 and its evolved ST types.•S. aureus isolates were mainly belonged to the immune evasion cluster (IEC) type B, S. argenteus mainly belonged to type E.•Comparing S. aureus and S. argenteus from the same source enhances understanding of their similarities and differences.</description><identifier>ISSN: 0168-1605</identifier><identifier>EISSN: 1879-3460</identifier><identifier>DOI: 10.1016/j.ijfoodmicro.2023.110348</identifier><identifier>PMID: 37573713</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Characterization ; Rice and flour product ; S. argenteus ; S. aureus ; WGS</subject><ispartof>International journal of food microbiology, 2023-12, Vol.406, p.110348-110348, Article 110348</ispartof><rights>2023 Elsevier B.V.</rights><rights>Copyright © 2023 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c377t-f3ebe37f842dac7161d1686479562a08a77b3ee23ac63fb5c5e300ec0a50e683</citedby><cites>FETCH-LOGICAL-c377t-f3ebe37f842dac7161d1686479562a08a77b3ee23ac63fb5c5e300ec0a50e683</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ijfoodmicro.2023.110348$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>315,781,785,3551,27929,27930,46000</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37573713$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rong, Dongli</creatorcontrib><creatorcontrib>Liu, Zhenjie</creatorcontrib><creatorcontrib>Huang, Jiahui</creatorcontrib><creatorcontrib>Zhang, Feng</creatorcontrib><creatorcontrib>Wu, Qingping</creatorcontrib><creatorcontrib>Dai, Jingsha</creatorcontrib><creatorcontrib>Li, Yuanyu</creatorcontrib><creatorcontrib>Zhao, Miao</creatorcontrib><creatorcontrib>Li, Qi</creatorcontrib><creatorcontrib>Zhang, Jumei</creatorcontrib><creatorcontrib>Wu, Shi</creatorcontrib><title>Prevalence and characterization of Staphylococcus aureus and Staphylococcus argenteus isolated from rice and flour products in Guangdong, China</title><title>International journal of food microbiology</title><addtitle>Int J Food Microbiol</addtitle><description>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 &lt;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. •The Staphylococcus argenteus was first found in rice and flour products, which are very popular on Chinese dinner tables.•Polysaccharide capsule (PC) mutation, especially Cap8H-K deletion, is more common in ST398 and its evolved ST types.•S. aureus isolates were mainly belonged to the immune evasion cluster (IEC) type B, S. argenteus mainly belonged to type E.•Comparing S. aureus and S. argenteus from the same source enhances understanding of their similarities and differences.</description><subject>Characterization</subject><subject>Rice and flour product</subject><subject>S. argenteus</subject><subject>S. aureus</subject><subject>WGS</subject><issn>0168-1605</issn><issn>1879-3460</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNqNkc2O0zAQgC0EYsvCKyBz40CKHcdxekTVsiCtBBJ7t6b2uHWV2MV2VlpeglfGUQtCnDjNYb75_Qh5w9maM96_P6790cVoJ29SXLesFWvOmeiGJ2TFB7VpRNezp2RV2aHhPZNX5EXOR8aYFII9J1dCSSUUFyvy82vCBxgxGKQQLDUHSGAKJv8Dio-BRke_FTgdHsdoojFzpjAnXEKl_82kPYayJH2OIxS01KU40eQv3d0Y50RPKdrZlEoFejtD2NsY9u_o9uADvCTPHIwZX13iNbn_eHO__dTcfbn9vP1w1xihVGmcwB0K5YautWAU77mtt_ad2si-BTaAUjuB2AowvXA7aSQKxtAwkAz7QVyTt-e2dZfvM-aiJ58NjiMEjHPW7SCZ4nLTsYpuzmj9dc4JnT4lP0F61JzpRYc-6r906EWHPuuota8vY-bdhPZP5e__V2B7BrDe-uAx6Wz8IsP6hKZoG_1_jPkFxHalUg</recordid><startdate>20231202</startdate><enddate>20231202</enddate><creator>Rong, Dongli</creator><creator>Liu, Zhenjie</creator><creator>Huang, Jiahui</creator><creator>Zhang, Feng</creator><creator>Wu, Qingping</creator><creator>Dai, Jingsha</creator><creator>Li, Yuanyu</creator><creator>Zhao, Miao</creator><creator>Li, Qi</creator><creator>Zhang, Jumei</creator><creator>Wu, Shi</creator><general>Elsevier B.V</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20231202</creationdate><title>Prevalence and characterization of Staphylococcus aureus and Staphylococcus argenteus isolated from rice and flour products in Guangdong, China</title><author>Rong, Dongli ; Liu, Zhenjie ; Huang, Jiahui ; Zhang, Feng ; Wu, Qingping ; Dai, Jingsha ; Li, Yuanyu ; Zhao, Miao ; Li, Qi ; Zhang, Jumei ; Wu, Shi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c377t-f3ebe37f842dac7161d1686479562a08a77b3ee23ac63fb5c5e300ec0a50e683</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Characterization</topic><topic>Rice and flour product</topic><topic>S. argenteus</topic><topic>S. aureus</topic><topic>WGS</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rong, Dongli</creatorcontrib><creatorcontrib>Liu, Zhenjie</creatorcontrib><creatorcontrib>Huang, Jiahui</creatorcontrib><creatorcontrib>Zhang, Feng</creatorcontrib><creatorcontrib>Wu, Qingping</creatorcontrib><creatorcontrib>Dai, Jingsha</creatorcontrib><creatorcontrib>Li, Yuanyu</creatorcontrib><creatorcontrib>Zhao, Miao</creatorcontrib><creatorcontrib>Li, Qi</creatorcontrib><creatorcontrib>Zhang, Jumei</creatorcontrib><creatorcontrib>Wu, Shi</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>International journal of food microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rong, Dongli</au><au>Liu, Zhenjie</au><au>Huang, Jiahui</au><au>Zhang, Feng</au><au>Wu, Qingping</au><au>Dai, Jingsha</au><au>Li, Yuanyu</au><au>Zhao, Miao</au><au>Li, Qi</au><au>Zhang, Jumei</au><au>Wu, Shi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prevalence and characterization of Staphylococcus aureus and Staphylococcus argenteus isolated from rice and flour products in Guangdong, China</atitle><jtitle>International journal of food microbiology</jtitle><addtitle>Int J Food Microbiol</addtitle><date>2023-12-02</date><risdate>2023</risdate><volume>406</volume><spage>110348</spage><epage>110348</epage><pages>110348-110348</pages><artnum>110348</artnum><issn>0168-1605</issn><eissn>1879-3460</eissn><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 &lt;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. •The Staphylococcus argenteus was first found in rice and flour products, which are very popular on Chinese dinner tables.•Polysaccharide capsule (PC) mutation, especially Cap8H-K deletion, is more common in ST398 and its evolved ST types.•S. aureus isolates were mainly belonged to the immune evasion cluster (IEC) type B, S. argenteus mainly belonged to type E.•Comparing S. aureus and S. argenteus from the same source enhances understanding of their similarities and differences.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>37573713</pmid><doi>10.1016/j.ijfoodmicro.2023.110348</doi><tpages>1</tpages></addata></record>
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subjects Characterization
Rice and flour product
S. argenteus
S. aureus
WGS
title Prevalence and characterization of Staphylococcus aureus and Staphylococcus argenteus isolated from rice and flour products in Guangdong, China
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