Staphylococcus aureus is an important pathogen of humans and animals. The aim of this study was to characterize 71 of S. aureus isolates from raw cow milk in southern Xinjiang of China, including molecular typing, distribution of virulence genes, and antimicrobial susceptibility. The isolates belonged to 18 sequence types (STs) (including 11 novel STs) and 6 spa types which were divided into five different clonal complexes (CCs), including CC188, CC352, CC22, CC398, and CC5406. The majority of the strains was grouped into multilocus sequence typing (MLST) CC188 (n = 41), t189 (n = 40), and ST5796 (n = 17). Only 30.9, 12.7, 11.3, and 9.9% of the isolates were resistant to erythromycin, clindamycin/norfloxacin, tetracycline, and gentamicin, respectively. Nine of multidrug resistant (MDR) isolates were observed which was associated with CC398-t2876. The adhesion molecules clfa, clfb, and hlb were most frequently detected with the percentage rate of 98.6% (70/71), 98.6% (70/71), and 90.1% (64/71), respectively. The percentage rates of the staphylococcal enterotoxin genes sea, seb, sec, sed, seg, and sei in S. aureus isolates were 5.6, 19.8, 40.8, 1.4, 49.3, and 30.9%, respectively. The see, seh, and sej genes were not found. This study provides data about the occurrence of S. aureus in raw cow milk, revealing high carriage frequency, drug resistance, and population structure of S. aureus. Furthermore, this study suggests that effective hygienic measures be taken when handling dairy cows, in order to prevent spreading MDR strains to human through direct contact and/or consumption of contaminated food.

College of Animal Sciences Key Laboratory of Tarim Animal Husbandry and Science Technology of Xinjiang Production and Construction Corps Tarim University Alar 86 843300 China

Key Laboratory of Protection and Utilization of Biological Resources in Tarim Basin of Xinjiang Production and Construction Corps College of Life Sciences Tarim University Alar 86 843300 China

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Aslantaş Ö, Demir C (2016) Investigation of the antibiotic resistance and biofilm-forming ability of Staphylococcus aureus from subclinical bovine mastitis cases. J Dairy Sci 99:8607–8613. https://doi.org/10.3168/jds.2016-11310 PubMed DOI

Basanisi MG, La BG, Nobili G, Franconieri I, La SG (2017) Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol 62:141–146. https://doi.org/10.1016/j.fm.2016.10.020 PubMed DOI

Baym M, Stone LK, Kishony R (2016) Multidrug evolutionary strategies to reverse antibiotic resistance. Science 351:(6268). https://doi.org/10.1016/j.fm.2016.10.020

CLSI (2015) Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria: approved guideline. Clinical Laboratory Standards Institute

Chajęcka-Wierzchowska W, Zadernowska A, Nalepa B, Sierpińska M, Łaniewska-Trokenheim Ł (2015) Coagulase-negative staphylococci (CoNS) isolated from ready-to-eat food of animal origin–phenotypic and genotypic antibiotic resistance. Food Microbiol 46:222–226. https://doi.org/10.1016/j.fm.2014.08.001 PubMed DOI

Eriksson J, Espinosa-Gongora C, Stamphøj I, Larsen AR, Guardabassi L (2013) Carriage frequency, diversity and methicillin resistance of Staphylococcus aureus in Danish small ruminants. Veterinary Microbiol 163:110–115. https://doi.org/10.1016/j.vetmic.2012.12.006 DOI

Feng Y, Chen CJ, Su LH, Hu S, Yu J, Chiu CH (2008) Evolution and pathogenesis of Staphylococcus aureus: lessons learned from genotyping and comparative genomics. Fems Microbiol Reviews 1:23–37. https://doi.org/10.1111/j.1574-6976.2007.00086.x DOI

Gomes F, Henriques M (2016) Control of bovine mastitis: old and recent therapeutic approaches. Current Microbiol 72:377–382. https://doi.org/10.1007/s00284-015-0958-8 PubMed DOI

Hasman H, Moodley A, Guardabassi L, Stegger M, Skov RL, Aarestrup FM (2010) Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Veterinary Microbiol 141:326–331. https://doi.org/10.1016/j.vetmic.2009.09.025 DOI

Haveri M, Hovinen M, Roslöf A, Pyörälä S (2008) Molecular types and genetic profiles of Staphylococcus aureus strains isolated from bovine intramammary infections and extramammary sites. J Clin Microbiol 46:3728–3735. https://doi.org/10.1128/JCM.00769-08 PubMed DOI PMC

Jakobsen RA, Heggebø R, Sunde EB, Skjervheim M (2011) Staphylococcus aureus and Listeria monocytogenes in Norwegian raw milk cheese production. Food Microbiol 28:492–496. https://doi.org/10.1016/j.fm.2010.10.017 PubMed DOI

Jessen LR, Sørensen TM, Lilja ZL, Kristensen M, Hald T, Damborg P (2017) Cross-sectional survey on the use and impact of the Danish national antibiotic use guidelines for companion animal practice. Acta Vet Scand 59:81. https://doi.org/10.1186/s13028-017-0350-8 PubMed DOI PMC

Kateete DP, Kabugo U, Baluku H, Nyakarahuka L, Kyobe S, Okee M, Najjuka CF, Joloba ML (2013) Prevalence and antimicrobial susceptibility patterns of bacteria from milkmen and cows with clinical mastitis in and around Kampala, Uganda. PLoS One 8(5).  https://doi.org/10.1371/journal.pone.0063413

Lowder BV, Guinane CM, Ben NL, Weinert LA, ConwayMorris A, Cartwright RA, Simpson AJ, Rambaut A, Nu¨bel U, Fitzgerald JR, (2009) Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad, USA 106:19545–19550. https://doi.org/10.1073/pnas.0909285106 DOI

Liu H, Li SL, Meng L, Dong L, Zhao SG, Lan XY, Wang JQ, Zheng N (2017) Prevalence, antimicrobial susceptibility, and molecular characterization of Staphylococcus aureus isolated from dairy herds in northern China. J Dairy Sci 100:8796–8803. https://doi.org/10.3168/jds.2017-13370 PubMed DOI

Li M, Diep BA, Villaruz AE, Braughton KR, Jiang X, DeLeo FR (2009) Evolution of virulence in epidemic community-associated methicillinresistant Staphylococcus aureus. Proc Natl Acad, USA 106:5883–5888. https://doi.org/10.1073/pnas.0900743106 DOI

Li LP, Zhou LX, Wang LH, Xue HP, Zhao X (2015) Characterization of methicillin-resistant and -susceptible staphylococcal isolates from bovine milk in northwestern China. PLoS One 10(3). https://doi.org/10.1371/journal.pone.0116699

Li TM, Lu HY, Wang X, Gao QQ, Dai YG, Shang J, Li M (2017) Molecular characteristics of Staphylococcus aureus causing bovine mastitis between 2014 and 2015. Front Cell Infect Microbiol 7:127. https://doi.org/10.3389/fcimb.2017.00127 PubMed DOI PMC

Montanaro L, Ravaioli S, Ruppitsch W, Campoccia D, Pietrocola G, Visai L, Speziale P, Allerberger F, Arciola CR (2016) Molecular characterization of a prevalent ribocluster of methicillin-sensitive Staphylococcus aureus from orthopedic implant infections. Correspondence with MLST CC30. Front Cell Infect Microbiol 6:8. https://doi.org/10.3389/fcimb.2016.00008

Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, Gillece J, Driebe E, Liu CM, Springer B, Zdovc I, Battisti A, Franco A, Zmudzki J, Schwarz S, Butaye P, Jouy E, Pomba C, Porrero MC, Ruimy R, Smith TC, Robinson DA, Weese JS, Arriola CS, Yu F, Laurent F, Keim P, Skov R, Aarestrup FM (2012) Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. Mbio 31.  https://doi.org/10.1128/mBio.00305-11

Porrero MC, Hasman H, Vela AI, Fernández-Garayzábal JF, Domínguez L, Aarestrup FM (2012) Clonal diversity of Staphylococcus aureus originating from the small ruminants goats and sheep. Veterinary Microbiol 156:157–161. https://doi.org/10.1016/j.vetmic.2011.10.015 DOI

Panahi M, Saei HD (2019) Genetic diversity and methicillin resistance of Staphylococcus aureus originating from buffaloes with mastitis in Iran. Comp. Immunol Comparative Immunology, Microbiology and Infectious Diseases 62:19–24. https://doi.org/10.1016/j.cimid.2018.11.014 PubMed DOI

Rola JG, Czubkowska A, Korpysa-Dzirba W, Osek J (2016) Occurrence of Staphylococcus aureus on farms with small scale production of raw milk cheeses in poland. Toxins 8:62. https://doi.org/10.3390/toxins8030062 DOI PMC

Ren Q, Liao GH, Wu ZH, Lv JF, Chen W (2020) Prevalence and characterization of Staphylococcus aureus isolates from subclinical bovine mastitis in southern Xinjiang, China. J Dairy Sci 103:3368–3380. https://doi.org/10.3168/jds.2019-17420 PubMed DOI

Rajagopal M, Martin MJ, Santiago M, Lee W, Kos VN, Meredith T, Gilmore MS, Walker S (2016) Multidrug intrinsic resistance factors in Staphylococcus aureus identified by profiling fitness within high-diversity transposon libraries. mBio 7:4. https://doi.org/10.1128/mBio.00950-16

Ruegg PL, Oliveira L, Jin W, Okwumabua O (2015) Phenotypic antimicrobial susceptibility and occurrence of selected resistance genes in gram-positive mastitis pathogens isolated from Wisconsin dairy cows. J Dairy Sci 98:4521–4534. https://doi.org/10.3168/jds.2014-9137 PubMed DOI

Sung JM, Lloyd DH, Lindsay JA (2008) Staphylococcus aureus host specificity: comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology 154:1949–1959. https://doi.org/10.1099/mic.0.2007/015289-0 PubMed DOI

Song MH, Bai YL, Xu J, Carter MQ, Shi CL, Shi XM (2015) Genetic diversity and virulence potential of Staphylococcus aureus isolates from raw and processed food commodities in Shanghai. Int J Food Microbiol 195:1–8. https://doi.org/10.1016/j.ijfoodmicro.2014.11.020 PubMed DOI

Tarekgne EK, Skjerdal T, Skeie S, Rudi K, Porcellato D, Félix B, Narvhus JA (2016) Enterotoxin gene profile and molecular characterization of Staphylococcus aureus isolates from bovine bulk milk and milk products of Tigray Region, Northern Ethiopia. J Food Protect 79:1387–1395. https://doi.org/10.4315/0362-028X.JFP-16-003 DOI

Wang W, Lin XH, Jiang T, Peng ZX, Xu J, Yi LX, Li FQ, Fanning S, Baloch Z (2018) Prevalence and characterization of Staphylococcus aureus cultured from raw milk taken from dairy cows with mastitis in Beijing. China Front Microbiol 9:1123. https://doi.org/10.3389/fmicb.2018.01123 PubMed DOI

Wang D, Zhang LM, Zhou XZ, He YL, Yong CF, Shen ML, Szenci O, Han B (2016) Antimicrobial susceptibility, virulence genes, and randomly amplified polymorphic DNA analysis of Staphylococcus aureus recovered from bovine mastitis in Ningxia, China. J Dairy Sci 99:9560–9569. https://doi.org/10.3168/jds.2016-11625 PubMed DOI

Wu S, Huang J, Zhang F, Wu Q, Zhang J, Pang R, Zeng H, Yang X, Chen M, Wang J, Dai J, Xue L, Lei T, Wei X (2019) Prevalence and characterization of food-related methicillinresistant Staphylococcus aureus (MRSA) in China. Front Microbiol 10:304 DOI