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Molecular and Phenotypic Characterization of Aerococcus Viridans Associated with Subclinical Bovine Mastitis

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Molecular and Phenotypic Characterization of Aerococcus Viridans Associated with Subclinical Bovine Mastitis RESEARCH ARTICLE Molecular and Phenotypic Characterization of Aerococcus viridans Associated with Subclinical Bovine Mastitis Gang Liu1☯, Yongxia Liu1☯, Tariq Ali1, Miro Ferreri1, Jian Gao1, Wei Chen1, Jinhua Yin1, Jingliang Su1, Séamus Fanning2,BoHan1* 1 Department of Clinical Veterinary Medicine, College of Veterinary Medicine, China Agricultural University, Beijing, P.R. China, 2 UCD-Centre for Food Safety, School of Public Health, Physiotherapy & Population Science, University College Dublin, Belfield, Dublin 4, Ireland ☯ These authors contributed equally to this work. * [email protected] Abstract OPEN ACCESS Aerococcus viridans is a wide spread bacterium in the environment and clinically this organ- Citation: Liu G, Liu Y, Ali T, Ferreri M, Gao J, Chen ism is associated with different diseases in animals and humans. However, the geno- and W, et al. (2015) Molecular and Phenotypic phenotypic characterization of A. viridans associated with bovine mastitis has not yet been Characterization of Aerococcus viridans Associated reported. The objectives of this study were to investigate the genetic and phenotypic diversi- with Subclinical Bovine Mastitis. PLoS ONE 10(4): e0125001. doi:10.1371/journal.pone.0125001 ty of A. viridans isolates using three different molecular methods including 16S rRNA gene sequencing, pulsed-field gel electrophoresis and random amplified polymorphic DNA Academic Editor: Patrick CY Woo, The University of Hong Kong, HONG KONG (RAPD) along with biochemical tests, including antimicrobial susceptibility test. In total, 60 A. viridans strains were cultured from dairy herds presenting with subclinical mastitis. The Received: January 11, 2015 results of biochemical tests revealed that most of the isolates (75.0%) were accurately iden- Accepted: March 19, 2015 tified by API Rapid 20 Strep system and the majority of A. viridans strains (96.7%) were Published: April 28, 2015 found to be catalase negative, while two (3.3%) isolates were weakly positive. All isolates Copyright: © 2015 Liu et al. This is an open access were resistant to trimethoprim-sulfamethoxazole, followed by streptomycin (96.7%), tetracy- article distributed under the terms of the Creative cline (65.0%) and clindamycin (56.7%) by minimum inhibition concentration-determining Commons Attribution License, which permits broth microdilution technique. As compared to the sequence of 16S rRNA gene, both PFGE unrestricted use, distribution, and reproduction in any medium, provided the original author and source are and RAPD showed their capacities to discriminate the intra-species diversity of A. viridans. credited. Furthermore, most of the isolates obtained from the same herd or region belonged to the Data Availability Statement: All relevant data are same major RAPD group, which indicated that RAPD is an appropriate assay for tracking within the paper and its Supporting Information files. the origins of isolates and epidemiological studies of A. viridans. This is a novel approach to All sequencing files are available from the Genbak use three molecular techniques and to compare their efficiency regarding the genetic diver- database (accession numbers KM096431, sity of A. viridans. The data suggest that A. viridans associated with subclinical mastitis has KM096432). a considerable phenotypic and genotypic diversity. Funding: This research was supported by the Chinese Twelfth “Five-year” National Science and Technology Support Project (No. 2012BAD12B03) BH, National Education Ministry's Major Project (No. 313054) BH, Specialized Research Fund for the Doctoral Program of Higher Education (SRFDP) State Education Ministry (No. 20120008110042) BH, China Postdoctoral Science Foundation (No. PLOS ONE | DOI:10.1371/journal.pone.0125001 April 28, 2015 1/14 Molecular, Phenotypic Properties of Aerococcus viridans from Mastitis 2014M561102) JG and High-end Foreign Experts Introduction Recruitment Program (No. GDT20141100043) BH. Aerococcus viridans is a gram positive coccus, which belongs to the family of Streptococcaceae Competing Interests: The authors declare that the under the genus of Aerococcus [1]. Phenotypically, A. viridans is an oxidase-negative, catalase- research was conducted in the absence of any commercial or financial relationships that could be negative or weakly-positive, facultative anaerobic bacterium [2], and usually shows green alpha construed as a potential conflict of interest. hemolysis on blood agar [3]. The aeroccocci may easily be misidentified as staphylococci or streptococci, and this may be the reason that the incidence of infections caused by aerococcal spp. has been underestimated [4]. A. viridans is wide spread organism in the environment [2], but it has been clinically associ- ated with different human and animal infections [5,6]. In veterinary medicine, A. viridans has been often associated with aquatic animal infections, like gaffkemia in lobster [7], septicemia in sea turtles [8] and mortality in tilapia [9]. Furthermore, A. viridans was isolated from swine ar- thritis, meningitis and pneumonia [10]. In dairy industry, A. viridans is associated with bovine severe respiratory syndrome [11], and has also been isolated from the milk of cows with sub- clinical and clinical mastitis [12–14]. Mastitis is an important problem affecting dairy cattle and constitutes a source of huge eco- nomic losses for the dairy industry due to the detrimental effects on milk quality and yield [15]. Although some previous studies reported the isolation of A. viridans from mastitic milk samples [12–14], the published information on molecular characterization of the bacteria from bovine mastitis is scarce, especially data from China. Moreover, a tool of accurate discrimina- tion and tracking of A. viridians isolated from milk is not yet clearly established, as well as a lack of knowledge regarding the genetic diversity of the strains, their biochemical and antimi- crobial susceptibility profiles. The present study was designed with the core objective to investigate the phenogenetic di- versity of A. viridans isolates associated with subclinical mastitis in dairy farms in Northern China. Therefore, the isolated A. viridans were defined phenotypically with their biochemical profiles and antimicrobial susceptibility. Furthermore, three different techniques: 16S rRNA gene sequencing, RAPD and PFGE analysis were applied and compared in their efficiency in discriminating and tracking A. viridans. Materials and Methods Ethics Milk samples were collected from animals with subclinical mastitis with the prior consent of farm owners and under the ethical approval granted by College of Veterinary Medicine, China Agricultural University. The protocol was permitted by the owners of the dairy farms and all efforts were made to minimize cows suffering. Sample collection From April 2010 to December 2013, milk samples (n = 1,008) were obtained from Chinese Holsteins lactating cows suffering from subclinical mastitis belonging to major dairy farms in the Northern China (Beijing = 256, Tianjin = 220 and Hebei = 532 samples). Subclinical masti- tis was determined when the somatic cell counts (SCC) 500,000 cells/ml (Fossomatic 5000TM, Foss Electric, Hillerød, Denmark), with decreased milk production and without visu- al inflammation of the udder [16]. Following, the teat was disinfected with 70% ethanol and the first three streams were discarded and quarter milk samples were aseptically collected in sterile tubes, cooled and transported to the laboratory [17]. PLOS ONE | DOI:10.1371/journal.pone.0125001 April 28, 2015 2/14 Molecular, Phenotypic Properties of Aerococcus viridans from Mastitis Isolation and identification of the bacterial isolates Milk samples (50 μl) were streaked on TSA (Trypticase Soya Agar; Sigma, India) supplemented with 5% defibrinated sheep blood (hereafter SBA, Sheep Blood Agar) and incubated aerobically at 37°C for 24 h. Following, all small (~1 mm), non-pigmented or yellow pigment colonies with alpha hemolytic activity were chosen for further identification [1]. Suspected colonies were picked, purified and primarily identified on the basis of conventional methods including colony morphology, Gram staining and hemolytic activity [1]. Confirmation of the suspected isolates was conducted by amplification of 750-bp fragments of 16S rRNA gene, with a pair of universal primers [18]. The PCR products were purified and sequenced on an ABI 3730 auto- mated sequencer at Beijing Sunbiotech, Inc. (Beijing, China). The sequence data were com- pared with the GenBank database using BLAST software and homology level 98% was considered adequate for species identification. All A. viridans isolates were stored in brain heart infusion broth (BHI; Invitrogen, Beijing, China) with 20% glycerol at -80°C until tested. Biochemical tests A commercially available identification system API Rapid 20 Strep system (bioMérieux, SA, Marcy l’Etoile, France) were used to achieve biochemical profiles of all A. viridans isolates ac- cording to the manufacturer’s instructions. Moreover, all of the isolates were tested for oxidase, catalase and the tolerance test in 6.5% and 10% NaCl [1]. In addition, the identification effi- ciency of API Rapid 20 Strep Strip was evaluated. Isolate identification to the species level was divided into four subgroups: (i) excellent species identification, %id of 99.9% and a T value of 0.75; (ii) very good species identification, %id of 99.0% and a T value of 0.5; (iii) good species identification, %id of 90.0% and a T value of 0.25; and (iv) acceptable
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