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Genome Sequences of Copper Resistant and Sensitive Zhang et al. Standards in Genomic Sciences (2015) 10:35 DOI 10.1186/s40793-015-0021-1 SHORT GENOME REPORT Open Access Genome sequences of copper resistant and sensitive Enterococcus faecalis strains isolated from copper-fed pigs in Denmark Siyu Zhang1,2, Dan Wang3, Yihua Wang1, Henrik Hasman4, Frank M. Aarestrup4, Hend A. Alwathnani5, Yong-Guan Zhu2,6 and Christopher Rensing1,6* Abstract Six strains of Enterococcus faecalis (S1, S12, S17, S18, S19 and S32) were isolated from copper fed pigs in Denmark. These Gram-positive bacteria within the genus Enterococcus are able to survive a variety of physical and chemical challenges by the acquisition of diverse genetic elements. The genome of strains S1, S12, S17, S18, S19 and S32 contained 2,615, 2,769, 2,625, 2,804, 2,853 and 2,935 protein-coding genes, with 41, 42, 27, 42, 32 and 44 genes encoding antibiotic and metal resistance, respectively. Differences between Cu resistant and sensitive E. faecalis strains, and possible co-transfer of Cu and antibiotic resistance determinants were detected through comparative genome analysis. Keywords: Enterococcus faecalis, Copper resistance, Antibiotic resistance, Genome sequence, Comparative genomics Introduction Enterococci belong to the gastrointestinal flora of Copper is an essential trace element with an ubiquitous humans and animals, and have been known for more cellular distribution and performs several biological than a century for their pathogenicity to humans, caus- functions [1]. It serves as an important structural com- ing urinary tract and surgical wound infections, bacter- ponent or catalytic co-factor for a wide range of different aemia and endocarditis [8]. Currently, more than 30 enzymes in various important biochemical pathways in species within the genus Enterococcus have been de- bacteria, plants and animals [2]. Because Cu, among scribed, and the two most studied enterococcal species many other micronutrients, is beneficial for growth pro- are Enterococcus faecium and Enterococcus faecalis [9]. motion and feed efficiency of farm animals [3, 4], it is Over the last two decades, E. faecalis and E. faecium extensively used as an additive in swine feed. Normally, have become increasingly important nosocomial patho- the concentration of Cu used in animal feed is in excess gens worldwide and are difficult treat due to their of the nutritional requirements of animals as it is used increasing multidrug resistance [10]. The intrinsic resist- as an alternative to in-feed antibiotics for prevention of ance of Enterococcus to many antibiotics and its acquisi- diarrheal disease [5]. Therefore, enteric bacteria, both tion of resistance determinants to other antimicrobial commensal and pathogenic, in these animals have typic- agents led to the emergence of Enterococcus as a noso- ally acquired several additional Cu resistance determi- comial pathogen [11, 12]. Recently, the co-selection of nants to survive its toxicity [1, 6, 7]. MDR isolates by antibiotics, metals and biocides has been reported [13, 14], and the resistance of Entero- coccus to both Cu and antibiotics has been established [15, 16]. However, few studies have addressed gene * Correspondence: [email protected] transfer and the underlying molecular mechanisms of 1Department of Plant and Environmental Science, University of Copenhagen, Frederiksberg, Denmark the various Cu resistance determinants in E. faecalis 6Key Laboratory of Urban Environment and Health, Institute of Urban [17]. Herein, we present the genome sequences along Environment, Chinese Academy of Sciences, Xiamen, China with the main features of six E. faecalis strains showing Full list of author information is available at the end of the article © 2015 Zhang et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhang et al. Standards in Genomic Sciences (2015) 10:35 Page 2 of 10 the differences between Cu resistant and sensitive strains a natural inhabitant of the mammalian gastrointestinal of E. faecalis, and suggesting possible co-transfer of Cu tract and is commonly found in soil, sewage, water and and antibiotic resistance determinants in these bacteria. food [8]. E. faecalis is quite versatile and able to survive a variety of physical and chemical challenges by the acquisi- Organism information tion of diverse genetic elements, which may contribute to Classification and Features their adaption to different hosts and environments [20, 21]. Phylogenetic analysis was performed using the 16S They are able to grow in temperatures ranging from 0 °C rRNA gene sequences on the six strains S1, S12, S17, up to 50 °C, and can survive in the presence of 6.5 % NaCl S18, S19 and S32 and related species. Sequences were and in broth at pH 9.6 [22]. They can also be resistant to aligned using Clustal W, and a phylogenetic tree was heavy and transition metals [17], as well as many different constructed using neighbor-joining (NJ) method imple- antibiotics [23–25], especially vancomycin [20, 21]. mented in MEGA version 6.0. The resultant tree topolo- gies were evaluated by bootstrap analyses with 1,000 Genome sequencing information random samplings. Phylogenetic analysis based on 16S Genome project history rRNA gene sequences showed that the six strains clus- The E. faecalis strains(S1,S12,S17,S18,S19andS32) tered together with E. faecalis ATCC 29212 and E. faeca- were isolated from Cu-fed pigs as part of the Danish lis SFL with a high bootstrap value (100 %). All the E. Integrated Antimicrobial Resistance Monitoring (DAN- faecalis are in a distinct branch with the other enterococci, MAP) surveillance program [23]. The isolates were such as E. casseliflavus, E. faecium, E. hirae and the an- collected from healthy animals at or just prior to other pig gut Firmicute,thatisStreptococcus equinus slaughter. Those whole-genome shotgun projects NCDO 1037 (Fig. 1). The six strains could be classified as have been deposited in DDBJ/EMBL/GenBank under members of the genus Enterococcus based on their 16S the accession number JTKS00000000, JTKT00000000, rRNA gene phylogeny and phenotypic characteristics JTKU00000000, JTKV00000000, JTKW00000000 and (Table 1). JTKX00000000. Table 2 presents the project information E. faecalis is a Gram-positive, oval-shaped, and often and its association with MIGS version 2.0 compliance highly pathogenic bacterium classified as a member of [26]. Cu resistant strains are E. faecalis strains S1, S18, the genus Enterococcus (Table 1 and Fig. 2) [18, 19]. It is S32, while the other three strains are Cu sensitive. Fig. 1 Phylogenetic tree highlighting the position of the six E. faecalis strains relative to phylogenetically closely related type strains within the genus Enterococcus. The sequences were aligned using Clustal W, and the neighbor-joining tree was constructed based on kimura 2-parameter distance model using MEGA 6.0. Bootstrap values above 50 % are shown obtained from 1,000 bootstrap replications. Bar, 0.02 substitutions per nucleotide position. GenBank accession numbers are displayed in parentheses. Large triangles represent the six Enterococcus strains sequenced in this study Zhang et al. Standards in Genomic Sciences (2015) 10:35 Page 3 of 10 Table 1 Classification and general features of the six Enterococcus faecalis strains according to the MIGS recommendations [26] MIGS ID Property Term Evidence codea Current classification Domain: Bacteria TAS [38] Phylum: Firmicutes TAS [39] Class: Bacilli TAS [40] Order: Lactobacillales TAS [41] Family: Enterococcaceae TAS [42] Genus: Enterococcus TAS [18, 19] Species: Enterococcus faecalis TAS [43] Strain: S1, S12, S17, S18, S19, S32 NAS Gram stain Positive TAS [42] Cell shape Oval cocci TAS [42] Motility None TAS [44] Sporulation Non-sporulating TAS [43] Temperature range 10-45 °C TAS [22] Optimum temperature 37 °C TAS [22] pH range 4.6-9.9 (Optimum pH at 7.5) TAS [22] MIGS-6 Habitat Gastrointestinal tracts of humans and other mammals TAS [8] MIGS-6.3 Salinity 0-6.5 % TAS [22] MIGS-22 Oxygen Facultatively anaerobic TAS [44] MIGS-15 Biotic relationship Commensal bacterium TAS [8] MIGS-14 Pathogenicity Highly pathogenic TAS [43] MIGS-4 Geographic location Denmark NAS MIGS-5 Sample collection 2011 NAS MIGS-4.1 Latitude Unknown NAS MIGS-4.2 Longitude Unknown NAS MIGS-4.3 Altitude Unknown NAS aEvidence codes - TAS: Traceable Author Statement (i.e., a direct exists in the literature); NAS: Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence). These evidence codes are from the Gene Ontology project [45] Growth conditions and genomic DNA preparation Genome annotation E. faecalis were streaked on Slanetz agar (BD Difco) The resulting contigs were uploaded onto the Rapid plates and grown for 48 h at 42 °C. Each strain was inoc- Annotation using Subsystem Technology server databases ulated separately into 25 ml of brain heart infusion broth and the gene-caller GLIMMER 3.02 [27, 28] to predict at 37 °C for 24 h. Genomic DNA was purified from the open reading frames. The predicted ORFs were translated isolates using the Easy-DNA extraction kit (Invitrogen), and annotated by searching against clusters of orthologous and DNA concentrations were determined by the Qubit groups using the SEED databases [29], as well as NCBI da- dsDNA BR assay kit (Invitrogen). tabases. RNAmmer 1.2 [30] and tRNAscan SE 1.23 [31] were used to identify rRNA genes and tRNA genes, re- Genome sequencing and assembly spectively. CRISPR repeats were examined using CRISPR Whole genome sequencing of E. faecalis strains S1, S12, recognition tool (CRT) [32]. S17, S18, S19 and S32 was carried out on an Illumina Miseq platform (Illumina, Inc., San Diego, CA).
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