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1 RIKILT Institute of Food Safety, PO Box 230, 6700 AE Wageningen, The Netherlands
2 Laboratory of Food Microbiology, Agrotechnology and Food Sciences Group, Wageningen University, PO Box 8129, 6700 EV Wageningen, The Netherlands
Correspondence
Tjakko Abee
tjakko.abee{at}wur.nl
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Also, the food-borne pathogen Salmonella has acquired a large number of virulence genes via horizontal gene transfer (Groisman & Ochman, 1997). Within the genomes of different Salmonella enterica subsp. enterica serovar Typhimurium (S. Typhimurium) isolates, many virulence factors have been reported to be located on prophages, which are bacteriophages integrated into the bacterial genome (Bakshi et al., 2000; Figueroa-Bossi & Bossi, 1999, 2001; Ho et al., 2002; Miao et al., 1999; Mirold et al., 1999; Stanley et al., 2000). For example, within the genome of S. Typhimurium lilleengen type (LT)2, which is an attenuated laboratory strain whose genome has been sequenced (McClelland et al., 2001), prophages Gifsy-1, Gifsy-2, Fels-1 and Fels-2 all encode one or more genes that are somehow involved in virulence (reviewed by Brussow et al., 2004). These prophages are often identified adjacent to tRNA genes (McClelland et al., 2001), which are hot spots for insertion of transferable elements in general (Cheetham & Katz, 1995; Reiter et al., 1989), because these genes are highly conserved among bacterial genomes (Campbell, 2003; Hou, 1999). Our study focused on the emerging multiple-antibiotic-resistant S. Typhimurium definitive type (DT)104. The isolates of S. Typhimurium DT104 that have emerged during the past decades have a core pattern of resistance to the five antibiotics ampicillin, chloramphenicol, streptomycin, sulfonamides and tetracycline, referred to as penta-resistance type ACSSuT (Glynn et al, 1998; Humphrey, 2001; Threlfall et al., 1994; Threlfall, 2000). The five genes for this penta-resistance type, aadA2, floR, pse-1, sul1 and tet(G), are clustered within the genome on the so-called Salmonella genomic island 1 (SGI-1), which also contains horizontally transferable genetic elements such as phage- and plasmid-related genes (Boyd et al., 2001; Briggs & Fratamico, 1999). Based on phage typing for S. Typhimurium by the Anderson scheme (Anderson et al., 1977), five subtypes have been described within DT104: DT104A, DT104B, DT04B low, DT104H and DT104L. Phage type U302 was previously referred to as being DT104-related (Briggs & Fratamico, 1999). Interestingly, of 160 DT104 isolates studied, the DT104L subtype isolates harbouring penta-resistance have been revealed to be the most frequently occurring subtype, with 40 % of all isolates (Malorny et al., 2002).
The currently used Anderson phage-typing scheme uses 34 bacteriophages to distinguish 207 DTs (Anderson et al., 1977) and the pattern of sensitivity of an isolate to these bacteriophages results in a phage-type number, such as DT104. However, this typing method has some drawbacks. Several S. Typhimurium isolates cannot be classified by this method, and the method itself requires considerable experience for scoring, and to achieve good standardization (Hu et al, 2002). Furthermore, Schmieger (1999) noted that, if the original Anderson typing bacteriophage stocks become exhausted, this may be the end of this method. Therefore, molecular methods have been developed and implemented to replace conventional phage typing (Hu et al., 2002; Tucker & Heuzenroeder, 2004). The presence of a prophage in the S. Typhimurium genome can affect the susceptibility to a bacteriophage, resulting in a different phage type, referred to as phage-type conversion (Mmolawa et al., 2002; Rabsch et al, 2002; Tucker & Heuzenroeder, 2004). Analysis of prophage distribution in different S. Typhimurium isolates may supply additional information for such a molecular method for phage typing.
In a previous genomic subtractive hybridization study, we identified novel S. Typhimurium DT104L sequences of mainly prophage origin (Hermans et al., 2005). The sequences obtained were similar to those of bacteriophages ST104 (Tanaka et al., 2004) and ST64B (Mmolawa et al., 2003a). Furthermore, a novel prophage remnant was identified, designated prophage ST104B in the current study, which harbours a homologue of the Escherichia coli O157 : H7 HldD LPS assembly-related protein and the irsA gene, which is suggested to be involved in macrophage survival (Baumler et al., 1994). The objective of the present study was to investigate the distribution of the prophages ST104, ST104B and ST64B among S. Typhimurium isolates of different phage types, with special focus on S. Typhimurium DT104 and related types. The four prophages Gifsy-1, Gifsy-2, Fels-1 and Fels-2 that have been described in the sequenced S. Typhimurium LT2 strain were also included. Because of our focus on DT104 and the importance of the multi-antibiotic resistance of this type, all isolates were also tested for the presence of the five SGI-1-located antibiotic-resistance genes. Differences in the presence of prophages can be indicative of the virulence potency of an S. Typhimurium strain, since many virulence factors have been reported to be located on prophages. Furthermore, these results will help to increase our knowledge of the relationship between prophage presence and conventional phage typing for S. Typhimurium.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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, and were obtained from RIKILT Institute of Food Safety, the Dutch National Institute of Public Health and the Environment (RIVM) and the American Type Culture Collection (ATCC). The isolates were typed at the National Salmonella Reference Laboratory of the Federal Institute for Risk Assessment, Germany. All isolates were stored at –80 °C in brain heart broth plus 50 % (v/v) glycerol. The isolates were grown overnight in brain heart broth at 37 °C without shaking. Genomic DNA was extracted from overnight cultures by using a genomic DNA wizard kit (Promega).
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), and prophages ST104 and ST64B and the prophage remnant ST104B, referred to as the non-LT2 prophages, which we could identify in S. Typhimurium DT104L. The non-LT2 prophages were identified in S. Typhimurium DT104L by using the sequences of: (a) our earlier DT104L genomic subtractive hybridization results (accession nos. AY462969–AY463002; Hermans et al., 2005); (b) bacteriophages ST104 (NC_005841; Tanaka et al., 2004) and ST64B (NC_004313; Mmolawa et al., 2003a); and (c) the DT104 genome (NC_004513). The sequence data of the DT104 genome were produced by the Salmonella spp. Sequencing Group at the Sanger Institute, Hinxton, UK, and can be obtained from ftp://ftp.sanger.ac.uk/pub/pathogens/Salmonella. A comparison between the genome sequences of LT2 and DT104 at the Gifsy and Fels prophage loci, by using the software package Vector NTI Suite version 5.1 (Invitrogen), revealed that the Fels prophages were absent in DT104. This resulted in the identification of the integration positions of the Fels bacteriophages and the design of primers to test the presence or absence of these prophages (Fig. 1). The Gifsy prophages were found in both LT2 and DT104, therefore, primers were designed based only on the annotation of these prophages within the LT2 genome. The genome comparison of both strains also revealed the location of the non-LT2 prophages ST104, ST104B and ST64B within the DT104 genome (Fig. 1). For the seven prophages selected, primer sets were designed on the left (LB-F and LB-R) and right (RB-F and RB-R) borders of the prophages, and an additional primer set on internal DNA fragments for the non-LT2 prophages ST104 (cI), ST104B (HldD homologue) and ST64B (non-coding region). Notably, primer sets for internal DNA fragments of the non-LT2 prophages were designed as an additional control because the prophage border primers were based on the bacteriophage sequences while, for the LT2 prophages, the primers were based on the actual prophage sequences. Furthermore, no prophage insertion (prophage absent) could be detected by combining the LB-F and RB-R primers for each prophage. An overview of all PCR primers and amplicons used to detect the seven prophages is shown in Table 2 and is schematically presented in Fig. 1. The primers (Isogen) at a 0.2 µmol l–1 concentration were combined with 0.2 mmol l–1 of each dNTP, 3 mmol l–1 MgCl2, 1xPCR reaction buffer and 
1–100 ng DNA template, and were amplified with 1 U Taq polymerase (all Invitrogen) in a total volume of 50 µl. After an initial denaturation at 95 °C for 3 min, the samples were subjected to 30 cycles of 95 °C for 30 s, 60 °C for 60 s, and 72 °C for 45 s, followed by a final 7 min incubation at 72 °C. The elongation step of 60 °C was performed for 90 s for the phage ST104B border primer combination. Samples were fractionated by 2 % (w/v) agarose gel electrophoresis and visualized by ethidium bromide staining. All PCRs were performed at least three times for each isolate. For several isolates, a weak prophage absent band was observed, although the prophages were detected as present (Fig. 2b, Table 3). Therefore, to exclude for these isolates any DNA contamination by other isolates of the PCRs performed, all PCR materials were tested for contamination, DNA was isolated from single colonies, and colony PCRs were performed directly from 50 single colonies. The PCR materials were all negative, and for the PCRs of the single colonies, again, a weak prophage absent band was observed, although the prophages were detected as present. A possible explanation for observing weak prophage absent bands while the prophages were detected as present, will be mentioned in the discussion.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. The loci of the LT2 prophages were derived from GenBank accession no. NC_003197 (McClelland et al., 2001). Bacteriophage Gifsy-1 was integrated into the GTP-binding elongation factor encoding the lepA gene of S. Typhimurium LT2 (GenBank accession no. AF001386), resulting in prophage Gifsy-1 as indicated, and prophage Gifsy-2 was located between the nicotinate phosphoribosyltransferase-encoding pncB and aminopeptidase N-encoding pepN genes. Prophage Fels-1 was located between the ORFs STM0892 (ybjP, putative lipoprotein) and STM0930 (putative cytoplasmic protein), and prophage Fels-2 between STM2693 (regulatory RNA 10Sa) and STM2740 (phage integrase protein). A comparison of the S. Typhimurium LT2 (NC_003197) and DT104 (NC_004513) genome sequences, by using the previously identified DT104 sequences derived from bacteriophages ST104 (NC_005841) and ST64B (NC_004313), and subtractive hybridization results (AY462969–AY463002), resulted in the identification of the genome loci and characteristics of the non-LT2 prophages ST104, ST104B and ST64B. Prophage ST104 was found in S. Typhimurium DT104, when compared to the LT2 genome, adjacent to the threonine tRNA gene thrW. The integration of bacteriophage ST104 into the DT104 genome resulted in a duplication of the 3' part of thrW. Prophage remnant ST104B, which contains an ORF homologous to HldD of E. coli O157 : H7 involved in LPS assembly, was found adjacent to ORF STM1871 (a putative phage integrase), which is part of the prophage remnant containing the sopE2, pagO and pagK genes. An identical copy of ORF STM1871 was identified on prophage remnant ST104B. Prophage ST64B was located adjacent to the serine tRNA gene serU. The genomic integration of the ST64B bacteriophage resulted in duplication of the 3' part of the tRNA serU.
Prophage detection
The PCR primers designed for the detection of the seven prophages (as presented in Table 2 and indicated with arrows in Fig. 1) were initially tested by using genomic DNA isolated from S. Typhimurium LT2 strain ATCC 700720 and S. Typhimurium DT104L strain 7945. Primer sets were designed to detect the left and right borders for each prophage and to detect internal prophage fragments for the non-LT2 prophages. Furthermore, if the combination of the outer-left and right border resulted in a product, we concluded that the prophage was not inserted into the genome (prophage absent). For example, the results of agarose gel electrophoresis of the PCR products of prophages ST104 (Fig. 2a) and ST64B (Fig. 2b) for the LT2 and DT104L strains are shown, for which left prophage border (LB), right prophage border (RB), internal prophage fragment (cI or int.), and outer-left and right prophage border (prophage absent) PCRs were performed. Both prophages were absent from the LT2 strain and present in the DT104L strain, based on the finding that, for LT2, only the prophage absent band was visible on the gels, while, for DT104L, three dominant bands were obtained, corresponding to the LB, RB and internal prophage fragments, respectively. Notably, an additional weak prophage absent band was observed for prophage ST64B in this DT104L strain (Fig. 2b). The PCR results obtained for these two strains for the seven prophages are presented in Table 3. The Gifsy prophages were detected in both strains, the LT2 Fels prophages only in LT2, and the non-LT2 prophages (ST104, ST104B and ST64B) were detected only in the DT104 isolate. Finally, prophages Fels-2 Gifsy-1 and ST64B showed an additional weak prophage absent band, although the prophages were detected as present, which was found not to be caused by any contamination (see Methods).
Prophage distribution among different S. Typhimurium isolates
All prophage detection PCRs, as mentioned above, were performed for the S. Typhimurium isolates listed in Table 1. For each isolate, the PCR results were scored as prophage present (+), prophage absent (–) or prophage borders present and internal fragment absent (o), as depicted in Table 4. Prophage Gifsy-1 was present in all isolates, except for the two DT104L isolates 433 and 455, and isolates 419 and 445. The Gifsy-2 prophage was present in all isolates. Prophage Fels-1 was only found in four isolates: the two LT2 isolates ATTC 700720 and 286, and the two DT193 isolates 389 and 390. Prophage Fels-2 was found in the two LT2 isolates and nine other isolates of different phage types. Prophages ST104 and ST104B were present in all 14 phage type DT104L isolates and the U302 isolate. All isolates of prophage profiles 1 and 10 that contained the ST104 and ST104B prophages, except the DT104L isolate 417 and the U302 isolate, were of penta-resistance type ACSSuT (depicted in Table 1). In addition, the prophage borders of ST104, without detecting the internal cI fragment, were also detected in 20 other isolates belonging to different phage types, including DT104A and DT104B low. Prophage ST64B was present in all 14 phage type DT104L isolates, the U302 isolate and nine other isolates. Also, for prophage ST64B, the borders were detected in two additional isolates (322 and 323), although the internal fragment was not detected.
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. In total, 12 different prophage profiles were identified. Based on the phage-typing numbers, several isolates of the same phage type resulted in the same profile, such as the two LT2 isolates resulting in profile 9, the three DT104B low isolates resulting in profile 4, and the 12 DT104L isolates, except for isolates 433 and 455, which lacked prophage Gifsy-1, resulting in profile 1. In contrast, analysis of the five DT193 isolates resulted in more, different profiles (2, 4 and 8), and the two DT208 isolates resulted in profiles 2 and 7. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Reiter et al., 1989). The HldD homologue, which has been described as a putative virulence factor candidate (Hermans et al., 2005), was located on a prophage-like, horizontally transferable genetic element designated prophage ST104B. The presence of virulence factors on such elements has also been described for other S. Typhimurium isolates (Bakshi et al., 2000; Figueroa-Bossi & Bossi, 1999; Figueroa-Bossi et al., 2001; Ho et al., 2002; Miao et al., 1999; Mirold et al., 1999; Stanley et al., 2000). If prophages Gifsy-1, Fels-2 and ST64B were detected in an isolate, shown by strong prophage present bands on the agarose gel, an additional weak prophage absent PCR band was observed. The latter observation may be explained by spontaneous prophage induction, leading to excision of the prophage from the genome, in a small fraction of the stationary-phase cells lacking the prophage in their genome (Bossi et al., 2003; Figueroa-Bossi & Bossi, 1999; Weinbauer, 2004). In our study, DNA was isolated from overnight-grown cultures (stationary growth phase), similar to the overnight cultures used for conventional phage typing, and the PCR results may have been obtained from cells with and without the prophages in their genome. For the other prophages, no double PCR results were obtained, indicating that these prophages were not spontaneously induced or induced at lower, non-detectable levels (Bossi et al., 2003).
The prophage borders of ST104 and ST64B were detected in many isolates, although for some of these isolates, the internal fragments of the prophages were not found. In these cases, the internal DNA fragment(s) may indeed be absent, resulting in a so-called prophage remnant, but alternatively, the internal sequence at this position may be different, which could indicate the presence of a different prophage, due to recombinations, rearrangements or deletions, which are common features of prophages (Casjens, 2005; Casjens et al., 2005; Mmolawa et al., 2003a, b; Pedulla et al, 2003; Yamamoto, 1969). Genetic diversity has previously been reported for prophage ST64B. This prophage has been found to be defective in different phage types of S. Typhimurium, and several strains appear to contain different sizes of internal prophage fragments (Tucker & Heuzenroeder, 2004). In S. Typhimurium DT104, active ST64B (Figueroa-Bossi & Bossi, 2004) and ST104 (Tanaka et al., 2004) prophages have been reported. The induced ST104 prophage has been isolated only from DT104 isolates. In our study, the internal fragment of prophage ST104, representing cI, was detected only in the S. Typhimurium DT104L isolates and the U302 isolate. Most likely, the other isolates contained a remnant or recombination of ST104, because the internal fragment was not detected.
Our study revealed 12 different prophage profiles for the 23 non-DT104 and 19 DT104 S. Typhimurium isolates. When the isolates resulting in similar prophage profiles were gauged against their phage-type numbers, no clear relationships were found with specific phage types. In some cases, the prophage typing distinguished more groups than conventional phage typing (DT104L or DT193), while in other cases, different phage types had a similar prophage profile (profile 2 or 5). Notably, discrimination between DT104A, DT104B low and DT104L isolates could be made based on the presence of prophages ST104, ST104B and ST64B. In earlier studies, the Fels prophages could not be detected, whereas the Gifsy prophages could be detected in the genomes of non-LT2 S. Typhimurium isolates (Porwollik et al., 2004; Reen et al., 2005). In our study, more variation in the presence of these LT2 prophages was identified among different non-LT2 isolates. Prophage Gifsy-1 was absent in four isolates, and prophage Fels-1 was detected in two and Fels-2 in nine non-LT2 isolates. Although prophage Gifsy-1 was absent in four isolates, both Gifsy prophages can be seen as common S. Typhimurium prophages. The prophage remnant ST104B, which harboured the putative virulence factor HldD homologue, was detected mainly in phage type DT104L isolates with prophage profile 1 and penta-resistance type ACSSuT (depicted in Table 1). Notably, the antibiotic-resistance genes for penta-resistance were detected only in DT104 isolates. The HldD homologue may be involved in LPS assembly in S. Typhimurium DT104, resulting in modification of the LPS structure and/or architecture (Hermans et al., 2005). This observation may offer an explanation for the phenotypic gel-based differences described elsewhere in LPS with various DT104 types (Lawson et al., 2002).
This study indicates the potential for molecular typing of S. Typhimurium based on prophage sequences. Previously, this potential was also described by using an amplified fragment length polymorphism (Hu et al., 2002), multilocus sequence typing (Ross & Heuzenroeder, 2005) or microarray-based approach (Pelludat et al., 2005). It is well established that phage-type conversion can occur when lambdoid bacteriophages integrate into the genome of S. Typhimurium (Mmolawa et al., 2002; Rabsch et al., 2002; Tucker & Heuzenroeder, 2004). In addition, the detection of prophages can also give information about the virulence potency of an S. Typhimurium strain, since many virulence factors have been reported to be located on prophages (Bakshi et al., 2000; Figueroa-Bossi & Bossi, 1999; Figueroa-Bossi et al., 2001; Ho et al., 2002; Miao et al., 1999; Mirold et al, 1999; Stanley et al., 2000), and can therefore be useful for risk assessment. The different isolates used in our study may contain as yet unidentified additional prophages, or recombinations of known prophages, called mosaics (Casjens, 2005; Casjens et al., 2005; Mmolawa et al., 2003a, b; Pedulla et al., 2003; Yamamoto, 1969). Our study is believed to be the first to reveal a relationship between prophage presence and phage type that may be useful for the development of a molecular method to replace conventional phage typing. However, more genome sequences of other S. Typhimurium strains or bacteriophages, combining earlier work (Hu et al., 2002; Pelludat et al., 2005; Ross & Heuzenroeder, 2005) and screening of the genomic regions adjacent to tRNAs of new emerging salmonellae as hot spots for bacteriophage integration into the genome (Campbell, 2003; Cheetham & Katz, 1995; Hou, 1999; Reiter et al., 1989), will help to gain more insight into the relationship between the presence of prophages and conventional phage typing, and their impact on virulence. Finally, our results suggest that the presence of the genes for penta-resistance type ACSSuT, the HldD homologue containing ST104 prophage remnant and phage type DT104L are most likely common features of the emerging subtype of S. Typhimurium DT104.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 16 January 2006;
revised 17 March 2006;
accepted 30 March 2006.
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