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J Med Microbiol 56 (2007), 102-109; DOI: 10.1099/jmm.0.46616-0
© 2007 Society for General Microbiology
ISSN 1473-5644

Amplified fragment length polymorphism of Streptococcus suis strains correlates with their profile of virulence-associated genes and clinical background

Thomas Rehm1, Christoph G. Baums1, Birgit Strommenger2, Martin Beyerbach3, Peter Valentin-Weigand1 and Ralph Goethe1

1 Institut für Mikrobiologie, Zentrum für Infektionsmedizin, Stiftung Tierärztliche Hochschule Hannover, D-30173 Hannover, Germany

2 Robert Koch Institut, Wernigerode Branch, D-38855 Wernigerode, Germany

3 Institut für Biometrie, Epidemiologie und Informationsverarbeitung, Stiftung Tierärztliche Hochschule Hannover, D-30173 Hannover, Germany

Correspondence
Christoph G. Baums
christoph.baums{at}gmx.de

Received 8 March 2006
Accepted 29 September 2006

Amplified fragment length polymorphism (AFLP) typing was applied to 116 Streptococcus suis isolates with different clinical backgrounds (invasive/pneumonia/carrier/human) and with known profiles of virulence-associated genes (cps1, -2, -7 and -9, as well as mrp, epf and sly). A dendrogram was generated that allowed identification of two clusters (A and C) with different subclusters (A1, A2, C1 and C2) and two heterogeneous groups of strains (B and D). For comparison, three strains from each AFLP subcluster and group were subjected to multilocus sequence typing (MLST) analysis. The closest relationship and lowest diversity were found for patterns clustering within AFLP subcluster A1, which corresponded with sequence type (ST) complex 1. Strains within subcluster A1 were mainly invasive cps1 and mrp+ epf+ (or epf*) sly+ cps2+ strains of porcine or human origin. A new finding of this study was the clustering of invasive mrp* cps9 isolates within subcluster A2. MLST analysis suggested that A2 correlates with a single ST complex (ST87). In contrast to A1 and A2, subclusters C1 and C2 contained mainly pneumonia isolates of genotype cps7 or cps2 and epf– sly–. In conclusion, this study demonstrates that AFLP allows identification of clusters of S. suis strains with clinical relevance.

Abbreviations: AFLP, amplified fragment length polymorphism; MLST, multilocus sequence typing; ST, sequence type.


   INTRODUCTION
TOP
 INTRODUCTION
METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Streptococcus suis causes invasive diseases such as meningitis, septicaemia, arthritis and polyserositis in piglets (MacInnes & Desrosiers, 1999). This pathogen is responsible for substantial economic losses in the swine industry (Staats et al., 1997). Clinically healthy pigs are carriers of the pathogen and are responsible for spreading disease (Clifton-Hadley et al., 1984). S. suis has also been associated with meningitis and other diseases in humans (Arends & Zanen, 1988). In 2005, an unusual outbreak of S. suis infections with a high mortality occurred among 215 humans in Sichuan, China (Yu et al., 2006), underlining that the zoonotic potential of S. suis might have been underestimated.

At present, 33 serotypes have been identified in S. suis. Serotype is determined by the gene cluster cps, which is in serotype 2 (cps2) strains so far the only gene locus identified to be essential for virulence (Smith et al., 1999). Serotype 2 strains are worldwide the most prevalent in association with disease in pigs and humans (Wisselink et al., 2000; Arends & Zanen, 1988). In addition, high prevalences of serotype 9 (cps9) and 1 (cps1) have been observed among porcine invasive isolates in central Europe and Great Britain, respectively. Serotype 7 strains have frequently been associated with pneumonia in Scandinavia and central Europe (Wisselink et al., 2000; Tian et al., 2004; Aarestrup et al., 1998).

The muramidase-released protein (MRP, mrp), the extracellular protein factor (EF, epf) and the suilysin (SLY, sly) are putative virulence factors of S. suis (Vecht et al., 1991; Staats et al., 1999). These factors contribute further to the diversity of S. suis strains, since various mrp and epf genotypes have been described (Smith et al., 1993; Silva et al., 2006). Serotype 2 strains, which express the 136 kDa MRP and the 110 kDa EF, are highly virulent, in contrast to European serotype 2 isolates that lack these factors (Wisselink et al., 2000).

In a study by King et al. (2002), 92 different multilocus sequence types (STs) were identified for S. suis. The vast majority of invasive isolates belonged to the ST1 complex. In contrast, the complexes of ST27 and ST87 were found to contain a higher proportion of lung isolates (King et al., 2002). There was a high prevalence of serotype 2 strains within the ST1 complex and of serotype 7 strains within the ST27 complex. However, single serotypes were found to be associated with multiple STs, indicating that serotypes are not reliable as phylogenetic markers.

In the present study, clusters of S. suis strains in amplified fragment length polymorphism (AFLP) typing were correlated with clinical background, profiles of virulence-associated genes as well as multilocus sequence typing (MLST) results.


   METHODS
TOP
 INTRODUCTION
 METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Bacterial strains. A total of 106 porcine and 10 human S. suis isolates were analysed in this study. The majority of the porcine isolates originated from northern Germany and had been characterized previously (Allgaier et al., 2001; Silva et al., 2006). Six of the human strains were from Germany and four from Canada. Strains isolated from affected organs of pigs or humans with meningitis, arthritis or septicaemia were designated invasive isolates (n=58), isolates from the lower respiratory tract of diseased animals were grouped as pneumonia isolates (n=32), and isolates from the tonsils, and nasal and vaginal swabs of healthy pigs were considered carrier isolates (n=26). Reference strains for differentiation of cps types and virulence-associated factors as described by Silva et al. (2006) were also included (Table 1Go). Bacteria were grown on sheep blood Columbia agar or in Todd–Hewitt broth for 24 h at 37 °C.


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  		Table 1. Profile of virulence-associated genes and origin of strains investigated in AFLP

 
Virulence-associated gene profiling of S. suis. DNA extraction and typing of virulence-associated genes was done as described previously (Silva et al., 2006).

AFLP typing of S. suis. A modification of the AFLP protocol of Gibson et al. (1998) was used. One microgram of HindIII-digested streptococcal DNA was used in the ligation reaction containing 30 µM adapter oligonucleotides ADH1 (5'-ACGGTATGCGACAG-3') and ADH2 (5'-AGCTCTGTCGCATACCGTGAG-3'), 1x T4 DNA ligase buffer and 1 U T4 DNA ligase (both Promega) in a final volume of 20 µl. Subsequently, PCR amplification was performed in a final reaction volume of 50 µl containing the following components: 5 µl of a 1 : 5 dilution of ligated DNA (50 ng DNA), 1.5 mM MgCl2, 1 µM primer HI-G (5'-GGTATGCGACAGAGCTTG-3'), 0.2 mM dNTPs (Invitrogen), 2.5 U Taq DNA polymerase (Invitrogen), and PCR buffer provided by the manufacturer. Initial denaturating was carried out for 4 min at 94 °C and followed by 33 cycles including denaturation for 1 min at 94 °C, annealing for 1 min at 60 °C and elongation for 2.5 min at 72 °C (final extension for 5 min). The amplified fragments were separated by 2.5 % (w/v) agarose gel electrophoresis. The primer HI-G was chosen in preliminary experiments because, in contrast to the other three primers described by Gibson et al. (1998), amplification of at least eight bands for each strain and appropriate differentiation of all tested isolates was observed. Reproducibility of band patterns independent of the DNA preparation was demonstrated. Reference strains were included in every gel to verify inter-gel reproducibility. The inter-gel similarity of the external reference strain was at least 88 % (including different DNA preparations). AFLP patterns were analysed using BioNumerics software 4.0 (Applied Maths). The pairwise comparison of band patterns was performed using the Pearson product-moment correlation coefficient, and the dendrogram was calculated by the unweighted pair-group method using average linkages (UPGMA).

MLST analysis of S. suis strains. MLST was performed as described by King et al. (2002), with the following modifications. For a few samples, the PCR did not yield a product with the described mutS primers. For these, primers mutS forward and mutS reverse were replaced by mutS forwardnew (5'-AAGCAGGCAGTCGGCGTGGT-3') and mutS reversenew (5'-AGTACAAACTACCATGCTTC-3'). The primer thrA forward was used as forward primer as well as for subsequent sequencing reactions. Sequencing reactions were performed using the DYEnamic ET Terminator kit and the MegaBase capillary sequencer (Amersham Biosciences). MLST alleles and resulting STs were assigned using BioNumerics software 4.0 based on the MLST scheme of King et al. (2002). Analysis of ST complexes was performed with eBURST (www.mlst.net) (Feil et al., 2004).

Allele and ST assignment. Novel alleles and STs were assigned through submission of the respective data to the S. suis MLST database (http://ssuis.mlst.net).

Statistical evaluation. Statistical analysis was performed to analyse relationships between AFLP cluster and clinical background as well as the profile of virulence-associated genes. The chi square test of homogenicity (n >5) or the Fischer's exact test (n <5) were used for these comparisons. Probabilities lower than 0.05 were considered significant.


   RESULTS AND DISCUSSION
TOP
 INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Cluster analysis based on AFLP pattern

Well-characterized S. suis strains were typed by AFLP to generate a dendrogram that allowed correlation of AFLP clusters with clinical background and the profile of virulence-associated genes (Fig. 1Go, Table 1Go). In general, substantial diversity of AFLP band patterns was observed among S. suis strains (<15 % overall similarity level). At the 55 % similarity level, two main AFLP clusters, A and C, were identified. The other strains were assigned either to group B or group D (Fig. 1Go). The dendrogram suggested division of cluster A into subclusters A1 and A2. Thirty isolates clustered at a comparable high linkage level of 70 % within subcluster A1. The patterns classified as group B were related to those of cluster A with a linkage level between 42 and 54 %. Patterns within cluster C (n=28) were distinct, as their relation to any of the remaining patterns was less than 45 % similarity. Cluster C was further divided into subclusters C1 and C2 at a linkage level of 57 %. An extremely high diversity was found for the remaining strains (group D). In this group, some similarity indices were almost equal to those with the Streptococcus pyogenes reference strain (Fig. 1Go).


Figure 1
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  		Fig. 1. Dendrogram of 116 S. suis strains based on AFLP band patterns. At a 55 % similarity level, two main AFLP clusters, A and C, were identified. Strains within subcluster A1 share a 70 % overall similarity. Subcluster A2 contains the remaining strains of cluster A. A linkage level of 57 % determines division of cluster C into C1 and C2. Based on their position in the dendrogram, strains that belong to neither cluster A nor cluster C were assigned to either group B or group D. If two or more strains with the same profile of virulence-associated genes generated the same band pattern (similarity index >95 %), only one of them was included in the dendrogram. The virulence-associated gene profiles and the origin of the strains are shown in Table 1Go.

 
Congruence between AFLP clusters and ST complexes

To evaluate the AFLP-based clustering results, three isolates each were selected randomly from A1, A2, B, C1, C2 and D, and were subjected to MLST analysis (Table 2Go). One additional reference strain (D282) investigated in this study had already been multilocus sequence-typed by King et al. (2002). Using eBURST with the most stringent group definition (Feil et al., 2004), six of the 18 sequence-typed isolates were assigned to either ST complex 1 or ST complex 87 (Table 2Go). Exclusively strains of ST complex 1 belonged to the distinct and relatively homogeneous AFLP subcluster A1, while the three from subcluster A2 were part of ST complex 87 (Table 2Go). The only discordance found between AFLP and MLST analysis was that, in addition to the investigated strains of A2, strain B2631/96 of AFLP group B also belonged to ST complex 87. Analysis of the complete S. suis MLST database revealed that ST1 and ST87 are the primary founders of the two respective ST complexes (bootstrap confidence values of 100 and 72 %, respectively). The six strains from either AFLP subcluster C1 or AFLP subcluster C2 belonged to the same ST complex (ST27), but with a less-stringent group definition (identical alleles at five or more of the seven loci; Table 2Go). Sequence typing of strains of group B as well as those of group D made clear that strains within these two groups might not be genetically related, as the investigated strains did not share a single allele in MLST analysis (Table 2Go). This is in agreement with the low linkage level between strains in these AFLP groups. In general, the results suggested congruence of AFLP and MLST, which has also been found in other pathogens, e. g. in Campylobacter jejuni (Schouls et al., 2003).


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  		Table 2. Multilocus STs for selected strains according to King et al. (2002) in comparison to AFLP cluster analysis

 
Correlation of AFLP-typing results with clinical background and virulence-associated gene profiles

The virulence-associated gene profile and the clinical background of each strain is presented in Table 1Go. Cluster A was significantly associated (P <0.0001) with strains that were classified as invasive, based on their source of isolation. Of all invasive isolates, 69 % belonged to cluster A. Furthermore, the two strains (D282 and P1/7) which have been demonstrated to be highly virulent in experimental infections (Vecht et al., 1989; Norton et al., 1999), were grouped in this rather homogeneous cluster. In accordance with this, PFGE patterns of invasive S. suis strains have also been found to be less heterogeneous than those of S. suis isolates from other sources (Berthelot-Herault et al., 2002; Allgaier et al., 2001; Vela et al., 2003).

With the exception of four isolates, cluster A contained only cps1 (n=5), cps2 (n=28) and cps9 (n=13) positive strains. All strains within this cluster were positive for the suilysin gene sly and, with the exception of two strains, also for mrp. The genotype sly+ mrp+ epf+ cps2+ was significantly associated with cluster A (P <0.0001) and with subcluster A1 (P=0.0075). Furthermore, all investigated cps1 isolates belonged to subcluster A1 (Table 1Go). The homogeneous AFLP subcluster A1 represented by virulent cps2 and cps1 genotypes is in accordance with the described unique ribotype profile of these pathotypes (Smith et al., 1997).

Subcluster A2 was significantly associated with mrp+ (all variants) cps9 strains (P <0.0001), most of which (10 of 13) had an invasive clinical background. Only two of the 15 mrp+ cps9 strains did not belong to A2. With the exception of one strain (A5263/93), all cps9+ strains of subcluster A2 were positive for a specific large variant of mrp (mrp*, GenBank accession no. DQ295197; Silva et al., 2006). Interestingly, homogeneous clustering of invasive cps9 strains has not been described so far. King et al. (2002) showed that serotype 9 strains might belong to different STs. In our study, MLST of three mrp* cps9 strains of subcluster A2 revealed that they belonged to ST complex 87 (Table 2Go), and that they were single-locus variants of the two invasive serotype 9 strains of ST complex 87 investigated by King et al. (2002). The virulence-associated mrp* cps9 type isolated frequently from diseased pigs in central Europe (Wisselink et al., 2000; Silva et al., 2006) might, thus, be represented in the MLST study of King et al. (2002) by only these two strains. Furthermore, we speculate that ST complex 87 might be associated with invasive infections in central Europe to a greater extent than suggested elsewhere (King et al., 2002).

In comparison with cluster A, the prevalence of the virulence-associated factors sly, mrp and epf was significantly lower among the other strains (not in cluster A: sly+, 39 %; mrp+ (all variants), 64 %; epf+, 3 %). The majority of the strains of group B (17 of 23) and D (nine of 15) did not belong to types cps1, -2, -7 or -9. Most carrier isolates were assigned to one of these two groups (42 % in B and 23 % in D).

In contrast to groups B and D, the virulence-associated gene profiling and clinical background of the strains suggested a more specific composition of strains of cluster C. All strains of cluster C were negative for sly and epf. Cluster C, and in particular subcluster C1, was significantly associated with cps7 strains (P <0.0001). These cps7 strains were all positive for one of the different mrp variants. The genotype mrp+ (different variants) epf– sly cps2+ was significantly associated with subcluster C2 (P <0.0001). Clustering of cps7 and cps2 strains has also been observed in MLST and PFGE typing (King et al., 2002; Vela et al., 2003). However, as these studies did not include profiling of virulence-associated genes, our study showed for the first time that these cps2 strains are representative of a geno- or phenotype (epf–, EF–, respectively) which has been shown to be avirulent in experimental infections (Vecht et al., 1992).

The distribution of invasive, pneumonia and carrier isolates suggested association of cluster C with pneumonia (P=0.0017). Of the pneumonia group, 47 % belonged to cluster C (28 and 19 % of the lung isolates within subclusters C1 and C2, respectively). Among the three major ST complexes described by King et al. (2002), ST complex 27 showed the highest fraction of lung isolates (28 %). This is in accordance with the AFLP-typing results of this study, as comparative MLST analysis of six cluster C strains provided evidence of congruence between AFLP cluster C and the ST complex 27 (Table 2Go). In Scandinavia and central Europe, serotype 7 strains have been isolated frequently from piglets with bronchopneumonia (Wisselink et al., 2000; Tian et al., 2004; Aarestrup et al., 1998; Silva et al., 2006). Although pneumonia has been elicited by experimental S. suis serotype 2 infection (Berthelot-Herault et al., 2001; Soerensen et al., 2005), pathotypes causing mainly pneumonia have not been identified in the respective experiments.

All investigated human isolates from Germany (n=6) were grouped into subcluster A1, which was found to correlate with ST complex 1 identified in MLST analysis (Table 2Go). Accordingly, the vast majority (87 %) of the human isolates investigated with MLST by King et al. (2002) belonged to ST complex 1. Furthermore, the isolates of the outbreak among humans in Sichuan in 2005 were all identified as ST7, a single-locus variant of ST1 within the ST1 complex (Ye et al., 2006). The human isolates assigned to AFLP subcluster A1 carried, except for one strain, a large variant of epf (epf*). This genotype has been detected frequently in serotype 2 strains of moderate virulence for piglets and also in human isolates from Europe (Smith et al., 1993). In contrast to the human isolates from Germany, the four examined human isolates from Canada belonged to cluster C or group D, were negative for epf and sly, and contained a large variant of the mrp gene. The different AFLP clustering of the few human isolates from central Europe, North America and Asia has to be further clarified in future experiments using more strains.

In conclusion, the described AFLP typing allowed identification of S. suis clusters of clinical relevance. Profiles of virulence-associated genes (cps, mrp, epf and sly) and the clinical background of strains showed homogeneous clustering (A1) of European invasive cps2+ isolates from pigs (typically mrp+ epf+ sly+) and humans (mrp + epf* sly+). Another very different cluster (C) was associated with pneumonia and consisted of cps7 and mrp– epf– sly– cps2 strains. Furthermore, this study suggests for the first time a correlation of invasive mrp* cps9+ strains in central Europe with a certain AFLP subcluster (A2) and a single ST complex (ST87) in MLST analysis.


   ACKNOWLEDGEMENTS
 
We thank Tosso Leeb and Heike Klippert (Institut für Tierzucht und Vererbungsforschung, Stiftung Tierärztliche Hochschule Hannover) for support in sequencing. This study was supported by a grant from the Deutsche Forschungsgemeinschaft (DFG), Bonn, Germany (SFB587).


   REFERENCES
TOP
 INTRODUCTION
 METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
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Arends, J. P. & Zanen, H. C. (1988). Meningitis caused by Streptococcus suis in humans. Rev Infect Dis 10, 131–137.[Medline]

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Berthelot-Herault, F., Marois, C., Gottschalk, M. & Kobisch, M. (2002). Genetic diversity of Streptococcus suis strains isolated from pigs and humans as revealed by pulsed-field gel electrophoresis. J Clin Microbiol 40, 615–619.[Abstract/Free Full Text]

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