J Med Microbiol 57 (2008), 1369-1376; DOI: 10.1099/jmm.0.47815-0
© 2008 Society for General Microbiology
ISSN 0022-2615
Phylogenetic relationships among Streptococcus agalactiae isolated from piscine, dolphin, bovine and human sources: a dolphin and piscine lineage associated with a fish epidemic in Kuwait is also associated with human neonatal infections in Japan
Joyce J. Evans1,2,
John F. Bohnsack3,
Phillip H. Klesius1,2,
April A. Whiting3,
Julio C. Garcia1,2,
Craig A. Shoemaker1,2 and
Shinji Takahashi4
1 United States Department of Agriculture, Agricultural Research Service, Aquatic Animal Health Research Laboratories, Chestertown, MD 21620, USA
2 United States Department of Agriculture, Agricultural Research Service, Aquatic Animal Health Research Laboratories, Auburn, AL, USA
3 Department of Pediatrics, University of Utah Health Sciences Center, Salt Lake City, UT, USA
4 Division of Microbiology, Joshi-Eiyoh University, Chiyoda, Sakado, Saitama 350-0288, Japan
Correspondence
Joyce J. Evans
joyce.evans{at}ars.usda.gov
Received December 10, 2007
Accepted July 17, 2008
Streptococcus agalactiae, commonly known as group B streptococcus (GBS), is a cause of infectious disease in numerous animal species. This study examined the genetic relatedness of piscine, dolphin and human GBS isolates and bovine GBS reference strains from different geographical regions using serological and molecular serotyping and multilocus sequence typing (MLST) techniques. Piscine isolates originating from Kuwait, Brazil, Israel and the USA were capsular serotype Ia, a serotype previously unreported in GBS isolated from fish. Sequence typing of piscine isolates produced six sequence types (ST-7, ST-257, ST-258, ST-259, ST-260 and ST-261), the latter five representing allelic designations and allelic combinations not previously reported in the S. agalactiae MLST database. Genomic diversity existed between dolphin and piscine GBS isolates from Kuwait and other geographical areas. Piscine GBS isolates from Brazil, Israel, Honduras and the USA appeared to represent a distinct genetic population of strains that were largely unrelated to human and bovine GBS. The Kuwait dolphin and piscine lineage (ST-7, Ia) was also associated with human neonatal infections in Japan. Comparative genomics of piscine, human and bovine GBS could help clarify those genes important for host tropism, the emergence of unique pathogenic clones and whether these hosts act as reservoirs of one another's pathogenic lineages.
Abbreviations: CAMP, Christie–Atkins–Munch-Petersen; GBS, group B streptococcus; MLST, multilocus sequence typing; ST, sequence type.
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INTRODUCTION
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Streptococcus agalactiae, commonly known as group B streptococcus (GBS), emerged as an important infectious agent in humans during the 1960s–1970s (Schuchat, 1998; Wilkinson, 1978) following its initial description by Brown (1939). GBS has been isolated from a variety of non-human sources and is well recognized as an important causative agent of bovine mastitis (Pattison et al., 1955). The potential for human GBS to be a zoonosis has been investigated in bovine isolates, and human GBS isolates have been shown largely to be genetically distinct from bovine GBS isolates based on phenotypic properties, PFGE and randomly amplified polymorphic DNA analysis (Bohnsack et al., 2004; Elliott et al., 1990; Finch & Martin, 1984; Martinez et al., 2000; Sukhnanand et al., 2005; Vandamme et al., 1997; Wilkinson et al., 1973).
More recently, multilocus sequence typing (MLST) has helped define the phylogenetic relationship between human and bovine strains. In MLST, GBS isolates are classified as sequence types (STs) based on their composite allele numbers, and phylogenetic relationships are inferred from the similarities between the allele numbers comprising each ST or between the concatenated sequences of the individual amplicons (Bisharat et al., 2004; Davies et al., 2004; Jones et al., 2003). MLST has demonstrated that many bovine GBS isolates do not share STs with human GBS isolates, confirming the largely divergent nature of human and bovine GBS. However, two lineages of bovine GBS (ST-23 and ST-61) do appear to have a genetic relationship with human GBS. Human serotype Ia strains in the ST-23 lineage and human ST-17 strains, which are almost entirely serotype III GBS and are related to bovine ST-61 strains, are frequently associated with neonatal infections. The latter finding has led to the hypothesis that human ST-17 strains arose from a bovine GBS ancestor (Bisharat et al., 2004; Bohnsack et al., 2004; Jones et al., 2006).
GBS also sporadically causes epizootic infections in fish. First recognized as a piscine pathogen in captive freshwater shiners, Notemigonus crysoleucas (Robinson & Meyer, 1966), GBS has subsequently been reported from wild and captive fish involved in epizootics in the USA, Israel, Kuwait, Thailand and Brazil (Baya et al., 1990; Duremdez et al., 2004; Eldar et al., 1994; Evans et al., 2002; Plumb et al., 1974; Salvador et al., 2005; Suanyuk et al., 2005). GBS has also been reported from aquatic mammals, both captive and wild bottlenose dolphins, Tursiops truncatus (Evans et al., 2006; Zappulli et al., 2005). The phylogenetic relationship between fish, dolphin, bovine and human GBS has not been studied. Therefore, we examined fish GBS isolates from various geographical locations using phenotypic, serotypic and molecular techniques, and used MLST to help elucidate their phylogenetic similarity with and differences from non-fish GBS isolates.
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METHODS
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Strain collection.
Fish isolates (n=21) originated from infections in Klunzinger's mullet (Liza klunzinger) and seabream (Sparus auratus) from Kuwait (Evans et al., 2002), hybrid striped bass (Morone chrysopsxMorone saxatilis) from Israel and Nile tilapia (Oreochromis niloticus) from the USA, Brazil and Honduras (Table 1
). Nile tilapia GBS isolates were provided by Dr John Hawke (Louisiana State University, LA, USA) and Dr Salvador (Parana State, Brazil). Dr Dina Zilberg (Ben-Gurion University of the Negev, Israel) provided the hybrid striped bass isolate. The bottlenose dolphin isolate (Kuwait) was obtained as described by Evans et al. (2006). Six ST-7, serotype Ia GBS isolates from humans in Japan were provided by S. Takahashi. Reference strains were obtained from the ATCC (ATCC 13813 and ATCC 27956 GBS from bovine species and ATCC 51487 deposited as Streptococcus difficilis from diseased tilapia).
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Table 1. Piscine, dolphin, bovine and human GBS phenotype properties
PYR, pyrrolidonylarylamidase reaction; VP, Voges–Proskauer reaction; +, positive reaction; –, negative reaction; NT, non-typable. Shaded areas denote differences between isolates.
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Identification and characterization of GBS strains.
Isolates were grown on 5 % sheep blood agar (Remel) as described previously (Evans et al., 2002). Conventional biochemical tests [haemolysis, Christie–Atkins–Munch-Petersen (CAMP) test, pyrrolidonylarylamidase reaction and hippurate, urea, starch, arginine and aesculin hydrolysis] were performed as described by MacFaddin (2000). The Voges–Proskauer reaction and fermentation of sorbitol, trehalose, ribose, inulin, mannose, xylulose and lactose were derived from the API 20 Strep Multi-test System (bioMérieux), following the manufacturer's instructions. Lancefield grouping was performed with type B antisera (Oxoid). Capsular serotyping was performed twice on all strains in the laboratories of J. F. Bohnsack and repeated in a second laboratory by P. H. Klesius with GBS typing antisera directed against capsular types Ia, Ib, II, III, IV and V (Denka Seiken). Serotypes were additionally identified using a multiplex PCR assay performed twice on all isolates. The protocol was modified from that of Poyart et al. (2007) and the serotypes was determined as Ia, Ib or II according to size in base pairs of the capsular polysaccharide (cps) gene amplicons. Briefly, a cocktail of type-specific primers was created for the PCR; cycling conditions were 94 °C for 5 min, followed by 40 cycles of denaturation at 94 °C for 1 min, annealing at 55 °C for 1 min and extension at 72 °C for 1 min, followed by a final extension at 72 °C for 5 min. Banding patterns were determined by electrophoresis on 2 % agarose gels and serotypes corresponded to 521 bp (Ia), 770 bp (Ib) or 397 bp (II).
Identification of species-specific 23S rRNA genes.
One colony of each GBS isolate was incubated in tryptic soy broth at 32 °C for 24 h. Genomic DNA templates were prepared using a DNeasy Tissue kit (Qiagen) according to the manufacturer's instructions. Species-specific target DNA amplification of the S. agalactiae 23S rRNA gene was carried out as described by Kawata et al. (2004). The primer sequences were 5'-AACAGCCTCGTATTTAAAATGATAGATTAAC-3' (forward) and 5'-TCCTACCATGACACTAATGTGTC-3' (reverse). The PCR products were analysed by 1 % agarose gel electrophoresis, stained with ethidium bromide and visualized under UV light.
MLST.
In MLST, 500 bp fragments of seven housekeeping genes are amplified by PCR and the amplicons sequenced. Allele numbers are then assigned to each sequence. Individual isolates are assigned STs based on their composite allele numbers. MLST, allelic assignment and sequence typing were performed as described previously (Jones et al., 2003). Allele sequences can be found at http://pubmlst.org/sagalactiae/. MEGA software (Kumar et al., 2004) was used to construct an unrooted dendrogram showing the relationships among fish, dolphin, bovine and human STs from this study and from a collection of human and bovine isolates from North America, Japan and Brazil. The origin and serotypes of these strains have been reported previously and the dendrogram was constructed using the STs from this collection of isolates, all of which have appeared in previous publications (Bohnsack et al., 2008; Jones et al., 2003; Lin et al., 2006; Oliveira et al., 2006; Seifert et al., 2006; Takahashi et al., 2002). The eBurst program (Feil et al., 2004) was used to identify clonal complexes among these isolates. A total of 1150 strains were used to perform the eBurst analysis.
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RESULTS AND DISCUSSION
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Identification of strains as GBS
All isolates were Lancefield group B, catalase-negative, Gram-positive cocci, appearing in pairs and chains. A 23S rRNA gene fragment specific for GBS was amplified by PCR from the genomic DNA of all isolates.
Serogroup typing
The dolphin GBS isolates and 18 of the 21 piscine GBS isolates were serotype Ia (Table 1
). The capsular serotypes of three piscine isolates could not be determined with the available antisera but were confirmed as serotype Ib by molecular multiplex PCR typing. Serotype Ia is previously unrecognized as a serotype among piscine GBS isolates. Wilkinson et al. (1973) serotyped non-haemolytic piscine GBS strains obtained from Alabama (one isolate) and Arkansas (three isolates), USA, and invasive neonatal GBS strains (four isolates) using agar gel diffusion techniques and found these to be type Ib. Eldar et al. (1994) originally reported the ATCC 51487 isolate to be a novel species, S. difficile, and to be non-typable. Later, Vandamme et al. (1997) and Brochet et al. (2006) provided evidence that this isolate is actually S. agalactiae and reported the isolate to be serotype Ib. In the study reported here, replicate capsular serotyping of the ATCC 51487 isolate using GBS antisera and multiplex PCR revealed the isolate to be serotype Ia, a result inconsistent with those of Eldar et al. (1994), Vandamme et al. (1997) and Brochet et al. (2006).
MLST
The fish isolates were found to have six different STs (ST-7, ST-257, ST-258, ST-259, ST-260 and ST-261). The 16 isolates from Kuwait were collected from a bottlenose dolphin, three seabream and 12 mullet following a disease outbreak in wild mullet in Kuwait Bay beginning in August 2001 (Evans et al., 2002). All of the Kuwait isolates were ST-7, whilst the six remaining fish isolates (03ARS-BZ-TN-05, 03ARS-BZ-TN-06, LADL05-108A, LADL00-351A, IS-ET-09-03 and ATCC 51487) were found to contain novel alleles and STs (Table 2). The novel STs were found in GBS strains isolated from diverse geographical areas and were clearly distinguishable from ST-7, as all of the novel STs shared two or fewer alleles with ST-7 (Table 2). Each ST was confined to a single geographical location.
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Table 2. Piscine and dolphin GBS isolates: serotype, ST, source and country of origin
Bold-formatted STs and allelic designations are new to the MLST database.
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The ST-7 and non-ST-7 fish isolates (ST-257, ST-258, ST-259, ST-260 and ST-261) appeared in separate branches of the dendrogram (Fig. 1), which was constructed using the STs of a collection of 1150 human, bovine and piscine GBS isolates (see Methods). The Kuwait dolphin and piscine GBS isolates were part of a clone of serotype Ia ST-7 GBS that has previously been reported to be associated with bloodstream infections in human neonates in Japan (Jones et al., 2003). This clone, which was originally recognized by analysis of restriction digest patterns and designated two closely related restriction digest pattern types, Ia-3 and Ia-4, by Nagano et al. (1991), appears to be extremely rare among GBS isolates associated with human infections or with maternal colonization in Sweden, Israel, the UK, Portugal, Italy and the USA (Bisharat et al., 2005; Gherardi et al., 2007; Jones et al., 2003, 2006; Luan et al., 2005; Martins et al., 2007; Nagano et al., 2002). Despite the rarity of serotype Ia ST-7 GBS among human isolates from Western countries, a serotype Ia strain from this clone, called A909, was isolated by R. Lancefield from a human source many years ago and its genome was recently sequenced (Tettelin et al., 2005).
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Fig. 1. Dendrogram illustrating the phylogenetic relationship of the piscine isolates to human and bovine isolates. Clonal complexes (CC) are indicated, as are the STs of the piscine isolates.
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The phenotypic properties of the dolphin and fish isolates were characterized and compared with those of six ST-7, serotype Ia human GBS strains and two bovine mastitis reference strains (Table 1). All of the human GBS strains were isolated in Japan: two from the genitourinary tract of women (560249 and 841254), one from the gastric aspirate from a neonate (510036) and three from the bloodstream or cerebrospinal fluid of neonates (630653, 510029 and 510012). All of the Kuwait ST-7 isolates (designated KU) and human ST-7 isolates were β-haemolytic and CAMP factor positive, and shared a similar biochemical profile.
Analysis of the human, bovine and piscine GBS isolates in the larger sample revealed that ST-7 clustered with human isolates with ST-6 and ST-84 into a single clonal complex (Fig. 2), here designated CC 7 but which has previously been designated CC 6 (Bisharat et al., 2005; Jones et al., 2006). All of the human ST-7 isolates that we have characterized have been serotype Ia, as has the sole ST-84 isolate (Bohnsack et al., 2008). Two ST-7, serotype V strains were isolated from neonates in a recent series of human isolates from Sweden (Luan et al., 2005), and a single non-typable ST-7 was reported in a series of isolates largely collected in the USA (Ramaswamy et al., 2006). The two ST-6 isolates from the USA that we described previously were both serotype Ib (Bohnsack et al., 2008; Seifert et al., 2006), as was the single ST-6 GBS isolate from the UK reported by Jones et al. (2003). Bisharat et al. (2005) described five ST-6 isolates in a sample from Israel, four of which were serotype Ib and one of which was serotype III. Jones et al. (2003) described nine human isolates in CC 6, five of which were ST-7, three ST-6 and one ST-89. Five of these were associated with invasive disease, but the serotype was not provided for these isolates. It cannot be determined from the available data whether CC 7 GBS isolates will be similar to most of the other GBS clonal complexes and will comprise strains with a predominant serotype, or whether they will be more heterogeneous (Bohnsack et al., 2008; Jones et al., 2003; Luan et al., 2005).
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Fig. 2. Clonal complexes of the fish, dolphin, human and bovine STs characterized in this study in comparison with previously characterized human and bovine GBS STs (Bohnsack et al., 2008) using the eBurst software program.
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All of the other piscine isolates causing epizootics from four different geographical regions (Brazil, Israel, USA and Honduras) had STs not previously deposited in the MLST database. The STs of these isolates were quite dissimilar from the STs of human and bovine isolates, including ST-7, and eBurst did not cluster these five novel STs with any of the STs from the human or bovine sample. The five novel piscine STs also did not cluster into a single clonal complex, despite the appearance of genetic relatedness that could be surmised from the number of shared alleles in the non-ST-7 strains (Table 2). Nonetheless, the six piscine isolates with the five novel STs were similar in that they all lacked β-haemolysis and CAMP factor (Table 1), phenotypic properties that are almost always present in human GBS isolates (Facklam et al., 1974). In addition, the non-ST-7 fish isolates fermented trehalose and hydrolysed arginine less often than the fish, dolphin and human ST-7 isolates (Table 1). ATCC 51487, the isolate originally designated S. difficilis, is one of these non-ST-7 GBS and was described previously as ST-246 (Tettelin et al., 2005). We determined the ST of ATCC 51487 to be ST-261, which is identical to ST-246 except for a deletion in the adhP amplicon. The ATCC isolate may have acquired the deletion during passage, been overlooked by previous authors or had replicate errors made during sequencing. MLST confirmed the divergence of ATCC 51487 from most human and bovine GBS isolates, as previously proposed by Vandamme et al. (1997) based on comparisons of whole-cell protein patterns identified by PAGE among isolates from various streptococcal species. MLST also corroborated the genomic drift of ATCC 51487 from human, bovine and other mammalian GBS described by Brochet et al. (2006). It is possible that these non-ST-7 isolates belong to a broadly related group of GBS that is distributed worldwide and is capable of causing fish epidemics, but the available evidence indicates that strains from the non-ST-7 piscine isolates rarely, if ever, colonize or infect humans.
Whilst fish have previously been identified as a host for GBS, the population structure of piscine GBS has not been investigated. The data presented here demonstrate that at least two divergent populations of GBS are capable of causing epizootics in fish, and that one of these populations is also capable of causing human infections, although rarely and apparently in restricted geographical areas. These findings raise the possibility that humans or dolphins were the source of the Kuwait epizootic and, conversely, that ST-7, serotype Ia GBS may be a zoonosis. Comparative genomics of piscine, human and bovine GBS could help clarify those genes important for host tropism and for the emergence of unique pathogenic clones, and whether these hosts act as reservoirs for one another's pathogenic lineages.
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ACKNOWLEDGEMENTS
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We thank Nicole Jones, Nuffield Department of Clinical Laboratory Sciences and Paediatric Molecular Medicine, Institute for Molecular Medicine, John Radcliffe Hospital, Oxford, UK, for the assignment of ST numbers to GBS fish alleles. We acknowledge the following individuals for providing GBS strains: Dr John Hawke, Louisiana Veterinary Diagnostic Laboratory, Louisiana State University, Baton Rouge, LA, USA; Dr Dina Zilberg, The Albert Katz Department of Dryland Biotechnologies, Ben-Gurion University of the Negev, Israel; and Dr Salvador, Parana State, Brazil. We also thank Crystal Baden, Paige Mumma and Dr David J. Pasnik, US Department of Agriculture (USDA), Agricultural Research Service, Aquatic Animal Health Research Laboratories, Chestertown, MD, USA, for technical assistance and Lisa Biggar for editing the manuscript. This work was supported by a grant (to J. F. B.) from the Thrasher Research Fund. Mention of trade names does not imply recommendation or endorsement by the USDA.
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References
|
|---|
Baya, A. M., Lupiani, B., Hetrick, F. M., Roberson, B. S., Lukacovic, R., May, E. & Poukish, C. (1990). Association of Streptococcus sp. with fish mortalities in the Chesapeake Bay and its tributaries. J Fish Dis 13, 251–253.[CrossRef]
Bisharat, N., Crook, D. W., Leigh, J., Harding, R. M., Ward, P. N., Coffey, T. J., Maiden, M. C., Peto, T. & Jones, N. (2004). Hyperinvasive neonatal group B streptococcus has arisen from a bovine ancestor. J Clin Microbiol 42, 2161–2167.[Abstract/Free Full Text]
Bisharat, N., Jones, N., Marchaim, D., Block, C., Harding, R. M., Yagupsky, P., Peto, T. & Crook, D. W. (2005). Population structure of group B streptococcus from a low-incidence region for invasive neonatal disease. Microbiology 151, 1875–1881.[Abstract/Free Full Text]
Bohnsack, J. F., Whiting, A. A., Martinez, G., Jones, N., Adderson, E. E., Detrick, S., Blashchke-Bonkowsky, A. J., Bisharat, N. & Gottschalk, M. (2004). Serotype III Streptococcus agalactiae from bovine milk and human neonatal infections. Emerg Infect Dis 10, 1412–1419.[Medline]
Bohnsack, J. F., Whiting, A. A., Gottschalk, M., Dunn, D. M., Weiss, R., Azimi, P. H., Phillips, J. B., Weisman, L. E., Rhoads, G. G. & Lin, F.-Y. C. (2008). Population structure of invasive and colonizing strains of Streptococcus agalactiae from neonates of six US academic centers from 1995–1999. J Clin Microbiol 46, 1285–1291.[Abstract/Free Full Text]
Brochet, M., Couvé, E., Zouine, M., Vallaeys, T., Rusniok, C., Lamy, M.-C., Buchrieser, C., Trieu-Cuot, P., Kunst, F. & other authors (2006). Genomic diversity and evolution within the species Streptococcus agalactiae. Microbes Infect 8, 1227–1243.[CrossRef][Medline]
Brown, J. H. (1939). Double-zone β-hemolytic streptococci: their cultural characteristics, serological grouping, occurrence and pathogenic significance. J Bacteriol 37, 133–144.[Free Full Text]
Davies, H. D., Jones, N., Whittam, T. S., Elsayed, S., Bisharat, N. & Baker, C. J. (2004). Multilocus sequence typing of serotype III group B streptococcus and correlation with pathogenic potential. J Infect Dis 189, 1097–1102.[CrossRef][Medline]
Duremdez, R., Al-Marzouk, A., Qasem, J. A., Al-Harbi, A. & Gharabally, H. (2004). Isolation of Streptococcus agalactiae from cultured silver pomfret, Pampus argenteus (Euphrasen), in Kuwait. J Fish Dis 27, 307–310.[CrossRef][Medline]
Eldar, A., Bejerano, Y. & Bercovier, H. (1994). Streptococcus shiloi and Streptococcus difficile: two new streptococcal species causing a meningoencephalitis in fish. Curr Microbiol 28, 139–143.[Medline]
Elliott, J. A., Facklam, R. R. & Richter, C. B. (1990). Whole-cell protein patterns of nonhemolytic group B, type 1b, streptococci isolated from humans, mice, cattle, frogs, and fish. J Clin Microbiol 28, 628–630.[Abstract/Free Full Text]
Evans, J. J., Klesius, P. H., Glibert, P. M., Shoemaker, C. A., Al Sarawi, M. A., Landsberg, J., Duremdez, R., Al Marzouk, A. & Al Zenki, S. (2002). Characterization of β-haemolytic Group B Streptococcus agalactiae in cultured seabream, Sparus auratus (L.), and wild mullet, Liza klunzingeri (Day), in Kuwait. J Fish Dis 25, 505–513.[CrossRef]
Evans, J. J., Pasnik, D. J., Klesius, P. H. & Al-Ablani, S. (2006). First report of Streptococcus agalactiae and Lactococcus garvieae from a wild bottlenose dolphin (Tursiops truncatus). J Wildl Dis 42, 561–569.[Abstract/Free Full Text]
Facklam, R. R., Padula, J. F., Thacker, L. G., Wortham, E. C. & Sconyers, B. J. (1974). Presumptive identification of group A, B, and D streptococci. Appl Microbiol 27, 107–113.[Medline]
Feil, E. J., Li, B. C., Aanensen, D. M., Hanage, W. P. & Spratt, B. G. (2004). eBurst: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186, 1518–1530.[Abstract/Free Full Text]
Finch, L. A. & Martin, D. R. (1984). Human and bovine group B streptococci: two distinct populations. J Appl Bacteriol 57, 273–278.[Medline]
Gherardi, G., Imperi, M., Baldassarri, L., Pataracchia, M., Alfarone, G., Recchia, S., Orefici, G., Dicuonzo, G. & Creti, R. (2007). Molecular epidemiology and distribution of serotypes, surface proteins, and antibiotic resistance among group B streptococci in Italy. J Clin Microbiol 45, 2909–2916.[Abstract/Free Full Text]
Jones, N., Bohnsack, J. F., Takahashi, S., Oliver, K. A., Chan, M.-S., Kunst, F., Glaser, P., Rusniok, C., Crook, D. W. M. & other authors (2003). Multilocus sequence typing system for group B streptococcus. J Clin Microbiol 41, 2530–2536.[Abstract/Free Full Text]
Jones, N., Oliver, K. A., Barry, J., Harding, R. M., Bisharat, N., Spratt, B. G., Peto, T., Crook, D. W. & , the Oxford Group B Streptococcus Consortium (2006). Enhanced invasiveness of bovine-derived neonatal sequence type 17 group B streptococcus is independent of capsular serotype. Clin Infect Dis 42, 915–924.[CrossRef][Medline]
Kawata, K., Anzai, T., Senna, K., Kikuchi, N., Ezawa, A. & Takahashi, T. (2004). Simple and rapid PCR method for identification of streptococcal species relevant to animal infections based on 23S rDNA sequence. FEMS Microbiol Lett 237, 57–64.[CrossRef][Medline]
Kumar, S., Tamura, K. & Nei, M. (2004). MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5, 150–163.[Abstract/Free Full Text]
Lin, F. Y., Whiting, A., Adderson, E., Takahashi, S., Dunn, D. M., Weiss, R., Azimi, P. H., Philips, J. B., III, Weisman, L. E. & other authors (2006). Phylogenetic lineages of invasive and colonizing strains of serotype III group B streptococci from neonates: a multicenter prospective study. J Clin Microbiol 44, 1257–1261.[Abstract/Free Full Text]
Luan, S. L., Granlund, M., Sellin, M., Lagergard, T., Spratt, B. G. & Norgren, M. (2005). Multilocus sequence typing of Swedish invasive group B streptococcus isolates indicates a neonatally associated genetic lineage and capsule switching. J Clin Microbiol 43, 3727–3733.[Abstract/Free Full Text]
MacFaddin, J. F. (2000). Biochemical Tests for Identification of Medical Bacteria, 3rd edn. Philadelphia, PA: Lippincott Williams & Wilkins.
Martinez, G., Harel, J., Higgins, R., LaCouture, S., Daignault, D. & Gottschalk, M. (2000). Characterization of Streptococcus agalactiae isolates of bovine and human origin by randomly amplified polymorphic DNA analysis. J Clin Microbiol 38, 71–78.[Abstract/Free Full Text]
Martins, E. R., Pessanha, M. A., Ramirez, M. & Melo-Cristino, J. (2007). Analysis of group B streptococcal isolates from infants and pregnant women in Portugal revealing two lineages with enhanced invasiveness. J Clin Microbiol 45, 3224–3229.[Abstract/Free Full Text]
Nagano, Y., Nagano, N., Takahashi, S., Murono, K., Fujita, K., Taguchi, F. & Okuwaki, Y. (1991). Restriction endonuclease digest patterns of chromosomal DNA from group B β-haemolytic streptococci. J Med Microbiol 35, 297–303.[Abstract/Free Full Text]
Nagano, N., Nagano, Y. & Taguchi, F. (2002). High expression of a C protein β antigen gene among invasive strains from certain clonally related groups of type Ia and Ib group B streptococci. Infect Immun 70, 4643–4649.[Abstract/Free Full Text]
Oliveira, I. C., de Mattos, M. C., Pinto, T. A., Ferreira-Carvalho, B. T., Benchetrit, L. C., Whiting, A. A., Bohnsack, J. F. & Figueiredo, A. M. (2006). Genetic relatedness between group B streptococci originating from bovine mastitis and a human group B streptococcus type V cluster displaying an identical pulsed-field gel electrophoresis pattern. Clin Microbiol Infect 12, 887–893.[CrossRef][Medline]
Pattison, I. H., Matthews, P. R. J. & Howell, D. G. (1955). The type classification of group B streptococci, with special reference to bovine strains apparently lacking in type polysaccharide. J Pathol Bacteriol 69, 51–60.[Medline]
Plumb, J. A., Schachte, J. H., Gaines, J. L., Peltier, W. & Carroll, B. (1974). Streptococcus sp. from marine fishes along the Alabama and Northwest Florida coast of the Gulf of Mexico. Trans Am Fish Soc 103, 358–361.[CrossRef]
Poyart, C., Tazi, A., Réglier-Poupet, H., Billoët, A., Tavares, N., Raymond, J. & Trieu-Cuot, P. (2007). Multiplex PCR assay for rapid and accurate capsular typing of group B streptococci. J Clin Microbiol 45, 1985–1988.[Abstract/Free Full Text]
Ramaswamy, S. V., Ferrieri, P., Flores, A. E. & Paoletti, L. C. (2006). Molecular characterization of nontypable group B streptococcus. J Clin Microbiol 44, 2398–2403.[Abstract/Free Full Text]
Robinson, J. A. & Meyer, F. P. (1966). Streptococcal fish pathogen. J Bacteriol 92, 512[Free Full Text]
Salvador, R., Muller, E. E., de Freitas, J. C., Leonhadt, J. H., Pretto-Giordano, L. G. & Dias, J. A. (2005). Isolation and characterization of Streptococcus spp. group B in Nile tilapias (Oreochromis niloticus) reared in hapas nets and earth nurseries in the northern region of Parana State, Brazil. Ciência Rural Santa Maria 35, 1374–1378.
Schuchat, A. (1998). Epidemiology of group B streptococcal disease in the United States: shifting paradigms. Clin Microbiol Rev 11, 497–513.[Abstract/Free Full Text]
Seifert, K. N., Adderson, E. E., Whiting, A., Bohnsack, J. F., Crowley, P. J. & Brady, L. J. (2006). A unique serine-rich repeat protein (Srr-2) and novel surface antigen (epsilon) associated with a virulent lineage of serotype III Streptococcus agalactiae. Microbiology 152, 1029–1040.[Abstract/Free Full Text]
Suanyuk, N., Kanghear, H., Khongpradit, R. & Supamattaya, K. (2005). Streptococcus agalactiae infection in tilapia (Oreochromis niloticus). Songklanakarin J Sci Technol Aquat Sci 27, 307–319.
Sukhnanand, S., Dogan, B., Ayodele, M. O., Zadoks, R. N., Craver, M. P. J., Dumas, N. B., Schukken, Y. H., Boor, K. J. & Wiedmann, M. (2005). Molecular subtyping and characterization of bovine and human Streptococcus agalactiae isolates. J Clin Microbiol 43, 1177–1186.[Abstract/Free Full Text]
Takahashi, S., Detrick, S., Whiting, A. A., Blaschke-Bonkowksy, A. J., Aoyagi, Y., Adderson, E. E. & Bohnsack, J. F. (2002). Correlation of phylogenetic lineages of group B streptococci, identified by analysis of restriction-digestion patterns of genomic DNA, with infB alleles and mobile genetic elements. J Infect Dis 186, 1034–1038.[CrossRef][Medline]
Tettelin, H., Masignani, V., Cieslewicz, M. J., Donati, C., Medini, D., Ward, N. L., Angiuoli, S. V. & Crabtree, J. (2005). Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". Proc Natl Acad Sci U S A 102, 13950–13955.[Abstract/Free Full Text]
Vandamme, P., Devriese, L. A., Pot, B., Kersters, K. & Melin, P. (1997). Streptococcus difficile is a nonhemolytic group B, type Ib streptococcus. Int J Syst Bacteriol 47, 81–85.[Abstract/Free Full Text]
Wilkinson, H. W. (1978). Analysis of group B streptococcal types associated with disease in human infants and adults. J Clin Microbiol 7, 176–179.[Abstract/Free Full Text]
Wilkinson, H. W., Thacker, L. G. & Facklam, R. R. (1973). Nonhemolytic group B streptococci of human, bovine, and ichthyic origin. Infect Immun 7, 496–498.[Abstract/Free Full Text]
Zappulli, V., Mazzariol, S., Cavicchiolo, L., Petterino, C., Bargelloni, L. & Castagnaro, M. (2005). Fatal necrotizing fasciitis and myositis in a captive common bottlenose dolphin (Tursiops truncatus) associated with Streptococcus agalactiae. J Vet Diagn Invest 17, 617–622.[Abstract/Free Full Text]
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