Genetic Relationships between Clinical Isolates of Streptococcus pneumoniae, Streptococcus oralis, and Streptococcus mitis: Characterization of "Atypical" Pneumococci and Organisms Allied to S. mitis Harboring S. pneumoniae Virulence Factor-Encoding Genes

doi:10.1128/IAI.68.3.1374-1382.2000

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Infection and Immunity, March 2000, p. 1374-1382, Vol. 68, No. 3
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Genetic Relationships between Clinical Isolates of Streptococcus pneumoniae, Streptococcus oralis, and Streptococcus mitis: Characterization of "Atypical" Pneumococci and Organisms Allied to S. mitis Harboring S. pneumoniae Virulence Factor-Encoding Genes

Adrian M. Whatmore,¹^,^* Androulla Efstratiou,² A. Paul Pickerill,¹ Karen Broughton,² Geoffrey Woodard,¹ Daniel Sturgeon,¹ Robert George,² and Christopher G. Dowson¹

Department of Biological Sciences, University of Warwick, Coventry, CV4 7AL,¹ and Respiratory and Systemic Infection Laboratory, Central Public Health Laboratory, London, NW9 5HT,² United Kingdom

Received 25 August 1999/Returned for modification 17 September 1999/Accepted 10 November 1999

The oral streptococcal group (mitis phylogenetic group) currently consists of nine recognized species, although the grouphas been traditionally difficult to classify, with frequent changesin nomenclature over the years. The pneumococcus (Streptococcuspneumoniae), an important human pathogen, is traditionally distinguishedfrom the most closely related oral streptococcal species Streptococcusmitis and Streptococcus oralis on the basis of three differentiatingcharacteristics: optochin susceptibility, bile solubility, andagglutination with antipneumococcal polysaccharide capsule antibodies.However, there are many reports in the literature of pneumococcilacking one or more of these defining characteristics. Sometimescalled "atypical" pneumococci, these isolates can be the sourceof considerable confusion in the clinical laboratory. Little isknown to date about the genetic relationships of such organismswith classical S. pneumoniae isolates. Here we describe theserelationships based on sequence analysis of housekeeping genesin comparison with previously characterized isolates of S. pneumoniae,S. mitis, and S. oralis. While most pneumococci were found torepresent a closely related group these studies identified a subgroupof atypical pneumococcal isolates (bile insoluble and/or "acapsular")distinct from, though most closely related to, the "typical" pneumococcalisolates. However, a large proportion of isolates, found to beatypical on the basis of capsule reaction alone, did group withtypical pneumococci, suggesting that they have either lost capsuleproduction or represent as-yet-unrecognized capsular types. Incontrast to typical S. pneumoniae, isolates phenotypically identifiedas S. mitis and S. oralis, which included isolates previouslycharacterized in taxonomic studies, were genetically diverse.While most of the S. oralis isolates did fall into a well-separatedgroup, S. mitis isolates did not cluster into a well-separatedgroup. During the course of these studies we also identified anumber of potentially important pathogenic isolates, which werefrequently associated with respiratory disease, that phenotypicallyand genetically are most closely related to S. mitis but whichharbor genes encoding the virulence determinants pneumolysin andautolysin classically associated with S. pneumoniae.

^* Corresponding author. Mailing address: Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UnitedKingdom. Phone: 44-2476-528359. Fax: 44-2476-523701. E-mail: a.m.whatmore{at}warwick.ac.uk.

Infection and Immunity, March 2000, p. 1374-1382, Vol. 68, No. 3
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

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