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Phylogenetic Analysis of Prevotella Nigrescens, Prevotella Intermedia

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Phylogenetic Analysis of Prevotella Nigrescens, Prevotella Intermedia International Journal of Systematic and Evolutionary Microbiology (2002), 52, 1391–1395 DOI: 10.1099/ijs.0.02021-0 Phylogenetic analysis of Prevotella nigrescens, NOTE Prevotella intermedia and Porphyromonas gingivalis clinical strains reveals a clear species clustering Institute of Veterinary Peter Kuhnert,1 Joachim Frey,1 Niklaus P. Lang2 and Lisa Mayfield2 Bacteriology1 and School of Dental Medicine2 , University of Bern, Switzerland Author for correspondence: Peter Kuhnert. Tel: j41 31 6312485. Fax: j41 31 6312634. e-mail: peter.kuhnert!vbi.unibe.ch Prevotella nigrescens, Prevotella intermedia and Porphyromonas gingivalis are oral pathogens from the family Bacteroidaceae, regularly isolated from cases of gingivitis and periodontitis. In this study, the phylogenetic variability of these three bacterial species was investigated by means of 16S rRNA (rrs) gene sequence comparisons of a set of epidemiologically and geographically diverse isolates. For each of the three species, the rrs gene sequences of 11 clinical isolates as well as the corresponding type strains was determined. Comparison of all rrs sequences obtained with those of closely related species revealed a clear clustering of species, with only a little intraspecies variability but a clear difference in the rrs gene with respect to the next related taxon. The results indicate that the three species form stable, homogeneous genetic groups, which favours an rrs-based species identification of these oral pathogens. This is especially useful given the 7% sequence divergence between Prevotella intermedia and Prevotella nigrescens, since phenotypic distinction between the two Prevotella species is inconsistent or involves techniques not applicable in routine identification. Keywords: phylogeny, variation, 16S rRNA, oral pathogens The periodontal pocket provides a unique habitat for parison, these periodontal pathogens are found rela- over 500 species of micro-organisms. These micro- tively infrequently and at low proportions within organisms are organized in a biofilm such that specific plaque samples from periodontally healthy individ- groups of bacteria are associated with one another in uals. Further evidence of the role of these pathogens complexes (Socransky et al., 1988). It is evident that a in destructive periodontal disease is provided by limited number of species of the oral microflora are studies demonstrating that the treatment aimed at associated with periodontal disease and may be identi- suppression of these species results in clinical im- fied in high proportions at sites with periodontal provement registered as reduced bleeding, reduced inflammation and destruction (Slots et al., 1986; Dzink pocket depth and gains in probing attachment level et al., 1988). (Slots et al., 1985; van Winkelhoff et al., 1988; Loos et al., 1988; Renvert et al., 1990). Microbial monitoring Prevotella intermedia and Porphyromonas gingivalis in dental practice may be an adjunct to diagnosis, are frequently isolated from subgingival plaque of choice of therapy, treatment evaluation, and risk individuals with periodontal disease. Prevotella nigres- evaluation and prognosis (Greenstein, 1988; Listgar- cens has been found to occur less frequently in ten, 1988; Maiden et al., 1990). Thus, a simple, reliable periodontal sites compared with Prevotella intermedia and reproducible method for identification of the (Dahlen et al., 1990; Haffajee et al., 1992). In com- bacterial species is desirable. ................................................................................................................................................. The three periodontal pathogens investigated in this Published online ahead of print on 28 January 2002 as DOI 10.1099/ study are all from the family Bacteroidaceae. Por- ijs.0.02021-0. phyromonas gingivalis (formerly Bacteroides gingivalis) The GenBank accession numbers for the 16S rRNA sequences from the has been recognized for some time as a single species family Bacteroidaceae are listed in Table 1. and can be relatively easily identified by phenotypic 02021 # 2002 IUMS Printed in Great Britain 1391 P. Kuhnert and others Table 1. List of strains used for rrs gene sequence comparison Strain* Original name Geographical origin† Clinical origin‡ Accession no. Porphyromonas gingivalis Type strain ATCC 33277T ATCC Gingival sulcus AF414809 1-PGI OMGS 945 Sweden Periodontitis AF414810 2-PGI OMGS 2101 Kenya Periodontitis AF414811 3-PGI PFG 83 Indonesia AF414812 40-PGI OMGS 716 Sweden AF414813 42-PGI OMGS 789 Sweden AF414814 25-PGI P02-2 Switzerland Periodontitis AF414815 26-PGI P06-2 Switzerland Periodontitis AF414816 27-PGI P06-3 Switzerland Periodontitis AF414817 28-PGI P10-1 Switzerland Periodontitis AF414818 29-PGI P11-6rough Switzerland Periodontitis AF414819 30-PGI P12-1 Switzerland Periodontitis AF414820 Prevotella intermedia Type strain ATCC 25611T ATCC Empyema AF414821 5-PIN MH 7 UK AF414822 6-PIN MH 16 UK AF414823 32-PIN HG 1674 The Netherlands AF414824 35-PIN OMGS 874 Sweden Periodontitis AF414825 36-PIN OMGS 1277 Sweden Periodontitis AF414826 10-PIN P02-1 Switzerland Periodontitis AF414827 15-PIN P05-6 Switzerland Periodontitis AF414828 16-PIN P05-7 Switzerland Periodontitis AF414829 22-PIN P09-14 Switzerland Periodontitis AF414830 23-PIN P09-15 Switzerland Periodontitis AF414831 24-PIN P09-16 Switzerland Periodontitis AF414832 Prevotella nigrescens Type strain ATCC 33563T UK Gingivitis AF414833 7-PNIG MHS 1-18 Denmark Periodontitis AF414834 8-PNIG MH 20 UK AF414835 9-PNIG MH 11 UK AF414836 31-PNIG HG 1672 The Netherlands AF414837 37-PNIG OMGS 865 Sweden AF414838 11-PNIG P03-2 Switzerland Periodontitis AF414839 13-PNIG P04-4 Switzerland Periodontitis AF414840 17-PNIG P06-9 Switzerland Periodontitis AF414841 18-PNIG P07-10 Switzerland Periodontitis AF414842 20-PNIG P08-12 Switzerland Periodontitis AF414843 21-PNIG P08-13 Switzerland Periodontitis AF414844 * Strain acronyms: PGI for Porphyromonas gingivalis, PIN for Prevotella intermedia, PNIG for Prevotella nigrescens. † ATCC, American Type Culture Collection, Manassas, VA, USA. ‡ The strains were isolated from human individuals; , not determined. means (Krieg & Holt, 1984). Prevotella intermedia is groups representing the two species (Frandsen et al., an anaerobic, black-pigmented, Gram-negative rod 1995). and was recently split into two distinct species – Prevotella intermedia and Prevotella nigrescens –on Several methods have since been utilized to distinguish the basis of biochemical and DNA reassociation Prevotella intermedia from Prevotella nigrescens in the studies (Shah & Gharbia, 1992). The two species were clinical laboratory, with varying reliability. Phenotypic later confirmed by a polyphasic approach including identification and discrimination of Prevotella nigres- multilocus enzyme electrophoresis, ribotyping, and cens and Prevotella intermedia based on lipase pro- SDS-PAGE profiles. These different approaches car- duction, as originally described by Shah & Gharbia ried out with a representative sample number of (1992), proved to be problematic and was not repro- isolates produced clustering in the same two distinct ducible in different laboratories (Frandsen et al., 1995). 1392 International Journal of Systematic and Evolutionary Microbiology 52 Phylogeny of Prevotella and Porphyromonas spp. Table 2. PCR and sequencing primers used for rrs amplification and sequence determination ..................................................................................................................................................................................................................................... The optimized primer set was adapted from Kuhnert et al. (1996). Name Sequence Position* 16SUNI-L AGAGTTTGATCATGGCTCAG 8–27 16SUNI-R GTGTGACGGGCGGTGTGTAC 1410–1391 16SRNAI-S CTACGGGAGGCAGCAGTGGGG 341–361 16SRNA1-S CTACGGGAGGCAGCAGTGAGG 341–361 16SRNAII-S GTGTAGCGGTGAAATGCGTAG 682–702 16SRNA2-S GTGTAGGGGTAAAATCCGTAG 682–702 16SRNAIV-S GGTTAAGTCCCGCAACGAGCGC 1087–1108 16SRNA4-S GCTTAAGTGCCATAACGAGCGC 1087–1108 16SRNAV-S CCCCACTGCTGCCTCCCGTAG 361–341 16SRNAVI-S CTACGCATTTCACCGCTACAC 702–682 16SRNA6-S CTACGGATTTTACCCCTACAC 702–682 16SRNAVIII-S GCGCTCGTTGCGGGACTTAACC 1108–1087 16SRNA8-S GCGCTCGTTATGGCACTTAAGC 1108–1087 * Relative to the Escherichia coli sequence (J01859). The usefulness of separation of whole-cell proteins by of the rrs gene and to evaluate published PCR assays, SDS-PAGE was also questioned (Premaraj et al., we carried out a study on the rrs gene sequences of 1999), and the ultimate comparison of genomic DNA clinical isolates of the three species Porphyromonas is time-consuming. Therefore, to distinguish the two gingivalis, Prevotella intermedia and Prevotella nigres- species, several methods are normally used in parallel. cens in comparison to their corresponding type A simple and robust identification method, however, is strains. For that purpose, we selected a representative needed for the clinical laboratory. sample of different geographically and epidemiologi- cally unrelated strains. They are listed in Table 1 and Paster et al. (1994) did a comprehensive study to included strains from individual patients, with perio- determine the phylogenetic relationships within the dontal disease, from Sweden, the UK, Denmark, The family Bacteroidaceae, using sequence analysis of the Netherlands, Kenya, Indonesia and Switzerland. In 16S rRNA. They found Porphyromonas gingivalis in addition, the type strains of the three species were the Porphyromonas cluster, and Prevotella intermedia
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