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Evaluation of the Hypervariable Region in the 16S Rdna Sequence As an Index for Rapid Species Identification in the Genus Paenibacillus

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Evaluation of the Hypervariable Region in the 16S Rdna Sequence As an Index for Rapid Species Identification in the Genus Paenibacillus J. Gen. Appl. Microbiol., 48, 281–285 (2002) Short Communication Evaluation of the hypervariable region in the 16S rDNA sequence as an index for rapid species identification in the genus Paenibacillus Keiichi Goto,* Yuko Kato, Mika Asahara, and Akira Yokota1 Microbiological & Analytical Group, Food Research Laboratories, Mitsui Norin Co., Ltd., Fujieda 426–0133, Japan 1 Institute of Molecular and Cellular Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo 113–0032, Japan (Received January 9, 2002; Accepted August 29, 2002) Key Words——Bacillus; grouping; hypervariable region; identification; Paenibacillus; 16S rRNA gene The genus Paenibacillus (Ash et al., 1993) compris- additional strains of Paenibacillus species were sub- ing aerobic or facultatively anaerobic endospore-form- jected to a sequence comparison of the HV regions ing bacilli is represented by rRNA group 3 and con- and the use of this HV region for molecular typing of tains 28 validated species and 2 subspecies. The the various species of the genus Paenibacillus was genus is phenotypically similar to other members of evaluated. the family Bacillaceae but is difficult to distinguish from The 59 strains used in this study were obtained from the other genera by morphology alone. Recently a ATCC (American Type Culture Collection, Manassas, highly specific primer set directed to the 16S rDNA of VA, USA), DSM (Deutsche Sammlung von Mikroor- Paenibacillus was described (Shida et al., 1997), ganismen und Zellkulturen GmbH, Braunschweig, Ger- which enabled the rapid identification of Paenibacillus many), IAM (Institute of Molecular and Cellular Bio- to the genus level. However the identification of Paeni- sciences, The University of Tokyo, Tokyo, Japan), IFO bacillus below the genus level remains difficult and (Institute for Fermentation, Osaka, Japan) and NCIMB time-consuming due to the absence of well-defined (National Collection of Industrial and Marine Bacteria, phenotypes that differentiate species (Reva et al., Aberdeen, UK). The Paenibacillus strains were culti- 2001). vated by the methods recommended in the ATCC, In our previous studies, we have demonstrated that DSM, IAM, IFO and NCIMB strain catalogues, respec- a hypervariable (HV) region, corresponding to the 5Ј tively. The two newest species, P. azoreducens (Mee- end region of 16S rDNA (nucleotide positions 70 to han et al., 2001) and P. jamilae (Aguilera et al., 2001), 344; Bacillus subtilis numbering), is a useful marker for were not included because these type strains were not the rapid identification and grouping of Alicyclobacillus available for distribution at the time of this study. Ex- species (Goto et al., 2002b, c) and Bacillus species traction and purification of genomic DNA, sequencing (Goto et al., 2000). In this study, 28 type strains and 31 of the 16S rDNA and HV region, and phylogenetic analysis were performed as described in our previous papers (Goto et al., 2000, 2002a, b). Sequences deter- * Address reprint requests to: Dr. Keiichi Goto, Microbiological & Analytical Group, Food Research Laboratories, Mitsui Norin mined during the present work have been deposited in Co., Ltd., 223–1 Miyahara, Fujieda 426–0133, Japan. the DNA data bank of Japan (DDBJ) under the acces- E-mail: [email protected] sion numbers AB073186 to AB073206 and AB073362 282 GOTO et al. Vol. 48 to AB073364. The accession numbers of 16S rDNA the type strain of each species (Fig. 1). Relatedness sequences used in this study are as follows: Alicy- between these strains was further supported by high clobacillus acidocaldarius ATCC 27009T, AB042056; DNA-DNA reassociation values (Table 1). On the basis Bacillus subtilis IAM 12118T, AB042061; Paenibacillus of the comparative sequence analysis, the strains of P. dendritiformis BGSC 30A1T, AJ131119; Paenibacillus apiarius (group C), P. azotofixans (group B) and P. granivorans A30T, AF237682; Paenibacillus koreensis validus (group E) could be readily distinguished from YC300T, AB130254; Paenibacillus polymyxa IAM phylogenetically related Paenibacillus species. 13419T, AB042063. DNA-DNA reassociation experi- Strains of P. thiaminolyticus tested could be distin- ment was carried out as described by Ezaki et al. guished from type strains of phylogenetically related P. (1989) using photobiotin-labelled DNA probes in mi- lentimorbus and P. popilliae with 7 and 8 nucleotide croplate format and a CytoFluor series 4000TC (Ap- differences, respectively, although these differences plied Biosystems, Branchburg, NJ, USA). Phenotypic were not reflected on the phylogenetic dendrogram characterization was carried out by API 20E and API (Fig. 1) because these informative positions were 50CH (bioMerieux, Marcy l’Etoile). deleted by gap removal to create the final data set to In order to ascertain the most informative region of be used for subsequent phylogenetic calculations. On the 16S rDNA among Paenibacillus species, a multiple the other hand, insect pathogens P. lentimorbus and P. sequence alignment was performed using the almost popilliae are closely related species (Klein and Kaya, complete 16S rDNA sequences from 28 type strains of 1995; Rippere et al., 1998; Pettersson et al., 1999), 26 species and 2 subspecies of the genus Paenibacil- but the HV region sequence of P. lentimorbus ATCC lus. The results showed that sequence similarity val- 14707T was different to that of P. popilliae ATCC ues of the V1 and V2 variable regions (Gray et al., 14706T at 8 nucleotide positions. Interestingly, P. thi- 1984; Neefs et al., 1993) among type strains were 0% aminolyticus IFO 15656T showed low-intermediate and 25%, respectively, and these values were clearly 40% and 45% DNA-DNA reassociation values to P. lower than those of the V3–V9 variable regions lentimorbus ATCC 14707T and P. popilliae ATCC (56–90%). Other regions, other than the V1–V9 vari- 14706T (Table 1), respectively. Moreover, DNA-DNA able regions in 16S rDNA, were also highly conserved. reassociation experiments and RAPD analysis by Rip- Thus the 5Ј region of the gene, including the V1 and pere et al. (1998) have revealed a close genetic rela- V2 region which corresponds to the hypervariable re- tionship between P. lentimorbus and P. popilliae gion (positions 70–344) of Alicyclobacillus and (45–66% DNA-DNA reassociation values) and the ex- Bacillus, was the most informative region common to istence of two groups within the respective species. all type strains of Paenibacillus. Except for the case From the above observations, these three species between P. larvae subsp. larvae and P. larvae subsp. may be in subspecific relation to each other, and fur- pulvifaciens (100% 16S rDNA sequence identity), the ther studies with more strains and under same experi- mean sequence similarity value for the HV region was mental conditions are necessary to clarify the appropri- 87.7% (rangeϭ78.9–99.6%), which was significantly ate taxonomic positions of these species and intraspe- lower than that of the almost complete 16S rDNA (av- cific group. erageϭ94.0%, rangeϭ91.0–99.6%). Therefore the HV Strains of P. polymyxa were subdivided into two region was found to be specific for individual type groups, A-1 and A-2, based on a single nucleotide dif- strains, indicating that the HV region could provide a ference at position 212 (group A-1: G and group A-2: useful index to differentiate Paenibacillus species. A), and the sequences of group A-1 were identical to Next, to confirm the conservation of the HV region that of P. polymyxa IAM 13419T while the sequences within a species, we extracted genomic DNAs from 31 of group A-2 were identical to that of P. peoriae IFO authentic strains representing 6 Paenibacillus species 15541T (group A-3). The type strain of P. peoriae, IFO (P. apiarius, P. azotofixans, P. peoriae, P. polymyxa, P. 15541T (group A-3), showed 16S rDNA sequence sim- thiaminolyticus and P. validus; Fig. 1) and sequenced ilarity values of 99.6% and 99.7% with the reference the amplified HV region. Comparative sequence analy- strains of P. polymyxa IAM 13419T (group A-1) and P. sis of the HV region revealed that strains of P. apiarius, polymyxa DSM 292 (group A-2). Group A-1 strains P. azotofixans, P. peoriae, P. thiaminolyticus and P. had DNA-DNA reassociation values between 87 to validus tested possessed 100% sequence similarity to 99% when tested against P. polymyxa IAM 13419T. 2002 Molecular identification of Paenibacillus species 283 Fig. 1. Phylogenetic dendrogram of Paenibacillus species, inferred from sequences of the HV region. The dendrogram, constructed using the neighbor-joining method, were based on a comparison of 229 nt. Alicy- clobacillus acidocaldarius ATCC 27009T was used as the outgroup. Bootstrap values (expressed as percentage of 1,000 replications) greater than 70% are shown at the branch points. Group A-2 strains showed 89 to 99% relatedness with production from carbohydrates and could not be differ- the group A-2 reference strain DSM 292. Reciprocal entiated phenotypically (data not shown). Furthermore, pairings between group A-1 and A-2 strains gave DNA previous polyphasic taxonomic studies suggested that reassociation values of 65 to 75%. Moreover, DNA re- P. peoriae was phenotypically closely related to P. association values of 40 to 53% were measured be- polymyxa and could only be distinguished by a small tween P. peoriae IFO 15541T (group A-3) and strains number of tests (Heyndrickx et al., 1996; Montefusco of either group A-1 or A-2. On the other hand, group A- et al., 1993; Nakamura, 1987). Accordingly, these ob- 1 and A-2 showed typical characteristics of P. servations indicated that P. polymyxa group A-1, P. polymyxa with some intraspecific variations for acid polymyxa group A-2 and P. peoriae cluster tightly to- 284 GOTO et al. Vol. 48 Table 1. DNA-DNA reassociation values. Table 1. Continued. DNA-DNA reassociation (%) with: DNA-DNA reassociation (%) with: Strains Strains T T T T T T T T T T T T IAM 13419 DSM 292 IFO 15541 DSM 5976 DSM 5581 IFO 15656 JCM 9077 IAM 13419 DSM 292 IFO 15541 DSM 5976 DSM 5581 IFO 15656 JCM 9077 Group A-1 P.
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