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Departamento de Biotecnología, Instituto de Agroquímica y Tecnología de Alimentos (CSIC), Apartado de Correos 73, 46100 – Burjassot, Valencia, Spain
Correspondence
Gaspar Pérez-Martínez
gaspar.perez{at}iata.csic.es
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The GenBank accession numbers for the partial 23S rDNA sequences of BL 23 and BL 94T are AY112675 and AY112676, respectively; the GenBank accession numbers for the 16S rDNA sequences of BL 23 [ATCC 393 (pLZ15-)] and BL 94T (ATCC 393T) are AF385770 and AF469172, respectively.
Present address: Centro de Investigación en Alimentación y Desarrollo, AC, 83000 Hermosillo, Sonora, Mexico. 
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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; Dellaglio et al., 1975, 1991; Dicks et al., 1996; Collins et al., 1989; Ferrero et al., 1996; Mori et al., 1997; Zhong et al., 1998; Chen et al., 2000; Felis et al., 2001).
L. casei has been used in a number of pioneering studies on the physiology and genetics of the genus Lactobacillus. The type strain L. casei subsp. casei (L. casei) ATCC 393T especially has been used in studies on the fermentation of glucose, lactose, citrate and pyruvate (Hegazi & Abo-Elanga, 1987; Palles et al., 1998), comparative studies on and molecular characterization of the enzyme L-lactate dehydrogenase (Gordon & Doelle, 1976; Hensel et al., 1977; Kim et al., 1991), characterization of an intracellular 
-glucosidase (Coullon et al., 1998), proteolytic activity (Hegazi & Abo-Elanga, 1987) and studies on the composition of the cell wall, antibiotic resistance and adherence factors (Billot-Klein et al., 1997; Pelletier et al., 1997). Also, the isolation and characterization of extrachromosomal genetic elements in the genus Lactobacillus was reported for the first time in strains of L. casei, such as ATCC 393T, 61BG, 64H, ATCC 334, ATCC 4646 and ATCC 15820T (Chassy et al., 1976; Chassy & Giuffrida, 1980; Lee-Wickner & Chassy, 1984, 1985). Flickinger et al. (1986) obtained a number of plasmid-cured derivatives from L. casei strains; among these, an ATCC 393T variant cured of plasmid pLZ15 [ATCC 393 (pLZ15-)], which encodes a lactose permease and -galactosidase, was found (Chassy & Alpert, 1989). Besides the added value of being a derivative of the standing type strain, this plasmid-cured strain showed a great potential for studies on lactose metabolism, as it still carried a second lactose-specific transport and hydrolysis system, the lactose phosphoenolpyruvate : phosphotransferase system (PTS) and a 6-phospho--galactosidase. It was soon shown by the same research laboratory that this strain was amenable to genetic transformation by electroporation (Chassy & Flickinger, 1987). From this point in time, L. casei ATCC 393 (pLZ15-) became widely used in genetic and physiological studies on L. casei and it has been used for the characterization of lactose, glucose, xylose and sorbose transport and metabolism (Hemme et al., 1994; Veyrat et al., 1994; Gosalbes et al., 1997, 1999; Chaillou et al., 1999; Yebra et al., 2000), the characterization of the role of the general components of the PTS and other elements involved in carbon catabolism repression (Monedero et al., 1997; Gosalbes et al., 1997, 1999; Yebra et al., 2000; Viana et al., 2000; Dossonnet et al., 2000), as well as for the design of cloning and integration vectors (Leer et al., 1992; Alvarez et al., 1999; Gosalbes et al., 2000, 2001; Pérez-Arellano et al., 2001) and the characterization of protein secretion (Hols et al., 1997; Maassen et al., 1999).
As mentioned earlier, recent taxonomic studies using wild-type L. casei ATCC 393T have shown this strain to be phylogenetically more closely related to Lactobacillus zeae ATCC 15820T than to most other strains grouped in the L. casei–paracasei phylum (Dellaglio et al., 1975, 1991; Dicks et al., 1996; Collins et al., 1989; Ferrero et al., 1996; Mori et al., 1997; Zhong et al., 1998). The present study was prompted by the observation that, in daily laboratory work, certain differences were found between strain ATCC 393T – directly obtained from public culture collections – and the plasmid-cured derivative ATCC 393 (pLZ15-). Hence, strains of ATCC 393 (pLZ15-) were gathered from the laboratory of Professor B. Chassy and from two other research laboratories, so that they could be compared to four isolates of L. casei ATCC 393T obtained from different culture collections. Recently developed molecular techniques have been applied in this study as part of a polyphasic approach to correctly identify strains of L. casei ATCC 393 (pLZ15-), which are currently in use in many laboratories around the world. This study also constitutes an interesting exercise for comparing the different available rapid molecular techniques and for determining their respective resolving potentials among closely related strains.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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). They were maintained in a 10 % glycerol stock collection at -80 °C and were subcultured in MRS medium (Oxoid) when required.
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. The patterns of sugar fermentation were determined by using the API 50CHL system (BioMérieux) and, as an additional phenotypic test, catalase production was assayed. The Gram stain of the bacterial cells was determined as described by Murray et al. (1994).
DNA extraction.
Cultures were grown overnight at 37 °C in MRS broth. The protocol used for DNA extraction was as described by Veyrat et al. (1999). Purity of DNA was checked by determining the A260/280 value and by agarose gel electrophoresis. Purified DNA was aliquoted and stored at 4 °C. Plasmid DNA extraction was performed according to Anderson & McKay (1983).
Random amplified polymorphic DNA analysis (RAPD).
PCR for RAPD was carried out as described by Veyrat et al. (1999). Four oligonucleotides were used for the RAPD, ArgDei (ACCYTRGAAGGYGGYGATGTB), FAD1 (GGWTTTATCKCAGCWTTGG), ISS1Rev (GGATCCAAGACAACGTTTCAAA) and OPL5 (ACGCAGGCAC). Each reaction was performed in a total volume of 50 µl containing 50 pmol primer, 10 mM each dNTP, 1·0 U Taq DNA polymerase and 1·0xTaq buffer (both DyNAzyme II DNA Polymerase; Finnzymes). For numerical analyses of the banding patterns, photographs of the gels were scanned using an HP ScanJet 5100C scanner (Hewlett Packard) with the HPRSCAN software (Software HP Precision Scan, version 1.01). Digitalized gel images were analysed using TDI Lane Manager 2.1 and ADA (Advanced Dates Analyses) (TDI, SA, Spain, 1996). Numerical analyses of the banding patterns were performed according to Welsh & McClelland (1990), and the similarity coefficient and evolutionary distances were calculated.
Ribotyping.
Total DNA (10 µg) from each strain was digested with EcoRI, HindIII and PstI (GibcoBRL), according to the manufacturer's instructions. To get a good resolution of the hybridization bands, the digested DNA samples were separated by gel electrophoresis in 1xTBE buffer using 0·8 % (w/v) agarose for the EcoRI and HindIII digests and 0·5 % agarose for the PstI digest. DNA fragments were transferred to nylon membranes (Hybond+; Amersham-Pharmacia Biotech) by the capillary blot procedure (Sambrook et al., 1989). The hybridization probe was obtained by amplification of the 16S rDNA from L. casei ATCC 393T with oligonucleotides 27f (AGAGTTTGATCCTGGCTCAG) and 1492r (TACGGCACCTTGTTACGACTT) (Lane, 1991). PCR amplification was carried out in a thermal cycler (REAL) using 30 cycles at 94 °C for 1 min, 55 °C for 45 s and 70 °C for 1·5 min, with a final extension at 70 °C for 10 min. The components of the reaction mixture were the same as described above, but in a final volume of 100 µl. After electrophoresis through a 1·0 % (w/v) agarose gel, the DNA fragment obtained from the PCR was purified using the Gene CleanII Kit (Bio 101). Labelling of the fragment with digoxigenin-11-dUTP, overnight hybridization at 55 °C and immunological detection were carried out using the Random Primed DNA labelling and Detection Kit (Boehringer Mannheim), according to the manufacturer's instructions. Digoxigenin-labelled DNA molecular marker II (Boehringer Mannheim) was used as the size standard.
Amplified rDNA restriction analysis (ARDRA).
16S rDNA from the strains under study was amplified as described above. Aliquots (20 µl) of the amplified DNA were digested with the restriction enzymes AluI and HinfI (GibcoBRL). The bands were then resolved through 2·0 % (w/v) agarose gels using the 1 kb plus DNA ladder (GibcoBRL) as the size standard.
Macrorestriction and PFGE.
DNA isolation by gentle lysis of agarose-embedded bacterial cells and enzyme digests for PFGE were performed according to Tenreiro et al. (1994). For each agarose disc, 10 U AscI, 10 U SfiI and 4U I-CeuI (New England Biolabs) were used. PFGE was performed using the CHEF-MAPPER system (Bio-Rad) with 1·0 % (w/v) agarose gels (Seakem GTG; FMAC) in 0·5xTBE (45 mM Tris, 45 mM boric acid, 1 mM EDTA pH 8·0) at 14 °C. A constant voltage (6 V cm-1) was applied to the system and fragment separation was performed using a two-phase programme. In the first phase, the pulse times increased progressively from 5 to 30 s for 8 h; in the second phase, the pulse times increased from 30 to 90 s for 12 h. The Lambda Ladder PFG Marker and Low Range PFG Marker (New England BioLabs) were used as molecular size markers and were always loaded in at least two lanes flanking the samples in the gels. Gels were stained in ethidium bromide (0·5 µg ml-1 in water) and photographed under UV illumination.
Calculation of the genome sizes.
The mean size of each fragment was estimated from three repetitions, using linear interpolation as proposed by Heath et al. (1992). The presence of double bands was assessed by visual evaluation of the ethidium bromide stain.
Intergenic spacer sequences (ITS1 and ITS2).
Amplification of the intergenic spacer sequence 1 (ITS1), between the 16S and 23S rRNA genes, and intergenic spacer sequence 2 (ITS2), between the 23S and 5S rRNA genes, was carried out according to Nour (1998). The conditions and PCR mixture used to amplify the ITSs were as described above. The fragment corresponding to ITS1 was amplified using primers ITS1f (5'-TGGATCACCTCCTTTCTA-3') and ITS1r (5'-GTGCGCCCTTTATTAACTT-3'), and the fragment corresponding to ITS2 was amplified using primers ITS2f (5'-CTTAACTTCTGTGTTCGGCATG-3') and ITS2r (5'-CTAATAGGTCGAGGACTTGACCAA-3'). PCR products corresponding to both ITSs were separated by electrophoresis through a 1·0 % (w/v) agarose gel and visualized by UV illumination after ethidium bromide staining.
Amplification and sequencing of the complete 16S rDNA and domain I of the 16S and 23S rDNAs.
Complete 16S rDNA was amplified as described above; it was completely sequenced using primers 27f (AGAGTTTGATCCTGGCTCAG), 1492r (TACGGCACCTTGTTACGACTT), 530f (GTGCCAGCMGCCGCGG), 1100r (GGGTTGCGCTCGTTG) and 1114f (GCAACGAGCGCAACCC). Primers used for amplification and sequencing of domain I of the 16S rDNA were 27f and 558r (GTATTACCGCGGCTG); those used for domain I of the 23S rDNA were 22f (CGGTGGATGCCTTGGC) and 559r (CATTMTACAAAAGGYACGC). PCR products were purified by electrophoresis through a 1·2 % (w/v) agarose gel, and the resulting DNA bands were extracted by using GFX PCR DNA and the Gelo Band Purification Kit (Amersham Pharmacia Biotech) according to manufacturer's instructions. All of the DNA fragments were sequenced using a Taq DyeDeoxy Terminator Cycle Sequencing Kit (Applied Biosystems) and an ABI 310 automatic sequencer (Perkin Elmer). The DNAMAN for Windows sequence analysis software (Lynnon BioSoft) was used for sequence assembly; subsequent sequence alignments with sequences retrieved from the NCBI (http://www.ncbi.nlm.nih.gov/), GenBank and the Ribosomal Database Project (RDP) using BLASTN were created using DNAMAN.
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RESULTS AND DISCUSSION |
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-gentibiose, D-tagatose and gluconate. None of them fermented erythritol, D- or L-arabinose, D- or L-xylose, methyl -D-xyloside, rhamnose, dulcitol, inositol, methyl 
-D-mannoside, methyl -D-glucoside, melibiose, inulin, D-raffinose, starch, glycogen, xylitol, D- or L-fucose, D- or L-arabitol, or 5-ketogluconate. However, differences in the fermentation of nine sugars were detected among the seven strains, in addition to differences in their ability to grow at 15 °C and their exopolysaccharide production (Table 2).
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). Other relevant phenotypic differences between the two phenons included faster growth of the plasmid-cured strains at 15 °C and greater exopolysaccharide production by the wild-type strains of L. casei ATCC 393T. These initial results demonstrated the phenotypic heterogeneity between the two groups of strains compared in this work. Further tests were carried out to ascertain the genotypic relatedness or differences between the two phenons. From this point on, the two groups of strains will be simply referred to as ATCC 393T and ATCC 393 (pLZ15-).
Genotypic characterization
Plasmid profile.
This was identical for the group of four ATCC 393T strains and consisted of six bands, which probably corresponded to different plasmid forms and more than one plasmid (Fig. 1). This contrasted with data from Lee-Wickner & Chassy (1985), who reported the presence of a single plasmid in wild-type L. casei ATCC 393T. As expected, strains belonging to the ATCC 393 (pLZ15-) group had no plasmids.
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, the calculated similarity indexes between both groups were different for each oligonucleotide (98·9 % with OPL5; 99 % with FAD1 and ISSRev; 99·6 % with ArgDei). When data from all of the primers were integrated in a single analysis, the similarity index was 99·51 %. As an illustration, Fig. 2 shows the RAPD patterns produced when the primer ISSRev was used for all of the strains. At the taxonomic level, RAPD can be seen to be as discriminative as the phenotypic analysis.
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All of the strains tested produced five hybridization bands when digested with HindIII and four when digested with EcoRI. However, when digested with PstI, five hybridization bands were obtained for the ATCC 393 (pLZ15-) group and four were obtained for the ATCC 393T group. Table 3 shows the estimated mean sizes (kbp) of the hybridizing bands for both groups. Southern blot hybridization studies from different authors have shown that the number of bands of greater than 4·5 kb in length often corresponds to the minimum number of rRNA operons (or rrn alleles) in the genome (Sechi & Daneo-Moore, 1993; Bourget et al., 1993; Moschetti et al., 1997). This would suggest that the ATCC 393 (pLZ15-) group possibly has five copies of the rrn genes and that the ATCC 393T group has four copies of the rrn genes.
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) and were used to calculate the genome sizes for the two groups of strains. When the DNA of the ATCC 393T strains was digested with SfiI, the estimated size of the genome was much greater than that obtained with AscI and I-CeuI. These results were observed repeatedly, indicating that only a partial digestion was occurring with SfiI; for this reason the SfiI data were not considered in the calculations. A similar phenomenon has been reported when other enzymes have been used to digest L. casei (Ferrero et al., 1996). Hence, the genome sizes were estimated to be 2491·0±180·6 kbp for ATCC 393 (pLZ15-) and 2031·0±33·2 kbp for ATCC 393T. Previous studies have reported similar genome sizes for L. casei ATCC 393T (2·0 Mb; Chassy, 1976) and L. casei ATCC 334 (2·17 Mb; Ferrero et al., 1996).
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; Liu et al., 1993). The number of bands observed when the DNA was digested with this enzyme suggests that there should be five copies of the rrn operon in ATCC 393 (pLZ15-) and four copies of the rrn operon in ATCC 393T (Table 3
), which exactly coincides with the number of operons estimated by ribotyping. Data obtained from this set of experiments further prove that ATCC 393T and ATCC 393 (pLZ15-) are genetically different. Although macrorestriction analysis is technically more complex than the other techniques described here, it provides good discrimination between strains and, when performed properly, other useful genomic data, such as the genome size and the number of rrn operons.
ARDRA.
The 16S rDNA of all the strains was amplified by PCR and digested with the restriction enzymes AluI or HinfI. An identical pattern of bands was obtained in all cases (Fig. 3). With AluI, the observed band sizes were 610, 240 and 210 bp. The sequence map revealed that the band of 210 bp was actually composed of three fragments with very similar lengths, while a small band of 33 bp could not be detected (33, 207, 207, 213, 248, 614 bp). The sizes of the fragments obtained with HinfI were 980, 290, 190 and 70 bp. Despite the differences found between the two groups of strains with the other molecular techniques used here, ARDRA could not be used to distinguish them, indicating that the resolution threshold of this technique is at a higher taxon level.
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). Chen et al. (2000) described two 23S–5S ITS amplicons for the L. casei–paracasei group with sizes of 250 and 170 bp, which approximately coincide with the sizes we estimated for ITS2 of the ATCC 393 (pLZ15-) strains, indicating that the strain used by these authors as ATCC 393T was possibly the plasmid-cured derivative obtained by Flickinger et al. (1986). This is another example of the great confusion generated when two different strains are circulating as the reference strain.
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.
Positions of the variable bases in domain I of the 16S rDNA sequence were identified using sequences from the Ribosomal Database Project (RDP). They coincided with those published previously, which were in the region of the first 90 nt of the sequence; the signature sequence was also located in positions 47–85 (Mori et al., 1997).
Unfortunately, there are no complete sequences available for domain I of the 23S rDNA of the L. casei group; therefore, alignments could not be produced. However, nucleotide differences between our strains could be identified between positions 110 and 132, which contained the likely 23S domain I signature sequence (data not shown). The partial 23S rDNA sequences of strains BL 23 and BL 94T have been deposited in GenBank under accession nos AY112675 and AY112676, respectively.
The G+C content of the 16S rDNA sequence was 52 mol% for ATCC 393 (pLZ15-) and 51 mol% for ATCC 393T; for the 23S rDNA domain I sequence, the G+C content was 53 mol% for ATCC 393 (pLZ15-) and 52 mol% for ATCC 393T.
The complete sequence of the 16S rDNA (1518 nt) was then determined for BL 23 (GenBank accession no. AF385770) and BL 94T (GenBank accession no. AF469172), representing ATCC 393 (pLZ15-) and ATCC 393T, respectively. The sequence of strain ATCC 393T was 100 % similar to another reported 16S rDNA sequence of L. casei ATCC 393T (GenBank accession no. D16551) and 99 % similar to the 16S rDNA sequence of L. zeae ATCC 15820T (GenBank accession no. D86516). Most notably, the 16S rDNA sequence of ATCC 393 (pLZ15-) was 100 % similar to that of Lactobacillus paracasei subsp. paracasei ATCC 4022 (GenBank accession no. D79212). Strain L. casei BL 23 has been deposited in the Spanish National Culture Collection under reference no. CECT 5275T.
Many authors have proposed that L. casei ATCC 393T should be reassigned to the species L. zeae and that another strain should be proposed as the neotype of L. casei (e.g. Dellaglio et al., 1991; Dicks et al., 1996); however, this proposal was rejected by the Judicial Commission of the International Committee on Systematic Bacteriology (Wayne, 1994). In the present work, strains regularly used as ATCC 393T were examined and it was found that the four strains obtained from accredited type-culture collections were identical and were similar to L. zeae, as described previously, but strains received as plasmid-cured variants of L. casei ATCC 393T were identical to L. paracasei.
The history of the plasmid-cured derivative of ATCC 393T starts in the early 1970s, when B. Chassy carried out a number of biochemical and genetic studies on the L. casei ATCC 393T strain obtained from the American Type Culture Collection (personal communication). As consequence of this work, ATCC 393 (pLZ15-), which was later widely distributed, was obtained. However, the main conclusion of the present work is that strains ATCC 393T and ATCC 393 (pLZ15-) are phenotypically and genetically different. In fact, although their 16S and 23S rDNAs have highly similar sequences (97·7–97·8 %), according to the taxonomic structure of this group these strains should, at present, be included in different species, L. casei and L. paracasei, respectively. Therefore, the ancestral strain of ATCC 393 (pLZ15-) has never been the strain that is now held in culture collections.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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phage digested with PstI; 1, BL 23, L. casei ATCC 393 (pLZ15-); 2, BL 27, L. casei ATCC 393 (pLZ15-); 3, BL 54, L. casei ATCC 393 (pLZ15-); 4, BL 6T, L. casei ATCC 393T; 5, BL 70T, L. casei ATCC 393T; 6, BL 94T, L. casei ATCC 393T; 7, BL 119T, L. casei ATCC 393T.
