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1 Ministry of the Flemish Community, Centre for Agricultural Research, Department of Animal Product Quality, Brusselsesteenweg 370, 9090 Melle, Belgium
2 Universiteit Gent, Faculty of Sciences, Laboratory of Microbiology (WE10V), K. L. Ledeganckstraat 35, 9000 Gent, Belgium
3 Glasgow Caledonian University, School of Biological and Biomedical Sciences, Cowcaddens Road, Glasgow G4 0BA, UK
Correspondence
Patsy Scheldeman
P.Scheldeman{at}clo.fgov.be
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 TOP ABSTRACT MAIN TEXTDescription of Paenibacillus...REFERENCES |
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Published online ahead of print on 5 December 2003 as DOI 10.1099/ijs.0.02822-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of P. lactis MB 1871T, MB 1928, MB 2035 and Paenibacillus sp. MB 2039 are respectively AY257868–AY257871.
Detailed strain information, DNA–DNA relatedness and G+C content data, a full phylogenetic tree and a photomicrograph of sporangia and vegetative cells of the type strain are available as supplementary material in IJSEM Online.
Present address: Laboratory of Animal Genetics, Ghent University, Heidestraat 19, 9820 Merelbeke, Belgium. 
Present address: Department of Bacteriology and Immunology, Veterinary and Agrochemical Research Centre, VAR-CODA-CERVA, Groeselenberg 99, 1180 Ukkel, Belgium.
Present address: Center for Microbial Ecology, Michigan State University, 545 Plant and Soil Science Building, East Lansing, MI 48824-1325, USA.
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TOPABSTRACTMAIN TEXTDescription of Paenibacillus...REFERENCES |
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) and display physiologically diverse characteristics. One distinctive characteristic of members of the genus is their ability to degrade a variety of macromolecules, amongst others proteins (Ash et al., 1993), polysaccharides (Kanzawa et al., 1995; Claus & Berkeley, 1986) and polyaromatic hydrocarbons (Daane et al., 2002). Another is the ability of paenibacilli associated with plants to fix nitrogen. These include Paenibacillus azotofixans (Seldin et al., 1984), Paenibacillus polymyxa (Grau & Wilson, 1962) and Paenibacillus macerans (Witz et al., 1967). More recently, four more nitrogen-fixing species of Paenibacillus, Paenibacillus borealis (Elo et al., 2001), Paenibacillus brasilensis (von der Weid et al., 2002), Paenibacillus graminis and Paenibacillus odorifer (Berge et al., 2002), have been described. Some Paenibacillus strains also produce antibacterial (e.g. Martin et al., 2003; Piuri et al., 1998) or antifungal compounds (e.g. Beatty & Jensen, 2002; Chung et al., 2000).
Sporogenesis enables members of Bacillus, Paenibacillus and related organisms to withstand environmentally harsh conditions, allowing long-term survival (Setlow, 1994). The resulting omnipresence of Bacillus and its relatives favours contamination of many foods. The resistance of their endospores, which may be associated with psychrophilic or acidophilic properties of the vegetative cells, causes specific problems to the food industry (Andersson et al., 1995). Incidences of paenibacilli in food products such as pasteurized puréed vegetables have been reported previously (Berge et al., 2002; Guinebretière et al., 2001). The most common spore-forming bacteria (55 % of the isolates) found in the production process of refined paper products for food applications proved to be Paenibacillus species (Raaska et al., 2002).
Although Paenibacillus spores in raw and pasteurized milk are not predominant, their presence has been recognized (for an overview, see Heyndrickx & Scheldeman, 2002). Feeds for dairy cattle appear to be a significant source of contamination of raw milk with spores. Paenibacillus species are present in both silage (te Giffel et al., 2002) and feed concentrate for dairy cattle (Vaerewijck et al., 2001). To our knowledge, there have been no previous reports of Paenibacillus spores surviving industrial sterilization or UHT processing of milk. Nevertheless, te Giffel et al. (2002) reported that some Paenibacillus spores were able to withstand temperatures above 120 °C.
In this study, we elucidated the taxonomic position of 19 spore-formers isolated from contaminated industrial UHT milk and from the dairy farm. In addition to molecular typing, we used extensive phenotypic characterization, 16S rRNA gene sequencing and DNA–DNA reassociation to study these isolates.
Details of the strains included in this study are listed in Supplementary Table A available in IJSEM Online. All strains, except for LMG 11157T and SB150-2B, were isolated after a 30-min 100 °C heat treatment of the samples, either from a number of dairy farms (Scheldeman et al., 2002) or from contaminated UHT milk from different processing lines in a dairy plant. All MB-numbered strains were grown on brain heart infusion (BHI; Oxoid) supplemented with bacteriological agar no. 1 (Oxoid) and filter-sterilized vitamin B12 (1 mg l–1; Sigma). The type strain of Paenibacillus lautus, LMG 11157T, was grown according to the recommendations of the BCCM/LMG Bacteria Culture Collection.
Whole-cell DNA for PCR amplification was extracted from pure cultures by the method described by Pitcher et al. (1989). For DNA–DNA reassociation experiments, high-quality total genomic DNA was purified on a larger scale as described by Logan et al. (2000), except that lysozyme was dissolved in TE buffer with an increased EDTA concentration (1·21 g Tris, 6 ml 0·5 M EDTA, pH 8·0, in 1 l MilliQ water) and that the cell suspensions were incubated with lysozyme until the viscosity increased (usually after 10–15 min).
In this study, the term rep-PCR is used as an overall term to refer to molecular typing based on repetitive elements [including REP-, (GTG)5-, BOX- and ERIC-PCR], whereas REP-PCR refers to one specific method using the primers REP 1R-I and REP 2-I (Versalovic et al., 1994). The conditions for REP-PCR were described previously by Herman et al. (1998). In addition, the (GTG)5 primer (Versalovic et al., 1994) was used under the following PCR conditions. Amplification reactions were performed in a final volume of 25 µl containing PCR buffer (10 mM Tris/HCl, pH 8·3, and 50 mM KCl) (Applied Biosystems), 1·5 mM MgCl2, 0·2 mM of each dNTP (Pharmacia), 0·3 µg primer, 1 U Goldstar DNA polymerase (Eurogentec) and 25 ng DNA template. The PCR program (Versalovic et al., 1994) was run on a DNA thermal cycler (Perkin Elmer 9600). To avoid inter-PCR differences, all samples were included in one single PCR run.
The rep-PCR amplicons were separated in a 1·5 % LSI LE agarose gel (Life Science International) (20x25 cm) for 4 h at a constant voltage of 4 V cm–1 in 1x TBE (100 mM Tris/HCl, 100 mM boric acid, 2 mM EDTA, pH 8·0). rep-PCR profiles were visualized after staining with ethidium bromide, followed by digital image capturing using a GelDoc 2000 camera (Bio-Rad). A mixture of molecular mass markers VIII, IX and X (Roche) was used as references for intra- and inter-gel comparison. Numerical analysis of the resulting fingerprints was done using the GelCompar II version 2.0 software package (Applied Maths). Similarity among digitized profiles was calculated using Pearson's correlation coefficient and an average linkage (UPGMA) dendrogram was derived. Finally, both the REP- and (GTG)5-PCR patterns were linearly combined, assigning the same weight to each analysis.
Amplified rDNA restriction analysis (ARDRA) of 16S rDNA was performed as described previously (Heyndrickx et al., 1996).
The 16S rRNA genes of strains MB 1871T (=LMG 21940T=DSM 15596T), MB 1928 and MB 2035 were amplified by PCR using conserved primers pA (5'-AGAGTTTGATCCTGGCTCAG-3') and pH (5'-AAGGAGGTGATCCAGCCGCA-3'). The PCR products were purified and subsequently sequenced using an ABI 310 sequencer (Applied Biosystems) as described previously (Scheldeman et al., 2002). A combination of primers pA, *pD, *O, *R, *gamma and pH (Coenye et al., 1999) was used to obtain a continuous stretch of the 16S rRNA gene sequence. Sequence assembly was implemented using the GeneBase software (Applied Maths). The BioNumerics 3.0 software package (Applied Maths) was used for construction of a phylogenetic tree based on the neighbour-joining method.
DNA–DNA hybridizations were performed with photobiotin-labelled probes in microplate wells as described by Ezaki et al. (1989). For the fluorescence measurements, a Bio Assay Reader (HTS7000, Perkin Elmer) was used as described in detail by Willems et al. (2001). A hybridization temperature of 37 °C was applied for the experiments in this study.
The DNA base composition was determined by HPLC using further specifications given by Logan et al. (2000).
The culture conditions for fatty acid methyl ester (FAME) analysis were as described by Scheldeman et al. (2002). The methods used for fatty acid extraction, methyl ester preparation and separation by GC were described by Vancanneyt et al. (1996).
Phenotypic tests were performed as described by Logan & Berkeley (1984); other characters were determined and the data numerically analysed as described by Logan et al. (2000). For observations on sporangia, cells were grown on TSA MnSO4 at 30 °C.
During a period of obstinate contamination of the UHT-milk production in a dairy company, two colony types were isolated from nine individual packages from different processing lines (both direct and indirect UHT). The first colony type, present in only two samples, resembled Bacillus sporothermodurans and was indeed identified as such by the PCR-detection method described by Herman et al. (1997) (data not shown). Isolates of the second colony type, present in all nine samples, reacted negatively both to the latter PCR detection method and to the more universal PCR test of Scheldeman et al. (2002), based on the 16S rDNA of B. sporothermodurans. The contamination of the UHT-milk packages was therefore due to another spore-forming organism, present in co-contamination with B. sporothermodurans and probably also surviving the UHT process.
The 16S rRNA gene sequence of one of the nine non-B. sporothermodurans UHT isolates, MB 1928, was determined and the highest similarity in the EMBL database found by a FASTA search (Pearson & Lipman, 1988) was 97·0 % (1432 nt overlap) to Paenibacillus sp. SB-150-2B (=MB 2328; AF395029), a strain isolated from an ice core in Sajama, Bolivia. The highest similarity to a recognized species was only 96·6 %, to P. lautus NRRL NRS-666T (D78473; 1396 nt overlap). However, the 16S rRNA gene of strain MB 1928 did show a pairwise similarity of 99·1 % to MB 2035 (=R-6472), a strain isolated from raw milk during a survey for very heat-resistant spore-forming bacteria on dairy farms in 1999 (Scheldeman et al., 2002).
In addition to MB 2035 and MB 2328 (=SB-150-2B), more close relatives of the fresh-UHT isolate MB 1928 were sought among a large collection of strains on the basis of their whole-cell FAME profiles (data not shown) and a selection of representative strains was subsequently subjected to ARDRA (data not shown). In ARDRA, the raw-milk strain MB 2035 grouped together with three other strains, MB 1868 (=R-6435), MB 1871T (=R-7191T) and MB 1879 (=R-7193), with a similarity of 95 % (data not shown). Based on the FAME data, 15 other potentially related Paenibacillus strains from dairy farms (see Table 1), grouping within an Euclidian distance of 15 from the above-mentioned strains, were selected for polyphasic characterization.
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) could be delineated. The nine UHT isolates and one farm strain isolated from a cluster of the milking apparatus (MB 1868) all grouped together in cluster B at an internal similarity of 92·1 %. Interestingly, all these isolates showed virtually identical banding patterns and could thus be regarded as of clonal origin. A group of nine farm isolates grouped together in a more diverse cluster A, at a similarity level of 62·4 %. The remainder of the strains grouped together in three smaller clusters. Cluster C, with an internal similarity of 56·9 %, contained four raw milk strains, whereas cluster D consisted of a raw milk strain and a farm strain grouping together at 63·6 %. Three strains originating from the milking apparatus of the same farm grouped together in cluster E at a similarity level of 72·7 %. Finally, the ice-core strain MB 2328 took a single position in the dendrogram.
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), MB 2039, showed only 91·1 % similarity to the 16S rDNA of MB 1928. As a result, the strains of cluster C can not be considered as phylogenetically closely related to strains of clusters A and B.
Comparison of the 16S rDNA sequences of strains MB 1871T, MB 1928 and MB 2035 with those of all recognized species of the genus Paenibacillus is given in a phylogenetic neighbour-joining tree (Fig. 2; see also Supplementary Fig. A). The three strains MB 1871T, MB 1928 and MB 2035 showed mutual 16S rDNA similarities of over 99 % and they appeared as a well-separated branch in the phylogenetic tree (Fig. 2), with P. lautus JCM 9073T (approx. 97 % 16S rDNA similarity), Paenibacillus sp. SB-150-2B (approx. 97 %) and Paenibacillus glucanolyticus DSM 5162T (approx. 96 %) as their closest relatives.
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; Stackebrandt et al., 2002). The usefulness of rep-PCR for delineating groups of strains for taxonomic purposes was also demonstrated in previous studies (e.g. Rademaker et al., 2000; Goris et al., 2002). The status of the novel strains is also corroborated by their DNA base composition (Supplementary Table B), which falls within the range 45–54 mol% G+C, as reported for the genus Paenibacillus (Shida et al., 1997).
In the cellular fatty acid analysis (Table 1), a predominance of anteiso-C15 : 0, typical of paenibacilli (Shida et al., 1997), was also observed for MB 1871T (45·9 % of total cellular fatty acids). The fatty acid profile of MB 1871T resembles those of other type strains of Paenibacillus species, but there are significant differences in the proportions of anteiso-C15 : 0 and iso-C15 : 0 (Table 1).
The strains were found to be Gram-variable or Gram-negative, aerobic and motile rods. They formed ellipsoidal or cylindrical spores that lay paracentrally or subterminally in slightly swollen sporangia (Supplementary Fig. B). On TSA plates, the strains formed discrete colonies and occasionally formed spreading growth reminiscent of Paenibacillus alvei. Most of the strains clustered together at 87·5 % similarity in a UPGMA cluster analysis (not shown) based upon their biochemical reactions, and this cluster merged with other species of Paenibacillus, including P. lautus, P. macerans and P. polymyxa, at 80 % similarity. Two strains, MB 1868 and MB 2044, gave weak reactions in the biochemical tests and did not group with other Paenibacillus species, but with the type strain of Bacillus lentus; this misallocation could be attributed entirely to the weakness of their reactions in the API 50CHB gallery, rather than to them having different patterns of carbohydrate utilization. These results indicate that, although the majority of the milk isolates form a group phenotypically distinct from established species of Paenibacillus, weakly reacting strains may be misidentified if phenotypic tests alone are relied upon for identification (see Table 2).
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Strains of this novel species were isolated from both raw and heat-treated milk. Moreover, we detected a clonal relationship between a raw-milk strain (MB 1868) and isolates from a contaminated lot of UHT milk. A possible contamination route from raw milk on the dairy farm to heat-treated milk in the dairy is therefore not implausible. The fact that some of these strains were present jointly with B. sporothermodurans spores, known for its extreme heat resistance (Huemer et al., 1998), in several UHT-milk packages from different processing lines indicates that, by analogy, spores of the UHT isolates of this novel species might be capable of surviving severe heat treatment and, as a result, affecting the keeping quality or safety of food products.
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Description of Paenibacillus lactis sp. nov. |
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TOPABSTRACTMAIN TEXTDescription of Paenibacillus...REFERENCES |
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Cells are single, straight and round-ended, motile rods, that may occasionally be slightly tapered and curved. Gram-negative or Gram-variable. Cell diameter is 0·6–0·9 µm and cell length is 3–6 µm. Endospores are ellipsoidal or cylindrical, are located subterminally and occasionally paracentrally and usually swell the sporangia. Colonies grown for 4 days on TSA at 30 °C are opaque, cream-coloured, slightly convex and round, with rough or spreading transparent edges and with eggshell surface texture. Motile microcolonies may spread across the surface of the agar and rotate in a clockwise direction. Colony diameter is 1–2 mm. Aerobic. Maximum temperature for growth lies between 50 and 55 °C and the optimum temperature lies between 30 and 40 °C. Optimum pH for growth is 7·0; the minimum pH is between 5·0 and 6·0 and the maximum pH between 10·5 and 11. Casein is not hydrolysed. In the API 20E strip, o-nitrophenyl 
-D-galactopyranoside hydrolysis is positive. Nitrate reduction is variable and Voges–Proskauer reaction is negative or weak, while reactions for arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, citrate utilization, hydrogen sulphide production, urease, tryptophan deaminase, indole production and hydrolysis of gelatin are negative. In the API 50CH gallery using the CHB suspension medium, hydrolysis of aesculin is positive and acid is produced without gas from the following carbohydrates: amygdalin, L-arabinose, arbutin, D-cellobiose, D-fructose, D-glucose, glycogen, lactose, maltose, mannitol, D-mannose, D-melibiose, D-raffinose, ribose, starch, sucrose, D-trehalose, D-turanose and D-xylose. Occasional strains give weak reactions with the following substrates: amygdalin, L-arabinose, arbutin, D-cellobiose, D-fructose, D-glucose, lactose, maltose, mannitol, D-mannose, D-melibiose, D-raffinose, sucrose, D-turanose and D-xylose. Production of acid without gas is strain-dependent for D-arabinose, L-fucose, galactose, gentiobiose, gluconate, D-melezitose, methyl D-glucoside, methyl xyloside, N-acetylglucosamine and salicin. Acid is not produced from adonitol, D-arabitol, L-arabitol, dulcitol, erythritol, D-fucose, glycerol, inulin, 2-keto-D-gluconate, 5-keto-D-gluconate, D-lyxose, meso-inositol, methyl D-mannoside, rhamnose, sorbitol, L-sorbose, D-tagatose, L-xylose or xylitol. Of the variable results, the type strain was positive for D-arabinose, L-fucose, galactose, gentiobiose, gluconate, D-melezitose, methyl xyloside, N-acetylglucosamine and salicin and was weakly positive for methyl D-glucoside. Nitrate reduction is weak and Voges–Proskauer reaction is negative. The major cellular fatty acids are (means of 10 strains): anteiso-C15 : 0 (38·5±5·3 % of total cellular fatty acids), C16 : 0 (23·9±6·7), iso-C15 : 0 (11·1±1·4), anteiso-C17 : 0 (5·4±1·9), iso-C16 : 0 (5·4±1·4), iso-C17 : 0 (4·8±1·2), C16 : 1
11c (4·3±1·3), C14 : 0 (3·1±1·4), iso-C14 : 0 (2·0±0·6) and C15 : 0 (1·0±0·7). Fatty acids present at less than 1 % are not listed. The DNA G+C content varies from 51·6 mol% for MB 1871T to 51·7 mol% for strains MB 1928 and MB 2035.
The type strain is MB 1871T (=LMG 21940T=DSM 15596T).
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ACKNOWLEDGEMENTS |
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