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1 Unité Mixte de Recherche Génie et Microbiologie des Procédés Alimentaires (UMR GMPA), Institut National de la Recherche Agronomique, 78850 Thiverval-Grignon, France
2 Collection de l'Institut Pasteur, Institut Pasteur, 75724 Paris Cedex 15, France
3 Unité de Biodiversité des bactéries pathogènes émergentes, INSERM U389, Institut Pasteur, 75724 Paris Cedex 15, France
Correspondence
Françoise Irlinger
irlinger{at}grignon.inra.fr
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains Gor104, Ma107, Bres102, Cou102, Epo104, Po101, Po102, Re117T, Stp101, Ca106T, Ka101, La101 and Re127 are AJ609621–AJ609633, respectively.
A dendrogram based on ribotyping data, an extended 16S rRNA gene-based neighbour-joining tree and detailed DNA–DNA hybridization results are available as supplementary material in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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; Bockelmann, 2002; Brenann et al., 2002; Place et al., 2002, 2003). These two groups present similar physiological properties permitting their growth on the cheese surface: they are aerobic, alkaliphilic, mesophilic and salt-tolerant and cannot develop under acid conditions.
Fifteen years ago, in both the dairy industry and the literature, cheese coryneform bacteria were still either classified separately in pigmented groups (orange, yellow, cream, grey, unpigmented) or assigned to groups based on a few, subjectively weighted morphological and staining properties (Eliskases-Lechner & Ginzinger, 1995; Piton & Fontanier, 1990; Piton-Malleret & Gorrieri, 1992). To date, only a few taxonomic molecular studies have been carried out on the identification of these bacteria (Brennan et al., 2001a, b, 2002; Hoppe-Seyler et al., 2003) and knowledge of the species composition of the smear cheese is limited.
Members of the genus Arthrobacter are Gram-positive, catalase-positive, aerobic and asporogenous bacteria that display a coryneform morphology (Keddie et al., 1986). This genus is phenotypically heterogeneous and over 35 species are currently recognized (Euzéby, 2004; Stackebrandt & Schumann, 2000). Two main groups of species are distinguished within the genus Arthrobacter sensu stricto on the basis of their peptidoglycan type and menaquinone composition (Keddie et al., 1986; Schleifer & Kandler, 1972; Stackebrandt et al., 1983; Stackebrandt & Schumann, 2000). Group I species of Arthrobacter contain A3
peptidoglycan variant and include most species of the genus including Arthrobacter globiformis, the type species (Stackebrandt et al., 1983). Group II species possess the A4 peptidoglycan variant and include Arthrobacter nicotianae, Arthrobacter sulfureus, Arthrobacter mysorens, Arthrobacter uratoxydans and Arthrobacter protophormiae and also two relatively recently described species, Arthrobacter creatinolyticus (Hou et al., 1998) and Arthrobacter rhombi (Osario et al., 1999). Representatives of the group II species form a separate branch within the phylogenetic cluster of the genus Arthrobacter (Osario et al., 1999; Stackebrandt & Schumann, 2000).
The occurrence of yellow-pigmented Arthrobacter strains including those identified as A. nicotianae in surface-ripened cheeses (Valdès-Stauber et al., 1997) or in mould surface-ripened cheeses, such as Brie and Camembert (Marcellino & Benson, 1992), has been reported. A number of yellow coryneform isolates from several varieties of Austrian cheeses were preliminarily identified as A. globiformis, while most Arthrobacter strains could not be assigned to any known species (Bockelmann et al., 1997; Eliskases-Lechner & Ginzinger, 1995).
In this paper, we present the results of a polyphasic taxonomic study of 14 strains from the surface of smear-ripened cheeses and propose to classify them as two novel species of the genus Arthrobacter, Arthrobacter bergerei sp. nov. and Arthrobacter arilaitensis sp. nov.
The 14 strains under study were isolated from the surfaces of different smear-ripened cheeses (French cheeses unless stated otherwise): Bres102, from Bresso (a German cheese); Ca106T, Camembert; Cou102, Coulommiers; Ep104, Epoisses; Gor104, Gorgonzola (an Italian cheese); Ka101, Kamtohntv (a Russian cheese); La101, Langres; Ma107, Maroilles; Po101 and Po102, Pont l'Evêque; Re117T and Re127, Reblochon; Sne104, Saint-Nectaire; Stp101, Saint Paulin. All strains were cultivated on brain heart infusion (BHI) agar and incubated at 28 °C. The following reference strains were used in the comparative study: A. nicotianae LMG 16305T, A. nicotianae CIP 82.22, A. protophormiae DSM 20168T, A. protophormiae ATCC 21040, A. sulfureus LMG 16694T, A. uratoxydans CIP 102367T, A. mysorens LMG 16219T, A. mysorens LMG 16125, A. rhombi CCUG 38813T and A. creatinolyticus JCM 10102T. Stocks of all strains were prepared in 50 % (w/v) glycerol and stored at –80 °C.
Cell morphology was determined by phase-contrast microscopy of cells grown on BHI agar (Difco), motility by the hanging-drop method and the catalase test by the production of bubbles on the application of 3 % (v/v) H2O2 to a colony. Oxidase activity was determined by using the modified oxidase test of Faller & Schleifer (1981). Salt tolerance (NaCl) and optimal growth temperature range were determined using a multipoint inoculator (Kloos et al., 1974).
The commercially available API CORYNE kit (bioMérieux) was used to determine enzymic activities and some other phenotypic properties and interpreted according to the manufacturer's instructions; strips were read after 24 h incubation. Carbon-source utilization tests were performed with the Biotype 100 system using medium 2 (bioMérieux) after 2, 4 and 6 days incubation. All biochemical tests were performed at 28 °C.
Cell-wall material was prepared and hydrolysed by the method of Keddie & Cure (1977). A 3 µl aliquot was spotted onto a high-performance TLC cellulose plate, which was developed by two-dimensional chromatography as described by Brenner et al. (1969). Whole-cell sugars were analysed as described by Schaal (1985). Mycolic acids were detected as described by Minnikin et al. (1975, 1980).
Genomic DNA was extracted as follows. Strains were grown at 28 °C for 2 days with mixing in a 2 l Erlenmeyer flask containing 500 ml BHI broth. Cultures were harvested at 6000 g for 20 min and washed twice with 50 mM Tris/HCl (pH 8). Next, 15–50 ml (depending on the pellet size) of a solution containing Tris/HCl (50 mM), pH 8, sucrose (100 mM) and 0·5 % (v/v) Triton X-100 was added, mixed and incubated overnight at 30 °C. Subsequently, 250 mg lysozyme and 375 µl mutanolysin (5 U µl–1) were added, mixed and incubated for 1 h at 37 °C. Next, 3·75 ml proteinase K (20 mg ml–1) and 3·7 ml 10 % Sarkosyl were added, mixed and incubated for 24 h at 37 °C. Finally, 3·75 µl 25 % SDS was added, mixed and incubated for 1 h at 55 °C.
DNA was purified according to Brenner et al. (1982). DNA–DNA hybridization studies were carried out at the Institut Pasteur by the S1 nuclease method following a published procedure (Grimont et al., 1980). DNA–DNA hybridization was carried out at 60 °C. The temperature at which 50 % of the reassociated molecules are dissociated (Tm) has been determined (Crosa et al., 1973) when DNA relatedness was between 30 and 80 %. The difference (
Tm) between the Tm of the homoduplex and the Tm of the heteroduplex was calculated as a measure of divergence (Brenner, 1978).
PCR amplification of rrs gene fragments was performed as described by Dauga et al. (1997). Amplified fragments of 1500 bp were sequenced by Genome Express. The sequences obtained were assembled and aligned with the Lasergene software (DNASTAR) and compared to the GenBank database (http://ww2.ncbi.nlm.nih.gov/genbank/query_form.html). The rrs sequences of 13 strains were aligned with reference sequences (Fig. 1) from the GenBank/EMBL database, using the multiple sequence alignment program CLUSTAL V (Higgins et al., 1992). Phylogenetic distances were determined according to Jukes & Cantor (1969) and a tree was obtained by neighbour-joining (Saitou & Nei, 1987) as implemented by the Lasergene software.
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. Methods for cleavage of each DNA with either BglI or PvuII, electrophoresis, hybridization with 16S and 23S rRNA and visualization of ribotypes have been published (Lefresne et al., 2004; Regnault et al., 1997). Ribotypes were interpreted using various programs of the Taxotron package (Institut Pasteur) as described in Brosch et al. (1996).
The 14 isolates exhibited the general characteristics of the genus Arthrobacter. They were Gram-positive, non-spore-forming, non-motile, not acid-fast and displayed a rod–coccus growth cycle. They produced a cream or yellow pigment depending on the medium. The cell wall of all 14 strains contained L-lysine as the principal amino acid, galactose, glucose, ribose and mannose as whole-cell sugars and no mycolic acids. The 16S rRNA gene-based phylogenetic analysis showed that all 14 strains fall into a separate phylogenetic cluster (Fig. 1
; see also Supplementary Fig. A in IJSEM Online) encompassing seven Arthrobacter species that have peptidoglycan variation A4 (Osario et al., 1999; Stackebrandt & Schumann, 2000). It also indicated that the cheese isolates constituted two different phylogenetic groups and showed highest sequence similarity (>98 %) to A. nicotianae, A. mysorens and A. protophormiae (Fig. 1).
Ribotypes with PvuII and BglI restriction digests of cheese strains showed that three groups, composed respectively of five strains (Ma107, Po101, Po102, Re117T, Bres102), four strains (Cou102, Ep104, Stp101 and Gor104), subsequently referred to as Arthrobacter arilaitensis sp. nov., and five strains (Sne104, Re127, Ka101, La101, Ca106T), subsequently referred to as Arthrobacter bergerei sp. nov., could be distinguished by ribotyping (Supplementary Fig. B in IJSEM Online). The rrs sequences of A. arilaitensis and A. bergerei each showed more than 99 % within-group similarity, demonstrating their homogeneity.
DNA of the four strains Re117T, Po101, Ep104 and Ca106T, representing different ribotypes, was hybridized against that from all 14 cheese isolates and the type strains of phylogenetically neighbouring species. DNA–DNA reassociation values showed A. arilaitensis and A. bergerei to constitute genomic species with 78–100 % within-species relatedness and 23–28 % between-species relatedness (for detailed results see Supplementary Table in IJSEM Online). According to DNA–DNA hybridization studies, A. arilaitensis (represented by strains Re117T, Po101, Ep104) was less than 43, 34 and 18 % related to the respective type strains of A. nicotianae, A. protophormiae and A. uratoxydans. A. bergerei (strain Ca106T) was less than 18 % related to A. protophormiae DSM 20168T. A previous study at the Institut Pasteur (R. Brosch and P. A. D. Grimont, unpublished data) had shown A. nicotianae LMG 16305T (source of labelled DNA) and A. mysorens LMG 16219T (source of unlabelled DNA) to constitute a single DNA relatedness group (74 % DNA–DNA reassociation). Therefore, A. arilaitensis and A. bergerei are discrete genomic species.
Support for the distinctiveness of the novel species also came from phenotypic evidence (Table 1). On the basis of the results of physiological, chemical and molecular genetic analyses, it was concluded that the Arthrobacter isolates described should be classified as two novel species of the genus Arthrobacter, for which we propose the names Arthrobacter arilaitensis sp. nov. and Arthrobacter bergerei sp. nov.
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The description given below was based on the study of nine strains. Cells are aerobic, Gram-positive, catalase-positive, oxidase-negative, non-spore-forming, non-motile and exhibit a rod–coccus growth cycle. Colonies on BHI agar are yellow, round, smooth, convex and 2 mm in diameter. Grows between 10 and 30 °C and tolerates up to 10 % (w/v) NaCl. Gelatinase, 
-galactosidase, pyrazinamidase, pyrrolidonyl arylamidase, phosphatase and -glucosidase are produced. Urease and aesculin are not hydrolysed. Nitrate is not reduced. Glucose, ribose, xylose, mannitol, maltose, lactose, sucrose and glycogen are not fermented. In Biotype 100 strips using biotype 2 medium, most strains (>89 %) are able to use the following substrates as sole carbon sources: D-glucose, maltotriose, maltose, -lactose, D-arabitol, glycerol, 5-keto-D-gluconate, D-gluconate, protocatechuate, 4-hydroxybenzoate, lactate, glycerate and tyrosine. Other substrates are used less frequently (11–88 %): D-galactose, sucrose, D-fructose, D-trehalose, D-mannose, lactulose, L-arabinose, D-ribose, D-xylose, malonate, propionate, 2-oxoglutarate, malate, putrescine, succinate, fumarate, D-glucosamine, 3-hydroxybenzoate, 3-hydroxybutyrate, aspartate, glutamate, proline, alanine, L-histidine, serine, methyl -galactopyranoside, D-cellobiose, -gentiobiose, aesculin, D-turanose, D-sorbitol, aconitate, citrate, D-glucuronate, 2-keto-D-gluconate, L-tryptophan, phenylacetate, 4-aminobutyrate, caprylate and 5-aminovalerate. The following carbon sources are not utilized: sorbose, D-melibiose, D-raffinose, methyl -galactopyranoside, methyl -glucopyranoside, palatinose, L-rhamnose, fucose, D-melezitose, L-arabitol, xylitol, dulcitol, tagatose, myo-inositol, D-mannitol, maltitol, adonitol, lyxose, erythritol, methyl -D-glucopyranoside, methyl D-glucopyranose, saccharate, mucate, tartrate, tricarballylate, D-galacturonate, N-acetyl-D-glucosamine, quinate, gentisate, benzoate, 3-phenylpropionate, m-coumarate, trigonelline, betaine, histamine, caprate, glutarate, ethanolamine, tryptamine and itaconate.
The type strain, Re117T (=CIP 108037T=DSM 16368T), utilizes the following substrates as sole carbon sources: D-glucose, D-galactose, D-trehalose, sucrose, maltotriose, maltose, lactose, D-cellobiose, ribose, L-arabinose, D-xylose, D-arabitol, glycerol, turanose, 5-keto-D-gluconate, D-gluconate, protocatechuate, 4-hydroxybenzoate, lactate, glycerate, aspartate, glutamate, alanine, serine and tyrosine. The cell wall contains lysine, alanine and glutamic acid. The whole cell sugars are galactose, glucose, ribose and mannose. The type strain was isolated from the surface of Reblochon cheese.
Description of Arthrobacter bergerei sp. nov.
Arthrobacter bergerei (ber.ge're.i. N.L. gen. n. bergerei of Bergère, to honour Jean-Louis Bergère, a French microbiologist).
The description given below was based on the results of studies of five strains. Cells are aerobic, Gram-positive, catalase-positive, oxidase-negative, non-spore-forming, non-motile and exhibit a rod–coccus growth cycle. Colonies on BHI agar medium are yellow, round, smooth, convex and 2–3 mm in diameter. Grows between 10 and 30 °C and tolerates up to 7·5 % (w/v) NaCl. -Galactosidase, pyrazinamidase, pyrrolidonyl arylamidase and -glucosidase are produced. Urease, phosphatase, -glucuronidase and gelatinase are not produced. Aesculin is not hydrolysed. Nitrate is not reduced. D-Glucose, ribose, xylose, mannitol, maltose, lactose, sucrose and glycogen are not fermented. In Biotype 100 strips using biotype 2 medium, all strains (100 %) are able to use the following substrates as sole carbon sources: D-glucose, fructose, D-galactose, sucrose, maltose, lactose, ribose, L-arabinose, D-xylose, D-glycerol, D-gluconate, quinate, protocatechuate, lactate, aspartate and glutamate. Other substrates are used less frequently (20–80 %): lactulose, D-cellobiose, L-rhamnose, D-melezitose, D-mannitol, turanose, D-trehalose, D-mannose, maltotriose, arabitol, methyl -galactopyranoside, aconitate, citrate, 2-keto-D-gluconate, L-tryptophan, 4-hydroxybenzoate, 3-hydroxybenzoate, phenylacetate, malate, 5-keto-D-gluconate, betaine, 5-aminovalerate, ethanolamine, malonate, 3-phenylpropionate, coumarate, 4-aminobutyrate, benzoate, putrescine, glucosamine, 3-hydroxybutyrate, histidine, L-alanine, serine, propionate, -ketoglutarate, proline, D-alanine and tyrosine. The following carbon sources are not utilized: sorbose, D-melibiose, D-raffinose, methyl -galactopyranoside, -gentiobiose, methyl -glucopyranoside, aesculin, palatinose, fucose, L-arabitol, xylitol, dulcitol, tagatose, myo-inositol, maltitol, D-sorbitol, adonitol, lyxose, erythritol, methyl -D-glucopyranoside, methyl D-glucopyranose, saccharate, mucate, D-, L- and meso-tartrate, tricarballylate, D-glucuronate, D-galacturonate, N-acetyl-D-glucosamine, gentisate, trigonelline, histamine, caprate, caprylate, glutarate, glycerate, tryptamine and itaconate.
The type strain, Ca106T (=CIP 108036T=DSM 16367T), utilizes the following substrates as sole carbon sources: D-glucose, fructose, D-galactose, D-mannose, sucrose, lactulose, methyl -galactopyranoside, maltotriose, maltose, lactose, D-cellobiose, ribose, L-arabinose, D-xylose, D-arabitol, glycerol, D-gluconate, aconitate, citrate, phenylacetate, quinate, protocatechuate, 3-hydroxybenzoate, benzoate, 4-hydroxybenzoate, putrescine, 4-aminobutyrate, lactate, histidine, glucosamine, aspartate, glutamate, 3-hydroxybutyrate, proline, D-alanine, L-alanine, serine, propionate and tyrosine. The cell wall contains lysine, alanine and glutamic acid. The whole cell sugars are glucose, ribose and mannose. The type strain was isolated from the surface of Camembert cheese.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTREFERENCES |
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 M. C. Rea, S. Gorges, R. Gelsomino, N. M. Brennan, J. Mounier, M. Vancanneyt, S. Scherer, J. Swings, and T. M. Cogan Stability of the Biodiversity of the Surface Consortia of Gubbeen, a Red-Smear Cheese J Dairy Sci, May 1, 2007; 90(5): 2200 - 2210. [Abstract] [Full Text] [PDF]
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N. Bora, M. Vancanneyt, R. Gelsomino, J. Swings, N. Brennan, T. M. Cogan, S. Larpin, N. Desmasures, F. E. Lechner, R. M. Kroppenstedt, et al. Agrococcus casei sp. nov., isolated from the surfaces of smear-ripened cheeses Int J Syst Evol Microbiol, January 1, 2007; 57(1): 92 - 97. [Abstract] [Full Text] [PDF]
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C. Monnet, K. Correia, A.-S. Sarthou, and F. Irlinger Quantitative Detection of Corynebacterium casei in Cheese by Real-Time PCR Appl. Envir. Microbiol., November 1, 2006; 72(11): 6972 - 6979. [Abstract] [Full Text] [PDF]
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J. Mounier, R. Gelsomino, S. Goerges, M. Vancanneyt, K. Vandemeulebroecke, B. Hoste, S. Scherer, J. Swings, G. F. Fitzgerald, and T. M. Cogan Surface Microflora of Four Smear-Ripened Cheeses Appl. Envir. Microbiol., November 1, 2005; 71(11): 6489 - 6500. [Abstract] [Full Text] [PDF]
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