INTERNATIONAL JOURNAL OF SYSTEMATIC BACTERIOLOGY, Apr. 1990, p. 205-208 0020-7713/90/020205-04$02.00/0 Copyright 0 1990, International Union of Microbiological Societies
Vol. 40. No. 2
NOTES Prevotella, a New Genus To Include Bacteroides melaninogenicus and Related Species Formerly Classified in the Genus Bacteroides HAROUN N. SHAH,l* AND DAVID M. COLLINS2 Department of Oral Microbiology, The London Hospital Medical College, London El 2AD,l and Agricultural and Food Research Council Institute of Food Research, Shinfield, Reading, RG2 9AT,2 United Kingdom It was recently proposed that the genus Bacteroides should be restricted to Bacteroides fragilis (the type species) and closely related organisms (viz., B . caccae, B . distusonis, B . eggerthii, B . merdae, B . ovatus, B . stercoris, B . thetaiotaomicron, B . unifomtis, and B . vulgatus). By contrast, the moderately saccharolytic, predominantly oral Bacteroides species, which include B . melaninogenicus, B. oralis, and related species, form a phenotypically and phylogenetically coherent group of species which differ so significantly from the emended description of the genus Bacteroides that they should not be classified in the same genus. Therefore, we formally propose that these species be reclassified in a new genus, Prevotella. The type species is Prevotella melaninogenica.
The genus Bacteroides has recently undergone major taxonomic revision (32, 46, 47). It is now universely accepted that this genus is phenotypically and phylogenetically heterogeneous. Several new genera, most of which are monospecific, have recently been proposed to accomodate some of the atypical members of the group (Table 1). The majority of the more typical members of the genus (particularly those associated with humans) form three broad groups on the basis of their ability to ferment carbohydrates (viz., saccharolytic, moderately saccharolytic, and asaccharolytic groups of species [for example, see references 17 and 19). The first group consists of Bacteroides fragilis and related species which are generally isolated from gastrointestinal tracts (lo), whereas the second group comprises a large number of moderately saccharolytic species and includes B . melaninogenicus, B. oralis, and related species. The third group includes the pigmented, asaccharolytic species B. asaccharolyticus and B . endodontalis and the important periodontal pathogen B. gingivalis (8, 3 3 , 34, 53). The recognition of three major groups within the genus Bacteroides is supported by biochemical (6,17,27,40,44) and rRNA cistron similarities (19). It has recently been proposed that the genus Bacteroides be restricted to highly fermentative species that phenotypically resemble B. fragilis, the type species of the genus (47), and include B. caccae, B. distasonis, B. eggerthii, B . merdae, B. ovatus, B. stercoris, B. thetaiotaomicron, B. uniformis, and B. vulgatus. Similarly, a new genus, Porphyromonas, has been created to provide a niche for the asaccharolytic species mentioned above (46). However, the position of the moderately saccharolytic species that do not grow well in 2% oxgall remains unresolved. Most species of this group are indigenous to oral cavities (17, 33, 34), and several (B. corporis, B. intermedius, B. loescheii, B. melaninogenicus, and some strains qf B. denticola [16, 171) produce pigmented colonies on blood agar. The nonpigmented members of this group are B. bivius, B. buccae, B . buccalis, B . disiens, B . heparinolyticus, B . oralis, B. oris, B .
oulorum, B . ruminicola, B . veroralis, and B. zoogleoformans. Phenotypically, these species are all similar and can be readily distinguished from members of the genus Bacteroides sensu stricto (47). In addition to their moderately saccharolytic potential and sensitivity to bile, they differ markedly from members of the genus Bacteroides in lacking enzymes of the pentose phosphate pathway-hexose monophosphate shunt (viz., glucose 6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase) (6, 44, 50) (Table 2). Thus, the moderately saccharolytic species are biochemically homogeneous (6, 17, 44), and all of the species examined to date form a phylogenetically (19, 36) coherent group that is quite distinct from the genus Bacteroides sensu stricto (47) and therefore warrant separate generic status. A new genus, Prevotella, is proposed for this group of species. A complete description of Prevotella gen. nov. is given below. Description of Prevotella gen. nov. Prevotella (Pre.vo. tel'la. M.L. dim.ending ella; M.L. fem. n. Prevotella, named after the French microbiologist A. R. PrCvot, a pioneer in anaerobic microbiology). The description below is based on our own observations TABLE 1. Species listed in Bergey's Manual of Systematic Bacteriology which have been reclassified" Species or group
Taxonomic status
Reference
B. fragilis and related species B. asaccharolyticus B. gingivalis B. endodontalis J B. furcosus B. succinogenes B. hypermegas B. multiacidus B. microfusus B. amylophilus B. termitidis B. praeacutus B. ochraceus
Bacteroides (emended definition)
47
Porphy romonas
46
Anaerorha bdus Fibrobacter Megamonas Mitsuokella Rikenella Ruminobacter Se baldella Tissierella Capnocy tophaga
45 30 42 43 7 52
1
* Corresponding author.
" See reference 17. 205
4 5
24
206
NOTES
INT. J. SYST.BACTERIOL.
TABLE 2. Major ecological, biochemical, and chemical characteristics of the genera Prevotella and Bacteroides Usual site of isolation
Genus
Prevotella
Oral cavity, upper respiratory and urogenital tractse Gastrointestinal tract
Bacteroides sensu strict0
p
bile salts' to
~
Metabolismb ~ ~
S
ed
MF
R
-
F
MDH
+ +
~
Presence of c: ~ ~ G6PDH
GDH
+ +
n 6PGDH
-
-
+
+
' S, Sensitive; R, resistant. F, Fermentative; MF, moderately fermentative. MDH, Malate dehydrogenase; GDH, glutamate dehydrogenase; G6PDH, glucose 6-phosphate dehydrogenase; 6PGDH, 6-phosphogluconate dehydrogenase. Only some species produce pigment. Except B. nuninicola subspecies.
and on previous descriptions of the species (1-3, 6, 11-18, 20-23, 25-29, 31, 35, 37-41, 44, 48-51, 54, 55). Gramnegative, obligately anaerobic, nonsporeforming, nonmotile, pleomorphic rods. Surface colonies on blood agar plates vary from minute to 2.0 mm in diameter and are generally circular, entire, convex, shiny, and smooth. Colonies on blood agar are translucent, opaque, grey, light brown, or black. Hemolysis is variable. Glucose broth cultures are usually turbid with smooth or stringy sediments, and the terminal pH is between 4.5 and 5.2. The glucose utilization varies between 30 and 90% in BM (51) broth. The optimum temperature for growth is 37"C, but some strains grow at 25 and 45°C. Growth of most species is inhibited by 6.5% NaCl. Hemin and menadione are required for growth of most species. Growth is inhibited by 20% (wtlvol) bile. The major fermentation products from BM (51) medium or peptoneyeast extract-glucose medium (31) are acetic and succinic acids; occasionally lower levels of isobutyric, isovaleric, or lactic acid are produced. Malate dehydrogenase and glutamate dehydrogenase are present; glucose 6-phosphate dehyrogenase and 6-phosphogluconate dehydrogenase are absent. Proteolytic activity is variable. Most species have limited abilities to ferment amino acids. Nearly all species are indole negative. Nitrate is not reduced to nitrite. The cell wall peptidoglycan contains meso-diaminopimelicacid. The
principal respiratory quinones are unsaturated menaquinones with 10 to 13 isoprene units. Both nonhydroxylated and 3-hydroxylated fatty acids are present. The nonhydroxylated fatty acids are composed of predominantly straightchain saturated, anteiso- and iso-methyl, branched-chain types. Sphingolipids are produced. The DNA base compositions are within the approximate range of 40 to 52 mol% guanine plus cytosine. The type species of the genus Prevotella is Prevotella melaninogenica (Oliver and Wherry 1921) comb. nov. Other currently described species which conform to the generic description of Prevotella include B. bivius, B. buccae, B. buccalis, B. corporis, B. denticola, B. disiens, B. herparinolyticus, B. intemedius, B. loescheii, B. melaninogenicus, B. oralis, B. oris, B. oulorum, B. ruminicola, B. veroralis, and B. zoogleoformans. Phenotypic tests which are useful for the differentiation of these species are shown in Table 3. Description of PrevoteUa mehninogenica (Oliver and Wherry 1921) Shah and Collins 1990 comb. nov. A complete description of Prevotella melaninogenica is given in references 16 and 17. The type strain is strain ATCC 25845 (= Finegold B282 = VPI 4196). Description of Prevotelh bivia (Holdeman and Johnson 1977) comb. nov. A complete description of Prevotella bivia
TABLE 3. Distinguishing characteristics of species of the genus Prevotella
P. melaninogenica P. bivia P. buccae P. buccalis P. corporis P. denticola P. disiens P. heparinotytica P. intermedia P. loescheii P. oralis P. oris P. oulora P. ruminicola P. veroralis P. zoogleoformans
-
+b
-
-
-
+
+
-
-
-
-
-
-
-
-
-
-
+ -
+
+ +
-
-
~
f
+ -
-
+ +-
+(-)
-
-
-
-
+ -
-
+
+ + + ++ + -(+) + ++
+/w
+lw
+
-
-
v
v
-
+ +
-
+ -
a Tested by using the RapID-ANA system (9). +, Positive reaction; -, negative reaction; +/w, weak positive reaction; negative; v, variable reactions.
+/w -
V
+ + ++ + + + + + + + +
2 , positive
+ + + ++ + + +
+ +
+/w
+ +
-
-
-
+ + ++
+ + -(+) +(-) -++ + + -(+) +
+
++ + ++ ++ + +
+ +
+(-)
+ + ++ +(-) + ++ + + +
-
-
+ + - +
-
-
-
-
+ +
+(->
-+ ++ - + V
+
+ + -
5 -
or negative reaction; +(-), most reactions positive; -(+), most reactions
VOL. 40, 1990
is given in references 15 and 17. The type strain is strain ATCC 29303 (= NCTC 11156). Description of Prevotella buccae (Bacteroides pentosaceus Shah and Collins 1982; Bacteroides capillus Kornman and Holt 1982) (Holdeman, Moore, Churn, and Johnson 1982) comb. nov. A complete description of Prevotella buccae is given in references 17, 18, 21, 22, and 41. The type strain is strain ATCC 33574 (= VPI D3A-6). Description of Prevotella buccalis (Shah and Collins 1982) comb. nov. A complete description of Prevotella buccalis is given in references 31 and 41. The type strain is strain ATCC 35310 (= NCDO 2354 = DSM 20616). Description of PrevuteUa corporis (Johnson and Holdeman 1983) comb. nov. A complete description Prevotella corporis is given in references 17 and 20. The type strain is strain ATCC 33547 (= VPI 9342 = Lambe 532-70A). Description of Prevotella denticola (Shah and Collins 1982) comb. nov. A complete description of Prevotella denticola is given in references 16, 41, and 44. The type strain is strain NCDO 2352 (= Socransky 1210). Description of Prevotella disiens (Holdeman and Johnson 1977) comb. nov. A complete description of Prevotella disiens is given in references 15 and 17. The type strain is strain ATCC 29426 (= NCTC 11157). Description of Prevotella heparinolytica (Okuda, Kato, Shiozu, Takazoe, and Nakamura 1985) comb. nov. A complete description of Prevotella heparinolytica is given in references 31 and 35. The type strain is strain ATCC 35895 (= HEP). Description of Prevotella intemediu (Holdeman and Moore 1970) comb. nov. A complete description of Prevotella intermedia is given in references 17 and 20. The type strain is strain ATCC 25611 (= Finegold B422 = VPI 4197). Description of Prevotella loescheii (Holdeman and Johnson 1982) comb. nov. A complete description of Prevotella loescheii is given in references 16 and 17. The type strain is strain ATCC 15930 (= NCTC 11321 = VPI 9085 = Loesche 8B). Description of Prevotella oralis (Loesche, Socransky, and Gibbons 1964) comb. nov. A complete description of Prevotella oralis is given in references 17 and 25. The type strain is strain ATCC 33269 (= VPI D27B-24). Description of PrevoteUa oris (Holdeman, Moore, Churn, and Johnson 1982) comb. nov. A complete description of Prevotella oris is given in references 17 and 18. The type strain is strain ATCC 33573 (= VPI DIA-1A). Description of PrevoteUa oulora (Shah, Collins, Watabe, and Mitsuoka (1985) comb. nov. A complete description of Prevotella oulora is given in references 31 and 48. The type strain is strain NCTC 11871 (= WPH 179) Description of Prevotella ruminicola (Bryant, Small, Bouma, and Chu 1958) comb. nov. A complete description of Prevotella ruminicola is given in references 2 and 17. The type strain is strain ATCC 19189. Description of PrevoteUa veroralis (Watabe, Benno, and Mitsuoka 1983) comb. nov. A complete description of Prevotella veroralis is given in references 31 and 54. The type strain is strain ATCC 33779 (= VPID22A-7). Description of PrevoteUa zoogleoformans (Weinberg, Nativelle, and Prevot 1937) comb. nov. A complete description of Prevotella zoogleoformans is given in references 3, 37, 38 and 55. The type strain is strain ATCC 33285. LITERATURE CITED 1. Bailey, G. D., L. V. H. Moore, D. N. Love, and J. L. Johnson. 1988. Bacteroides heparinolyticus: deoxyribonucleic acid relat-
NOTES
2.
3.
4.
5.
6.
7.
8.
207
edness of strains from the oral cavity and oral-associated disease conditions from horses, cats, and humans. Int. J. Syst. Bacteriol. 38:42-44. Bryant, M. P., I. M. Robinson, C. Bouma, and H. Chu. 1958. Bacteroides ruminicola n. sp. and the new genus and species Succinirnonas amylolytica. Species of succinic acid-producing anaerobic bacteria of the bovine rumen. J. Bacteriol. 76:15-23. Cato, E. P., R. W. Kelley, W. E. C. Moore, and L. V. Holdeman. 1982. Bacteroides zoogleoformans (Weinberg, Nativelle, and Prkvot 1983) comg., comb. nov.: emended description. Int. J. Syst. Bacteriol. 32:271-274. Collins, M. D., and H. N. Shah. 1986. Reclassification of Bacteroides termitidis Sebald (Holdeman and Moore) in a new genus Sebaldella, as Sebaldella termiditis comb. nov. Int. J. Syst. Bacteriol. 36:349-350. Collins, M. D., and H. N. Shah. 1986. Reclassification of Bacteroides praeacutus Tissier (Holdeman and Moore) in a new genus, Tissierella, as Tissierella praeacuta comb. nov. Int. J. Syst. Bacteriol. 36:461-463. Collins, M. D., and H. N. Shah. 1987. Recent advances in the taxonomy of the genus Bacteroides, p. 249-258. In S. P. Borriello, J. M. Hardie, B. S. Drasar, B. I. Duerden, M. J. Hudson, and R. J. Lyson (ed.), Recent advances in anaerobic bacteriology. Martinus Nijhoff Publishers, Dordrecht, The Netherlands. Collins, M. D., H. N. Shah, and T. Mitsuoka. 1985. Reclassification of Bacteroides microfusus (Kaneuchi and Mitsuoka) in a new genus Rikenella, as Rikenella microfusus comb. nov. Syst. Appl. Microbiol. 6:79-81. Coykendall, A. L., F. S. Kaczmarek, and J. Slots. 1980. Genetic heterogeneity in Bacteroides asaccharolyticus (Holdeman and Moore 1970) Finegold and Barnes 1977 (Approved Lists, 1980) and proposal of Bacteroides gingivalis sp. nov. and Bacteroides macacae (Slots and Genco) comb. nov. Int. J. Syst. Bacteriol. 30559-564.
9. Dellinger, C. A., and L. V. H. Moore. 1986. Use of the RapID-ANA system to screen for enzyme activities that differ among species of bile-inhibited Bacteroides. J. Clin. Microbiol. 23:289-293. 10. Finegold, S. M. 1977. Anaerobic bacteria in human disease. Academic Press, Inc., New York. 11. Haapasalo, M., K. Lounatmaa, H. Ranta, H. Shah, and K. Ranta. 1985. Ultrastructures of Bacteroides capillus, Bacteroides buccae, Bacteroides pentosaceus, Bacteroides oris, Bacteroides oralis, Bacteroides veroralis, and pentose sugar-fermenting Bacteroides species from humans with periapical osteitis: occurrence of external proteinaceous cell wall layer. Int. J. Syst. Bacteriol. 35:65-75. 12. Hammann, R., and H. Werner. 1981. Presence of diaminopimelic acid in propionate-negative Bacteroides species and in some butyric acid-producing strains. J. Med. Microbiol. 14: 205-212. 13. Holbrook, W. P., and B. I. Duerden. 1974. A comparison of some characteristics of reference strains of Bacteroides oralis with Bacteroides melaninogenicus. Arch. Oral Biol. 19:12311235. 14. Holbrook, W. P., B. I. Duerden, and A. G. Deacon. 1977. The classification of Bacteroides melaninogenicus and related species. J. Appl. Bacteriol. 43:259-273. 15. Holdeman, L. V., and J. L. Johnson. 1977. Bacteroides disiens sp. nov. and Bacteroides bivius sp. nov. from human clinical infections. Int. J. Syst. Bacteriol. 27:337-345. 16. Holdeman, L. V., and J. L. Johnson. 1982. Description of Bacteroides loescheii sp. nov. and emendation of the descriptions of Bacteroides melaninogenicus (Oliver and Wherry) Roy and Kelly 1939 and Bacteroides denticola Shah and Collins 1981. Int. J. Syst. Bacteriol. 32:399-409. 17. Holdeman, L. V., R. W. Kelly, and W. E. C. Moore. 1984. Genus I. Bacteroides Castellani and Chalmers 1919, 959 p. 604-631. In N. R. Krieg and J. G. Holt (ed.), Bergey’s manual of systematic bacteriology. The Williams & Wilkins Co., Baltimore. 18. Holdeman, L. V., W. E. C. Moore, P. J. Churn, and J. L. Johnson. 1982. Bacteroides oris and Bacteroides buccae, new
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19. 20.
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23. 24. 25. 26. 27. 28. 29. 30.
31. 32.
33.
34.
35. 36.
37.
NOTES species from human periodontitis and other human infections. Int. J. Syst. Bacteriol. 32:125-131. Johnson, J. L., and B. Harich. 1986. Ribosomal ribonucleic acid homology among species of the genus Bacteroides. Int. J. Syst. Bacteriol. 36:7 1-79. Johnson, J. L., and L. V. Holdeman. 1983. Bacteroides intermedius comb. nov. and descriptions of Bacteroides corporis sp. nov. and Bacteroides levii sp. nov. Int. J. Syst. Bacteriol. 33: 15-25. Johnson, J. L.,and L. V. Holdeman. 1985. Bacteroides capillus Kornman and Holt and Bacteroides pentosaceus Shah and Collins, later synonyms of Bacteroides buccae Holdeman et al. Int. J. Syst. Bacteriol. 35114. Kornman, K. S., and S. C. Holt. 1981. Physiological and ultrastructural characterization of a new Bacteroides species (Bacteroides capillus) isolated from severe localized periodontitis. J. Periodontal Res. 16543-555. Lambe, D. W., Jr. 1974. Determination of Bacteroides melaninogenicus serogroups by fluorescent antibody staining. Appl. Microbiol. 28561-567. Leadbetter, E. R., S. C. Holt, and S. S. Socransky. 1979. Capnocytophaga: new genus of gram-negative gliding bacteria. Arch. Microbiol. 122:9-16. Loesche, W. J., S. S. Socransky, and R. J. Gibbons. 1964. Bacteroides oralis, proposed new species isolated from the oral cavity of man. J. Bacteriol. 88:1329-1337. Miyagawa, E., R. Azuma, and T. Suto. 1978. Distribution of sphingolipids in Bacteroides species. J. Gen. Appl. Microbiol. 24341-348. Miyagawa, E., R. Azuma, and T. Suto. 1979. Cellular fatty acid composition in gram-negative obligately anaerobic rods. J. Gen. Appl. Microbiol. 2541-5 1. Miyagawa, E., R. Azuma, and T. Suto. 1981. Peptidoglycan composition of gram-negative obligately anaerobic rods. J . Gen. Appl. Biol. 27:199-208. Miyagawa, E., and T. Suto. 1980. Cellular fatty acid composition in Bacteroides oralis and Bacteroides ruminicola. J. Gen. Appl. Biol. 26:331-343. Montgomery, L., B. Flesher, and D. Stahl. 1988. Transfer of Bacteroides succinogenes (Hungate) to Fibrobacter gen. nov. as Fibrobacter succinogenes comb. nov. and description of Fibrobacter intestinalis sp. nov. Int. J. Syst. Bacteriol. 38: 430435. Moore, L. V. H., E. P. Cato, and W. E. C. Moore. 1987. Anaerobe laboratory manual update. Virginia Polytechnic Institute and State University, Blacksburg. Moore, W. E. C., E. P. Cato, and L. V. H. Moore. 1985. Index of bacterial and yeast nomenclatural changes published in the International Journal of Systematic Bacteriology since the 1980 Approved Lists of Bacterial Names (1 January 1980 to January 1985). Int. J. Syst. Bacteriol. 35382407. Moore, W. E. C., L. V. Holdeman, R. M. Smibert, I. J. Good, J. A. Burmeister, K. G. Alcanis, and R. R. Ranney. 1982. Bacteriology of experimental gingivitis in young adult humans. Infect. Immun. 38:651467. Moore, W. E. C., L. V. Holdeman, R. M. Smibert, E. E. Hash, J. A. Burmeister, and R. R. Ranney. 1982. Bacteriology of severe periodontitis in young adult humans. Infect. Immun. 38:1137-1148. Okuda, K., T. Kato, J. Shiozu, I. Takazoe, and T. Nakamura. 1985. Bacteroides heparinolyticus sp. nov. isolated from humans with periodontitis. Int. J. Syst. Bacteriol. 35438442. Paster, B. J., W. Ludwig, W. G. Weisburg, E. Stackebrandt, R. B. Hespell, C. M. Hahn, H. Reichenbach, K. 0. Stetter, and C. R. Woese. 1985. A phylogenetic grouping of Bacteroides, cytophagas and certain flavobacteria. Syst. Appl. Microbiol. 6:3442. PrCvot, A. R. 1966. Manual for the classification and determi-
INT.J . SYST. BACTERIOL. nation of the anaerobic bacteria, 1st American edition. Lea & Febiger, Philadephia. (Translated by V. Fredette.) 38. Prbvot, A. R., A. Turpin, and P. Kaiser. 1967. Les bacteries anaerobis. Dunod, Paris. 39. Reddy, C. A., and M. P. Bryant. 1977. Deoxyribonucleic acid base composition of certain species of the genus Bacteroides. Can. J. Microbiol. 23:1252-1256. 40. Shah, H. N., and M. D. Collins. 1980. Fatty acid and isoprenoid quinone composition in the classification of Bacteroides melaninogenicus and related taxa. J . Appl. Bacteriol. 48:75-87. 41. Shah, H. N., and M. D. Collins. 1981. Bacteroides buccalis, sp. nov., Bacteroides denticola, sp. nov., and Bacteroides pentosaceus, sp. nov., new species of the genus Bacteroides from the oral cavity. Zentralbl. Bakteriol. Parasitenkd. Infektionskr . Hyg. Abt. 1 Orig. Reihe C 2:235-241. 42. Shah, H. N., and M. D. Collins. 1982. Reclassification of Bacteroides hypermegas (Harrison and Hansen) in a new genus Megamonas, as Megamonas hypermegas comb. nov. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. 1 Orig. Reihe C 3:394-398. 43. Shah, H. N., and M. D. Collins. 1982. Reclassification of Bacteroides multiacidus (Mitsuoka, Terada, Watanbe and Uchida) in a new genus Mitsuokella, as Mitsuokella rnultiacidus comb. nov. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. 1 Orig. Reihe C 3:491494. 44. Shah, H. N., and M. D. Collins. 1983. Genus Bacteroides: a chemotaxonomical perspective. J. Appl. Bacteriol. 55403416. 45. Shah, H. N., and M. D. Collins. 1986. Reclassification of Bacteroides furcosus Veillon and Zuber (Hauduroy , Ehringer, Urbain, Guillot and Magron) in a new genus Anaerorhabdus, as Anaerorhabdus furcosus comb. nov. Syst. Appl. Microbiol. 8:86-88. 46. Shah, H. N., and M. D. CoUins. 1988. Proposal for reclassification of Bacteroides asaccharolyticus, Bacteroides gingivalis, and Bacteroides endodontalis in a new genus, Porphyromonas. Int. J. Syst. Bacteriol. 38:128-131. 47. Shah, H. N., and M. D. Collins. 1989. Proposal to restrict the genus Bacteroides (Castellani and Chalmers) to Bacteroides fragilis and closely related species. Int. J. Syst. Bacteriol. 39:85-87. 48. Shah, H. N., M. D. Collins, J. Watabe, and T. Mitsuoka. 1985. Bacteroides oulorum sp. nov., a non-pigmented saccharolytic species from the oral cavity. Int. J. Syst. Bacteriol. 35193-197. 49. Shah, H. N., T. J. M. van Steenbergen, J. M. Hardie, and J. de Graaff. 1982. DNA base composition, DNA-DNA reassociation and isoelectric-focusing of proteins of strains designated Bacteroides oralis. FEMS Microbiol. Lett. 13:125-130. 50. Shah, H. N., and R. A. D. Williams. 1982. Dehydrogenase patterns in the taxonomy of Bacteroides. J . Gen. Microbiol. 128:2955-2965. 51. Shah, H. N., R. A. D. Williams, G. H. Bowden, and J. M. Hardie. 1976. Comparison of the biochemical properties of Bacteroides melaninogenicus from human dental plaque and other sites. J. Appl. Microbiol. 41:473492. 52. Stackebrandt, E., and H. Hippe. 1986. Transfer of Bacteroides amylophilus to a new genus Ruminobacter gen. nov., nom. rev. as Ruminobacter amylophilus comb. nov. Syst. Appl. Microbiol . 8:20&207. 53. van Steenbergen, T. J. M., A. J. van Winkelhoff, D. Mayrand, D. Grenier, and J. de Graaff. 1984. Bacteroides endodontalis sp. nov., an asaccharolytic black-pigmented Bacteroides species from infected dental root canals. Int. J. Syst. Bacteriol. 34: 118-120. 54. Watabe, J., Y.Benno, and T. Mitsuoka. 1983. Taxonomic study of Bacteroides oralis and related organisms and proposal of Bacteroides veroralis sp. nov. Int. J. Syst. Bacteriol. 3357-64. 55. Weinberg, M., R. Nativelle, and A. R. Prbvot. 1937. Les microbes anaerobies. Masson and Co., Paris.
Vol. 40. No. 2
NOTES Prevotella, a New Genus To Include Bacteroides melaninogenicus and Related Species Formerly Classified in the Genus Bacteroides HAROUN N. SHAH,l* AND DAVID M. COLLINS2 Department of Oral Microbiology, The London Hospital Medical College, London El 2AD,l and Agricultural and Food Research Council Institute of Food Research, Shinfield, Reading, RG2 9AT,2 United Kingdom It was recently proposed that the genus Bacteroides should be restricted to Bacteroides fragilis (the type species) and closely related organisms (viz., B . caccae, B . distusonis, B . eggerthii, B . merdae, B . ovatus, B . stercoris, B . thetaiotaomicron, B . unifomtis, and B . vulgatus). By contrast, the moderately saccharolytic, predominantly oral Bacteroides species, which include B . melaninogenicus, B. oralis, and related species, form a phenotypically and phylogenetically coherent group of species which differ so significantly from the emended description of the genus Bacteroides that they should not be classified in the same genus. Therefore, we formally propose that these species be reclassified in a new genus, Prevotella. The type species is Prevotella melaninogenica.
The genus Bacteroides has recently undergone major taxonomic revision (32, 46, 47). It is now universely accepted that this genus is phenotypically and phylogenetically heterogeneous. Several new genera, most of which are monospecific, have recently been proposed to accomodate some of the atypical members of the group (Table 1). The majority of the more typical members of the genus (particularly those associated with humans) form three broad groups on the basis of their ability to ferment carbohydrates (viz., saccharolytic, moderately saccharolytic, and asaccharolytic groups of species [for example, see references 17 and 19). The first group consists of Bacteroides fragilis and related species which are generally isolated from gastrointestinal tracts (lo), whereas the second group comprises a large number of moderately saccharolytic species and includes B . melaninogenicus, B. oralis, and related species. The third group includes the pigmented, asaccharolytic species B. asaccharolyticus and B . endodontalis and the important periodontal pathogen B. gingivalis (8, 3 3 , 34, 53). The recognition of three major groups within the genus Bacteroides is supported by biochemical (6,17,27,40,44) and rRNA cistron similarities (19). It has recently been proposed that the genus Bacteroides be restricted to highly fermentative species that phenotypically resemble B. fragilis, the type species of the genus (47), and include B. caccae, B. distasonis, B. eggerthii, B . merdae, B. ovatus, B. stercoris, B. thetaiotaomicron, B. uniformis, and B. vulgatus. Similarly, a new genus, Porphyromonas, has been created to provide a niche for the asaccharolytic species mentioned above (46). However, the position of the moderately saccharolytic species that do not grow well in 2% oxgall remains unresolved. Most species of this group are indigenous to oral cavities (17, 33, 34), and several (B. corporis, B. intermedius, B. loescheii, B. melaninogenicus, and some strains qf B. denticola [16, 171) produce pigmented colonies on blood agar. The nonpigmented members of this group are B. bivius, B. buccae, B . buccalis, B . disiens, B . heparinolyticus, B . oralis, B. oris, B .
oulorum, B . ruminicola, B . veroralis, and B. zoogleoformans. Phenotypically, these species are all similar and can be readily distinguished from members of the genus Bacteroides sensu stricto (47). In addition to their moderately saccharolytic potential and sensitivity to bile, they differ markedly from members of the genus Bacteroides in lacking enzymes of the pentose phosphate pathway-hexose monophosphate shunt (viz., glucose 6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase) (6, 44, 50) (Table 2). Thus, the moderately saccharolytic species are biochemically homogeneous (6, 17, 44), and all of the species examined to date form a phylogenetically (19, 36) coherent group that is quite distinct from the genus Bacteroides sensu stricto (47) and therefore warrant separate generic status. A new genus, Prevotella, is proposed for this group of species. A complete description of Prevotella gen. nov. is given below. Description of Prevotella gen. nov. Prevotella (Pre.vo. tel'la. M.L. dim.ending ella; M.L. fem. n. Prevotella, named after the French microbiologist A. R. PrCvot, a pioneer in anaerobic microbiology). The description below is based on our own observations TABLE 1. Species listed in Bergey's Manual of Systematic Bacteriology which have been reclassified" Species or group
Taxonomic status
Reference
B. fragilis and related species B. asaccharolyticus B. gingivalis B. endodontalis J B. furcosus B. succinogenes B. hypermegas B. multiacidus B. microfusus B. amylophilus B. termitidis B. praeacutus B. ochraceus
Bacteroides (emended definition)
47
Porphy romonas
46
Anaerorha bdus Fibrobacter Megamonas Mitsuokella Rikenella Ruminobacter Se baldella Tissierella Capnocy tophaga
45 30 42 43 7 52
1
* Corresponding author.
" See reference 17. 205
4 5
24
206
NOTES
INT. J. SYST.BACTERIOL.
TABLE 2. Major ecological, biochemical, and chemical characteristics of the genera Prevotella and Bacteroides Usual site of isolation
Genus
Prevotella
Oral cavity, upper respiratory and urogenital tractse Gastrointestinal tract
Bacteroides sensu strict0
p
bile salts' to
~
Metabolismb ~ ~
S
ed
MF
R
-
F
MDH
+ +
~
Presence of c: ~ ~ G6PDH
GDH
+ +
n 6PGDH
-
-
+
+
' S, Sensitive; R, resistant. F, Fermentative; MF, moderately fermentative. MDH, Malate dehydrogenase; GDH, glutamate dehydrogenase; G6PDH, glucose 6-phosphate dehydrogenase; 6PGDH, 6-phosphogluconate dehydrogenase. Only some species produce pigment. Except B. nuninicola subspecies.
and on previous descriptions of the species (1-3, 6, 11-18, 20-23, 25-29, 31, 35, 37-41, 44, 48-51, 54, 55). Gramnegative, obligately anaerobic, nonsporeforming, nonmotile, pleomorphic rods. Surface colonies on blood agar plates vary from minute to 2.0 mm in diameter and are generally circular, entire, convex, shiny, and smooth. Colonies on blood agar are translucent, opaque, grey, light brown, or black. Hemolysis is variable. Glucose broth cultures are usually turbid with smooth or stringy sediments, and the terminal pH is between 4.5 and 5.2. The glucose utilization varies between 30 and 90% in BM (51) broth. The optimum temperature for growth is 37"C, but some strains grow at 25 and 45°C. Growth of most species is inhibited by 6.5% NaCl. Hemin and menadione are required for growth of most species. Growth is inhibited by 20% (wtlvol) bile. The major fermentation products from BM (51) medium or peptoneyeast extract-glucose medium (31) are acetic and succinic acids; occasionally lower levels of isobutyric, isovaleric, or lactic acid are produced. Malate dehydrogenase and glutamate dehydrogenase are present; glucose 6-phosphate dehyrogenase and 6-phosphogluconate dehydrogenase are absent. Proteolytic activity is variable. Most species have limited abilities to ferment amino acids. Nearly all species are indole negative. Nitrate is not reduced to nitrite. The cell wall peptidoglycan contains meso-diaminopimelicacid. The
principal respiratory quinones are unsaturated menaquinones with 10 to 13 isoprene units. Both nonhydroxylated and 3-hydroxylated fatty acids are present. The nonhydroxylated fatty acids are composed of predominantly straightchain saturated, anteiso- and iso-methyl, branched-chain types. Sphingolipids are produced. The DNA base compositions are within the approximate range of 40 to 52 mol% guanine plus cytosine. The type species of the genus Prevotella is Prevotella melaninogenica (Oliver and Wherry 1921) comb. nov. Other currently described species which conform to the generic description of Prevotella include B. bivius, B. buccae, B. buccalis, B. corporis, B. denticola, B. disiens, B. herparinolyticus, B. intemedius, B. loescheii, B. melaninogenicus, B. oralis, B. oris, B. oulorum, B. ruminicola, B. veroralis, and B. zoogleoformans. Phenotypic tests which are useful for the differentiation of these species are shown in Table 3. Description of PrevoteUa mehninogenica (Oliver and Wherry 1921) Shah and Collins 1990 comb. nov. A complete description of Prevotella melaninogenica is given in references 16 and 17. The type strain is strain ATCC 25845 (= Finegold B282 = VPI 4196). Description of Prevotelh bivia (Holdeman and Johnson 1977) comb. nov. A complete description of Prevotella bivia
TABLE 3. Distinguishing characteristics of species of the genus Prevotella
P. melaninogenica P. bivia P. buccae P. buccalis P. corporis P. denticola P. disiens P. heparinotytica P. intermedia P. loescheii P. oralis P. oris P. oulora P. ruminicola P. veroralis P. zoogleoformans
-
+b
-
-
-
+
+
-
-
-
-
-
-
-
-
-
-
+ -
+
+ +
-
-
~
f
+ -
-
+ +-
+(-)
-
-
-
-
+ -
-
+
+ + + ++ + -(+) + ++
+/w
+lw
+
-
-
v
v
-
+ +
-
+ -
a Tested by using the RapID-ANA system (9). +, Positive reaction; -, negative reaction; +/w, weak positive reaction; negative; v, variable reactions.
+/w -
V
+ + ++ + + + + + + + +
2 , positive
+ + + ++ + + +
+ +
+/w
+ +
-
-
-
+ + ++
+ + -(+) +(-) -++ + + -(+) +
+
++ + ++ ++ + +
+ +
+(-)
+ + ++ +(-) + ++ + + +
-
-
+ + - +
-
-
-
-
+ +
+(->
-+ ++ - + V
+
+ + -
5 -
or negative reaction; +(-), most reactions positive; -(+), most reactions
VOL. 40, 1990
is given in references 15 and 17. The type strain is strain ATCC 29303 (= NCTC 11156). Description of Prevotella buccae (Bacteroides pentosaceus Shah and Collins 1982; Bacteroides capillus Kornman and Holt 1982) (Holdeman, Moore, Churn, and Johnson 1982) comb. nov. A complete description of Prevotella buccae is given in references 17, 18, 21, 22, and 41. The type strain is strain ATCC 33574 (= VPI D3A-6). Description of Prevotella buccalis (Shah and Collins 1982) comb. nov. A complete description of Prevotella buccalis is given in references 31 and 41. The type strain is strain ATCC 35310 (= NCDO 2354 = DSM 20616). Description of PrevuteUa corporis (Johnson and Holdeman 1983) comb. nov. A complete description Prevotella corporis is given in references 17 and 20. The type strain is strain ATCC 33547 (= VPI 9342 = Lambe 532-70A). Description of Prevotella denticola (Shah and Collins 1982) comb. nov. A complete description of Prevotella denticola is given in references 16, 41, and 44. The type strain is strain NCDO 2352 (= Socransky 1210). Description of Prevotella disiens (Holdeman and Johnson 1977) comb. nov. A complete description of Prevotella disiens is given in references 15 and 17. The type strain is strain ATCC 29426 (= NCTC 11157). Description of Prevotella heparinolytica (Okuda, Kato, Shiozu, Takazoe, and Nakamura 1985) comb. nov. A complete description of Prevotella heparinolytica is given in references 31 and 35. The type strain is strain ATCC 35895 (= HEP). Description of Prevotella intemediu (Holdeman and Moore 1970) comb. nov. A complete description of Prevotella intermedia is given in references 17 and 20. The type strain is strain ATCC 25611 (= Finegold B422 = VPI 4197). Description of Prevotella loescheii (Holdeman and Johnson 1982) comb. nov. A complete description of Prevotella loescheii is given in references 16 and 17. The type strain is strain ATCC 15930 (= NCTC 11321 = VPI 9085 = Loesche 8B). Description of Prevotella oralis (Loesche, Socransky, and Gibbons 1964) comb. nov. A complete description of Prevotella oralis is given in references 17 and 25. The type strain is strain ATCC 33269 (= VPI D27B-24). Description of PrevoteUa oris (Holdeman, Moore, Churn, and Johnson 1982) comb. nov. A complete description of Prevotella oris is given in references 17 and 18. The type strain is strain ATCC 33573 (= VPI DIA-1A). Description of PrevoteUa oulora (Shah, Collins, Watabe, and Mitsuoka (1985) comb. nov. A complete description of Prevotella oulora is given in references 31 and 48. The type strain is strain NCTC 11871 (= WPH 179) Description of Prevotella ruminicola (Bryant, Small, Bouma, and Chu 1958) comb. nov. A complete description of Prevotella ruminicola is given in references 2 and 17. The type strain is strain ATCC 19189. Description of PrevoteUa veroralis (Watabe, Benno, and Mitsuoka 1983) comb. nov. A complete description of Prevotella veroralis is given in references 31 and 54. The type strain is strain ATCC 33779 (= VPID22A-7). Description of PrevoteUa zoogleoformans (Weinberg, Nativelle, and Prevot 1937) comb. nov. A complete description of Prevotella zoogleoformans is given in references 3, 37, 38 and 55. The type strain is strain ATCC 33285. LITERATURE CITED 1. Bailey, G. D., L. V. H. Moore, D. N. Love, and J. L. Johnson. 1988. Bacteroides heparinolyticus: deoxyribonucleic acid relat-
NOTES
2.
3.
4.
5.
6.
7.
8.
207
edness of strains from the oral cavity and oral-associated disease conditions from horses, cats, and humans. Int. J. Syst. Bacteriol. 38:42-44. Bryant, M. P., I. M. Robinson, C. Bouma, and H. Chu. 1958. Bacteroides ruminicola n. sp. and the new genus and species Succinirnonas amylolytica. Species of succinic acid-producing anaerobic bacteria of the bovine rumen. J. Bacteriol. 76:15-23. Cato, E. P., R. W. Kelley, W. E. C. Moore, and L. V. Holdeman. 1982. Bacteroides zoogleoformans (Weinberg, Nativelle, and Prkvot 1983) comg., comb. nov.: emended description. Int. J. Syst. Bacteriol. 32:271-274. Collins, M. D., and H. N. Shah. 1986. Reclassification of Bacteroides termitidis Sebald (Holdeman and Moore) in a new genus Sebaldella, as Sebaldella termiditis comb. nov. Int. J. Syst. Bacteriol. 36:349-350. Collins, M. D., and H. N. Shah. 1986. Reclassification of Bacteroides praeacutus Tissier (Holdeman and Moore) in a new genus, Tissierella, as Tissierella praeacuta comb. nov. Int. J. Syst. Bacteriol. 36:461-463. Collins, M. D., and H. N. Shah. 1987. Recent advances in the taxonomy of the genus Bacteroides, p. 249-258. In S. P. Borriello, J. M. Hardie, B. S. Drasar, B. I. Duerden, M. J. Hudson, and R. J. Lyson (ed.), Recent advances in anaerobic bacteriology. Martinus Nijhoff Publishers, Dordrecht, The Netherlands. Collins, M. D., H. N. Shah, and T. Mitsuoka. 1985. Reclassification of Bacteroides microfusus (Kaneuchi and Mitsuoka) in a new genus Rikenella, as Rikenella microfusus comb. nov. Syst. Appl. Microbiol. 6:79-81. Coykendall, A. L., F. S. Kaczmarek, and J. Slots. 1980. Genetic heterogeneity in Bacteroides asaccharolyticus (Holdeman and Moore 1970) Finegold and Barnes 1977 (Approved Lists, 1980) and proposal of Bacteroides gingivalis sp. nov. and Bacteroides macacae (Slots and Genco) comb. nov. Int. J. Syst. Bacteriol. 30559-564.
9. Dellinger, C. A., and L. V. H. Moore. 1986. Use of the RapID-ANA system to screen for enzyme activities that differ among species of bile-inhibited Bacteroides. J. Clin. Microbiol. 23:289-293. 10. Finegold, S. M. 1977. Anaerobic bacteria in human disease. Academic Press, Inc., New York. 11. Haapasalo, M., K. Lounatmaa, H. Ranta, H. Shah, and K. Ranta. 1985. Ultrastructures of Bacteroides capillus, Bacteroides buccae, Bacteroides pentosaceus, Bacteroides oris, Bacteroides oralis, Bacteroides veroralis, and pentose sugar-fermenting Bacteroides species from humans with periapical osteitis: occurrence of external proteinaceous cell wall layer. Int. J. Syst. Bacteriol. 35:65-75. 12. Hammann, R., and H. Werner. 1981. Presence of diaminopimelic acid in propionate-negative Bacteroides species and in some butyric acid-producing strains. J. Med. Microbiol. 14: 205-212. 13. Holbrook, W. P., and B. I. Duerden. 1974. A comparison of some characteristics of reference strains of Bacteroides oralis with Bacteroides melaninogenicus. Arch. Oral Biol. 19:12311235. 14. Holbrook, W. P., B. I. Duerden, and A. G. Deacon. 1977. The classification of Bacteroides melaninogenicus and related species. J. Appl. Bacteriol. 43:259-273. 15. Holdeman, L. V., and J. L. Johnson. 1977. Bacteroides disiens sp. nov. and Bacteroides bivius sp. nov. from human clinical infections. Int. J. Syst. Bacteriol. 27:337-345. 16. Holdeman, L. V., and J. L. Johnson. 1982. Description of Bacteroides loescheii sp. nov. and emendation of the descriptions of Bacteroides melaninogenicus (Oliver and Wherry) Roy and Kelly 1939 and Bacteroides denticola Shah and Collins 1981. Int. J. Syst. Bacteriol. 32:399-409. 17. Holdeman, L. V., R. W. Kelly, and W. E. C. Moore. 1984. Genus I. Bacteroides Castellani and Chalmers 1919, 959 p. 604-631. In N. R. Krieg and J. G. Holt (ed.), Bergey’s manual of systematic bacteriology. The Williams & Wilkins Co., Baltimore. 18. Holdeman, L. V., W. E. C. Moore, P. J. Churn, and J. L. Johnson. 1982. Bacteroides oris and Bacteroides buccae, new
208
19. 20.
21.
22.
23. 24. 25. 26. 27. 28. 29. 30.
31. 32.
33.
34.
35. 36.
37.
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INT.J . SYST. BACTERIOL. nation of the anaerobic bacteria, 1st American edition. Lea & Febiger, Philadephia. (Translated by V. Fredette.) 38. Prbvot, A. R., A. Turpin, and P. Kaiser. 1967. Les bacteries anaerobis. Dunod, Paris. 39. Reddy, C. A., and M. P. Bryant. 1977. Deoxyribonucleic acid base composition of certain species of the genus Bacteroides. Can. J. Microbiol. 23:1252-1256. 40. Shah, H. N., and M. D. Collins. 1980. Fatty acid and isoprenoid quinone composition in the classification of Bacteroides melaninogenicus and related taxa. J . Appl. Bacteriol. 48:75-87. 41. Shah, H. N., and M. D. Collins. 1981. Bacteroides buccalis, sp. nov., Bacteroides denticola, sp. nov., and Bacteroides pentosaceus, sp. nov., new species of the genus Bacteroides from the oral cavity. Zentralbl. Bakteriol. Parasitenkd. Infektionskr . Hyg. Abt. 1 Orig. Reihe C 2:235-241. 42. Shah, H. N., and M. D. Collins. 1982. Reclassification of Bacteroides hypermegas (Harrison and Hansen) in a new genus Megamonas, as Megamonas hypermegas comb. nov. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. 1 Orig. Reihe C 3:394-398. 43. Shah, H. N., and M. D. Collins. 1982. Reclassification of Bacteroides multiacidus (Mitsuoka, Terada, Watanbe and Uchida) in a new genus Mitsuokella, as Mitsuokella rnultiacidus comb. nov. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. 1 Orig. Reihe C 3:491494. 44. Shah, H. N., and M. D. Collins. 1983. Genus Bacteroides: a chemotaxonomical perspective. J. Appl. Bacteriol. 55403416. 45. Shah, H. N., and M. D. Collins. 1986. Reclassification of Bacteroides furcosus Veillon and Zuber (Hauduroy , Ehringer, Urbain, Guillot and Magron) in a new genus Anaerorhabdus, as Anaerorhabdus furcosus comb. nov. Syst. Appl. Microbiol. 8:86-88. 46. Shah, H. N., and M. D. CoUins. 1988. Proposal for reclassification of Bacteroides asaccharolyticus, Bacteroides gingivalis, and Bacteroides endodontalis in a new genus, Porphyromonas. Int. J. Syst. Bacteriol. 38:128-131. 47. Shah, H. N., and M. D. Collins. 1989. Proposal to restrict the genus Bacteroides (Castellani and Chalmers) to Bacteroides fragilis and closely related species. Int. J. Syst. Bacteriol. 39:85-87. 48. Shah, H. N., M. D. Collins, J. Watabe, and T. Mitsuoka. 1985. Bacteroides oulorum sp. nov., a non-pigmented saccharolytic species from the oral cavity. Int. J. Syst. Bacteriol. 35193-197. 49. Shah, H. N., T. J. M. van Steenbergen, J. M. Hardie, and J. de Graaff. 1982. DNA base composition, DNA-DNA reassociation and isoelectric-focusing of proteins of strains designated Bacteroides oralis. FEMS Microbiol. Lett. 13:125-130. 50. Shah, H. N., and R. A. D. Williams. 1982. Dehydrogenase patterns in the taxonomy of Bacteroides. J . Gen. Microbiol. 128:2955-2965. 51. Shah, H. N., R. A. D. Williams, G. H. Bowden, and J. M. Hardie. 1976. Comparison of the biochemical properties of Bacteroides melaninogenicus from human dental plaque and other sites. J. Appl. Microbiol. 41:473492. 52. Stackebrandt, E., and H. Hippe. 1986. Transfer of Bacteroides amylophilus to a new genus Ruminobacter gen. nov., nom. rev. as Ruminobacter amylophilus comb. nov. Syst. Appl. Microbiol . 8:20&207. 53. van Steenbergen, T. J. M., A. J. van Winkelhoff, D. Mayrand, D. Grenier, and J. de Graaff. 1984. Bacteroides endodontalis sp. nov., an asaccharolytic black-pigmented Bacteroides species from infected dental root canals. Int. J. Syst. Bacteriol. 34: 118-120. 54. Watabe, J., Y.Benno, and T. Mitsuoka. 1983. Taxonomic study of Bacteroides oralis and related organisms and proposal of Bacteroides veroralis sp. nov. Int. J. Syst. Bacteriol. 3357-64. 55. Weinberg, M., R. Nativelle, and A. R. Prbvot. 1937. Les microbes anaerobies. Masson and Co., Paris.
