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Serpula Hyodysenteriae Comb INTERNATIONALJOURNAL OF SYSTEMATICBACTERIOLOGY, Jan. 1991, p. 50-58 Vol. 41, No. 1 0020-7713/91/0 10050-09$02.00/0 Copyright 0 1991, International Union of Microbiological Societies Reclassification of Treponema hyodysenteriae and Treponema innocens in a New Genus, Serpula gen. nov., as Serpula hyodysenteriae comb. nov. and Serpula innocens comb. nov. T. B. STANTON,l* N. S. JENSEN,l T. A. CASEY,l L. A. TORDOFF,2 F. E. DEWHIRST,2 AND B. J. PASTER2 Physiopathology Research Unit, National Animal Disease Center, Agricultural Research Service, U.S.Department of Agriculture, Ames, Iowa 50010,l and Forsyth Dental Center, Boston, Massachusetts 021152 The intestinal anaerobic spirochetes Treponema hyodysenteriae B7ST (T = type strain), B204, B169, and A-1, Treponema innocens B256T and 4/71, Treponema succinifaciens 6091T, and Treponema bryantii RUS-lT were compared by performing DNA-DNA reassociation experiments, sodium dodecyl sulfate-polyacrylamide gel electrophoresis of cell proteins, restriction endonuclease analysis of bNA, and 16s rRNA sequence analysis. DNA-DNA relative reassociation experiments in which the S1 nuclease method was used showed that T. hyodysenteriae B78T and B204 had 93% sequence homology with each other and approximately 40% sequence homology with T. innocens B256T and 4/71. Both T. hyodysenteriae B7ST and T. innocens B256T exhibited negligible levels of DNA homology (55%)with T. succinifaciens 6091T. The results of comparisons of protein electrophoretic profiles corroborated the DNA-DNA reassociation results. We found high levels of similarity (296%) in electrophoretic profiles among T. hyodysenteriae strains, moderate levels of similarity (43 to 49%) between T. hyodysenteriae and T. innocens, and no detectable similarity between the profiles of either T. hyodysenteriae or T. innocens and those of T. succinifaciens, T. bryantii, and Escherichiu coli. Restriction endonuclease analysis of DNA was not useful in assessing genetic relationships since there was heterogeneity even between strains of T. hyodysenteriae. Partial 16s rRNA sequences of the intestinal spirochetes were determined by using a modified Sanger method and were compared in order to evaluate the phylogenetic relationships among these and other spirochetes. The 16s rRNA sequences of T. hyodysenteriae B7ST, B204, and A-1 were nearly identical (99.8 to 99.9% base sequence similarity). T. innocens B256Tand 4/71 were closely related to the T. hyodysenteriae strains (99.4 and 99.0% similarity). Strains of T. hyodysenteriae and T. innocens exhibited low levels of 16s rRNA similarity (average, 76.5 %) with T. pallidum, Borrelia burgdorj'eri, and various other spirochetes. The results of our investigations indicate that T. hyodysenteriae and T. innocens are distinct but related species of spirochetes. T. hyodysenteriae and T. innocens are only distantly related to T.pallidum, the type species of the genus Treponema, and to other spirochetes. Consequently, we propose that the species T. hyodysenteriae and T. innocens be transferred to a new genus, Serpula, gen. nov. The bacterial agent of swine dysentery was established by T. innocens are genetically distinct from other known spiro- Taylor and Alexander in the United Kingdom (49) and by chetes, including other Treponema species. The guanine- Harris et al. in the United States (11). This organism has a plus-cytosine (G+C) content of DNA from either T. hyod- typical spirochete ultrastructure (protoplasmic cylinder, ysenteriae B204 or T. innocens B256T was estimated to be endoflagella, and outer sheath) and requires anaerobic con- 25.8 mol% (35). This value is significantly lower than the ditions for cultivation (9, 11, 22). Inasmuch as host-associ- value of 53 mol% reported for the DNA of Treponema ated, anaerobic spirochetes are classified as members of the pallidurn (34), the type species of the genus Treponema (42). genus Treponema (42), the agent of swine dysentery was T. hyodysenteriae B204 and A-1 and T. innocens B256T named Treponema hyodysenteriae (11). exhibited negligible levels of DNA sequence homology Initially, both pathogenic and nonpathogenic strains were (4%)with T. pallidum Nichols, Treponema phagedenis classified as T. hyodysenteriae (24). Colonies of nonpatho- biotype Reiter, or Treponema refringens biotype Noguchi genic strains were described as weakly beta-hemolytic, (35). 16s rRNA catalog comparisons have shown that T. whereas those of pathogenic strains were described as hyodysenteriae 94A007 (a subculture of strain B204) has strongly beta-hemolytic (24). More recently, Miao et al. (35) unique 16s rRNA regions that distinguish it from various found a level of relative reassociation of 28% between DNAs other spirochetes, including members of the genera Spiro- from pathogenic strains B204 and A-1 and DNAs from chaeta, Treponema, Leptospira, and Borrelia (38). T. hyod- nonpathogenic strains B256T (T = type strain) and 4/71. ysenteriae has been considered a distinct line of spirochete Strains B204 and A-1 exhibited 80% DNA sequence homol- evolution and, accordingly, a representative of a distinct ogy with each other, and the nonpathogenic strains exhibited spirochete genus (38). Neither the study of levels of DNA 90% sequence homology with each other. These results sequence homology between spirochetes (35) nor the 16s indicated that the pathogenic strains and the nonpathogenic rRNA cataloging study of spirochetes (38) included an strains are genetically distinct species. The nonpathogenic analysis of strain B78, the type strain of T. hyodysenteriae. organisms were reclassified as a new species, Treponema In addition, the 16s rRNA from T. innocens was not innocens, represented by type strain B256 (23). analyzed. There is substantial evidence that T. hyodysenteriae and In this study we used sodium dodecyl sulfate (SDS)- polyacrylamide gel electrophoresis (PAGE) of cell proteins, 16s rRNA sequence analysis, restriction endonuclease anal- * Corresponding author. ysis of DNA, and DNA-DNA reassociation experiments to 50 VOL.41, 1991 SERPULA GEN. NOV. 51 TABLE 1. Spirochete species used in this study G+C content Species Strain (rnol%) Characteristics Reference(s) Serpula hyodysenteriae" B7gT 26 Pathogen, swine intestine 23, 24 B 204 Pathogen, swine intestine 23, 24, 35 B169 Pathogen, swine intestine 23, 24 A- 1 Pathogen, swine intestine 23, 24 Serpula innocens B256T 26 Nonpathogen, swine intestine 23, 24, 35 4/7 1 Nonpathogen, swine intestine 23, 24 T. succinifaciens 6091T 36 Nonpathogen, swine intestine 6 T. bryantii RUS-lT 36 Nonpathogen, bovine rumen 46 a Serpula hyodysenteriue B7gT, B204, B169, and A-1 represent serotypes 1 through 4, respectively (2). compare strains of spirochetes, focusing on strains isolated resolving gel), using standard electrophoretic techniques from mammalian gastrointestinal tracts. On the basis of our (27). Proteins were stained with Coomassie blue R-250. results and the results of previous investigators, we propose Electrophoretic similarities between bacteria were evaluated a revision of the classification of T. hyodysenteriae and T. by visually examining photographs of gels and estimating the innocens and creation of a new genus, Serpula, containing percentages of protein bands with common alignments and the species Serpula hyodysentertae and Serpula innocens. relative staining intensities. Protein standards for molecular We also describe methods which can be used to distinguish weight determinations were purchased from Bio-Rad Labo- these species from each other and from other spirochetes. ratories, Richmond, Calif. Restriction endonuclease analysis. T. succinifaciens 6091T MATERIALS AND METHODS DNA was isolated as described above. Otherwise, bacterial DNAs were obtained by ultracentrifugation (Beckman type Bacterial strains. The spirochete strains used in this study Vti 65 rotor, 4 h, 404,000 x g) of cell lysates in a CsCl are shown in Table 1. In accordance with our proposal to solution as described by Hull et al. (14). DNAs were digested designate a new genus for T. hyodysenteriae and T. inno- with endonucleases BglII (Bethesda Research Laboratories, cens, the names Serpula hyodysenteriae and Serpula inno- Inc. , Gaithersburg, Md.), Hind111 (Bethesda Research Lab- cens are used in Table 1 and below. The conditions used for oratories), and Sau3A (Boehringer Mannheim, Indianapolis, culturing and maintaining bacteria and additional strain Ind.) by using incubation conditions recommended by the characteristics have been described elsewhere (6, 23, 24, 35, manufacturers. DNA fragments were separated in a 0.8% 46,47). Cells were harvested during the exponential phase of agarose gel by horizontal electrophoresis (40). growth. 16s rFWA isolation and sequencing. rRNAs were isolated DNA-DNA reassociation. The levels of DNA sequence and partially purified by using a modification of the proce- homology among the various spirochetes were estimated dure of Pace et al. (36), as previously described (37). The 16s from the results of DNA-DNA reassociation experiments. rRNA sequences of bacteria were determined by using an DNA was extracted from bacterial cells (2 to 3 g, wet weight) adaptation of the Sanger dideoxy chain termination tech- by using the techniques of Marmur (33), except that protein- nique (28). Primers complementary to conserved regions of ase K (total weight, 2 mg) was added after cell lysis by the 16s rRNA sequences were elongated by reverse tran- lysozyme-SDS and cell lysates were incubated for 3 to 4 h at scriptase. Eight primers were used to determine
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