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Complete Article JOURNAL OF BACTERIOLOGY, Dec. 1967, p. 2037-2047 Vol. 94, No. 6 Copyright © 1967 American Society for Microbiology Printed in U.S.A. Cell Wall Composition in Relation to the Taxonomy of Some Actinoplanaceae' PAUL J. SZANISZLO2 AND HARRY GOODER Department of Botany and Department of Bacteriology, University of North Carolina, Chapel Hill, North Carolina 27514 Received for publication 11 September 1967 Hydrolytic residues of the cell walls of 48 strains of Actinoplanaceae, previously assigned to 10 species and the four genera, Actinoplanes, Ampullariella, Amorpho- sporangium, and Pilimelia, were examined by paper chromatography and column chromatography. Comparisons were made for taxonomic purposes between the groupings obtained, by use of chemical characters and the groupings currently recognized morphologically. Most of the species investigated had qualitatively dis- tinct cell wall compositions. Often, however, the cell wall compositions of species in different genera were more similar, in some respects, than were those of species in the same genus. Quantification of the cell wall amino acids and amino sugars substan- tiated that cross-generic similarities existed. Based on these results and the morpho- logical conclusions reached by other investigators, a single-genus concept is sug- gested for the Actinoplanaceae examined. Existing schemes of bacterial classification often The present investigation was undertaken to need re-examination to determine whether tra- compare the cell wall composition of numerous ditional criteria are obscuring natural relation- strains of Actinoplanes, Ampullariella, and Amor- ships. Among the Actinoplanaceae (Actinomy- phosporangium to determine whether the tra- cetales), many species are placed in their genus ditional criteria are obscuring natural relation- category on the basis of a relatively few morpho- ships among species presently classified in these logical characters. This often necessitates classi- genera. Three strains of keratinophilic Actino- fying similar Actinoplanaceae into different planaceae were also examined. Couch (5) specu- genera. The most notable examples occur among lated that such Actinoplanaceae probably belong the species which are morphologically and cul- in the genus Ampullariella. However, Kane (12) turally very similar to Actinoplanes philippinensis, reported that morphological and cultural differ- the species on which the family Actinoplanaceae ences warranted placing the keratinophilic strains is based. These species are classified among three she studied in a new genus which she named genera predominantly on the basis of sporangio- Pilimelia. spore morphology (5, 6). Species producing While this investigation was in progress, sporangiospores morphologically similar to those Yamaguchi (23) and Becker, Lechevalier, and produced by Actinoplanes philippinensis (sub- Lechevalier (1) reported on the cell wall compo- spherical with a tuft of are sition of various aerobic actinomycetes. Their polar flagella) placed investigations revealed that strains of Actino- in the genus Actinoplanes. Species producing rod- planes, Ampullariella, and Amorphosporangium shaped sporangiospores with a tuft of polar flag- had similar, but not necessarily identical, cell ella are placed in the genus Ampullariella, and wall compositions. However, the investigations species producing rod-shaped sporangiospores of Yamaguchi and Becker et al. did not involve with no flagella are placed in the genus Amor- sufficient numbers of these Actinoplanaceae to phosporangium. allow for extensive speculation on the validity of 1 Part of a dissertation submitted to the faculty of their classification among three genera. the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree MATERIALS AND METHODS of Doctor of Philosophy in the Department of Botany. Organisms. The name, number, and general loca- 2 Present address: Laboratory of Applied Micro- tion of the original collection site of each laboratory biology, Division of Engineering and Applied Physics, stock strain examined are listed in Table 1. The strains Harvard University, Cambridge, Mass. 02138. of Actinoplanes, Ampullariella, and Amorphosporan- 2037 2038 SZANISZLO AND GOODER J. BACTERIOL. TABLE 1. Name, number, and general location of original collection site of each strain investigated Organism Strain no. Collection site I ~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~I_ Actinoplanes philippinensis.............. 2 Philippine Islands Actinoplanes utahensis.................. 258 Salt Lake City, Utah 259 Salt Lake City, Utah 260 Salt Lake City, Utah 261 Dunphy, Nev. Actinoplanes missouriensis............... 221 Palonio Pass, Calif. 222 Sierra Nevada Pass, Calif. 263 Dunphy, Nev. 267 Rainbow Valley, Wyo. 431 Hamilton, Mo. 443 Cameron, Mo. 657 North Bend, Ore. 825 Checotale, Okla. Ampullariella regularis.................. 28 Chapel Hill, N. C. 79 Madison, Wis. 154 Clemson, S. C. 164 Grenada County, Miss. 168 Grenada County, Miss. 312 Draper, Va. 395 Indianapolis, Ind. 850 Chapel Hill, N. C. 915 Joyce Kilmer National Park Ampullariella digitata................... 33 Cheboygan, Mich. 71 Madison, Wis. 118 Chapel Hill, N. C. 131 Chapel Hill, N. C. 137 Hindhead, England 370 Chillicothe, Ohio 386 Indianapolis, Ind. 399 Indianapolis, Ind. Ampullariella lobata..................... 72 Madison, Wis. 74 Madison, Wis. 337 Draper, Va. Ampullariella campanulata............... 65 Douglas, Kan. 126 Chapel Hill, N. C. 151 Chapel Hill, N. C. 182 Durham County, N. C. 640 Tahiti 641 Tahiti 642 Tahiti 643 Borabora Ampullariella sp......................... 1492 Bombay, India 1539 Mahabalipuram, India Amorphosporangium auranticolor. 253 Dunphy, Nev. 262 Dunphy, Nev. Pilimelia anulata........................ 1 Walkerton, Ind. Pilimelia terevasa....................... 1 Walkerton, Ind. Pilimelia sp............................. 1777 Hyderabad, India gium were identified by J. N. Couch (3, 4, 5, 6), and 1,000 ml of Czapek Dox broth (Difco), fortified with stock cultures of each strain are maintained in his 5 g of peptone (Difco), housed in 1,500-ml low-form laboratory on Czapek agar (Difco) and peptone- flasks, by suspending adequate amounts of each Czapek agar (Czapek agar fortified with 5 g/l ,000 ml strain in 50 ml of sterile broth and blending for 60 of Difco peptone). The strains of Pilimelia were sec at high speed in a cold Waring Blendor micro-cup. identified by W. D. Kane (12) and are maintained After inoculation, the cultures were grown for 5 days by her on peptone-Czapek agar. at 24 to 26 C with continuous agitation (100 strokes/ Medium and culture method. The organisms from min) on a gyratory shaker (model G-10, New Bruns- 3-week-old slants were prepared for inoculation into wick Scientific Co., New Brunswick, N.J.). The re- VOL. 94, 1967 CELL WALL COMPOSITION IN ACTINOPLANACEAE 2039 sulting vegetative hyphae were harvested by centrifu- both separately and after admixture with the hy- gation at 3,000 X g and washed three times with drolytic samples. distilled water. Galactose and glucose identification. When both Preparation of cell walls. The hyphae were me- galactose and glucose were present together, as in the chanically disrupted in a Braun homogenizer by the hydrolysate of walls of Actinoplanes philippinensis method of Bleiweis, Karakawa, and Krause (2). strain 2, the identity of each was verified by adding Disrupted suspensions were centrifuged at 10,000 X g separately and together glucose oxidase (0.5 unit) for 10 min. Hyphae with any remaining intact cells and galactose oxidase (0.125 unit) to hydrolysate in their length formed a tightly packed, colored layer samples containing 0.8-mg equivalent of wall material. at the bottom of the centrifuge tube. Completely Enzyme mixtures were incubated for 2 hr at 37 C, disrupted hyphae were devoid of color and formed a and the entire sample was then chromatographed to loosely packed, upper white layer, which was rinsed away from the colored layer by repeated washes with test for the disappearance of the respective sugar or distilled water. The cell walls were collected by sugars. centrifugation, treated for two periods of 1 hr each Deoxyhexose identification. Relatively pure samples in 1% sodium lauryl sulfate, rewashed thoroughly in of the fast-running sugar detected in wall hydrolysates distilled water, and lyophilized. were obtained by chromatographing as a band the Enzyme treatment of walls. Lyophilized walls in combined H2SO4 hydrolysates of 37 mg of cell walls, 100-mg amounts were treated with 10 mg of crystalline with BAW as solvent. After the position of the sugar ribonuclease in 10 ml of 0.1 M phosphate buffer was located with test strips, the band was eluted from (pH 7.8) for 3 hr at 37 C, then 5 mg of crystalline the paper and the eluate filtered through a washed trypsin was added, and incubation was continued filter, 0.45 , pore size (Millipore Corp., Bedford, for 3 hr at 37 C. The walls were deposited by centrifu- Mass.), and then taken to dryness over P205. Wash gation, washed three times with distilled water, sus- water from a blank chromatogram was similarly pended in 20 ml of 0.2 N HCI containing crystalline treated and used as a control. Both residues were pepsin (1 mg/ml), and incubated overnight at 37 C. taken up in 2 ml of distilled water. Samples of the The walls were collected by centrifugation, thoroughly sugar solution and control were subjected to the washed with distilled water, lyophilized, and used in Dische spectrophotometric procedure (9) for
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