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Micrococcus Kris Tinae INTERNATIONAL JOURNAL of SYSTEMATIC BACTERIOLOGY Vol. 24,No. 1 January 1974, p. 79-101 Printed in U.S.A. Copyright 0 1974 International Association of Microbiological Societies Isolation and Characterization of Micrococci From Human Skin, Including Two New Species: Micrococcus ZyZae and Micrococcus kris tinae WESLEY E. KLOOS, THOMAS G. TORNABENE, and KARL H. SCHLEIFER Department of Genetics, North Carolina State University, Raleigh, North Carolina 2 760 7; Department of Microbiology, Colorado State University, Fort Collins, Colorado 80521; and Botanisches Institut der Universitat Miinchen, 8 Miinchen 19, Germany Micrococci were commonly isolated from the skins of people living in various regions of the United States. Not all micrococci isolated in this investigation could be identified with the currently recognized species of Micrococcus, viz., M. luteus, M. varians, or M. roseus, and these micrococci therefore became the subject of further taxonomic study. As a result of this study, two new species are proposed: Micrococcus lylae and M. kristinae. The type strains of these species are ATCC 27566 and ATCC 27570, respectively. Numerous strains were isolated that were similar to M. sedentarius or M. nishinomiyaensis, species that were previously represented by only single strains. (ZoBell’s strain 541 [ ATCC 14392; CCM 3141 is designated herein as the type strain of M. sedentarius.) A few micrococci were left unclassified. A variety of morphological, physiological, biochemical, and genetic characters were examined for their use as taxonomic criteria, and key characters, many of which can be determined by simple laboratory procedures, were selected for species differentiation. The more sophisticated studies of aliphatic hydrocarbons and cell-wall peptidoglycans were also very useful in the taxonomy of the micrococci. The predominant micrococci found on human skin were M. luteus and M. varians. The medical literature has, for many years, The purpose of this investigation was to made reference to a group of aerobic, sapro- classify species of micrococci found on human phytic bacteria known as Sarcina that have skin by using the most current taxonomic been commonly isolated from human skin ( 14, critieria. We also became involved with evaluat- 18, 28, 29, 33). Recent taxonomic studies have ing existing taxonomic criteria, exploring new indicated that most aerobic strains maintained characters, and estimating species variation in in various culture collections under the name of cutaneous populations. Sarcina belong to the species Micrococcus Some of the preliminary results of this study luteus (Schroeter 1872) Cohn 1872 or Micro- have been previously reported (W.E. Kloos and coccus varians Migula 1900 (19, 21, 22, 24, K. H. Schleifer, Abst. Annu. Meet. Amer. SOC. 40). In line with this, Marples et al. (30) Microbiol., 73rd, Miami Beach, p- 116, 1973). recently made reference to the species M. luteus in studies on the aerobic microflora of the human scalp. M. varians has not yet been MATERIALS AND METHODS reported in studies of human skin. However, it was not until 1973 (22) that a comprehensive Bacterial straips. Micrococci were isolated from the report on the taxonomic status of this species healthy skins of two groups of people. One group was was made available. Earlier reports were some- composed of 20 people living in Raleigh, N.C., who what confusing, and, with the lack of a clearly were sampled once each month for 6-13 months. The defined species status, cutaneous isolates may second group was composed of 115 people from 21 have been simply placed in Baird-Parker’s different regions of the United States who were Micrococcus subgroups together with other sampled once during the winter. These people were species (2). residents of the following areas: Seattle, Wash.; Fargo, N.D.; Orono, Me.; Durham, N.H.; Erie, Pa.; Cleveland, Paper no. 4198 of the Journal Series of the North Ohio; Somerville, N.J.; New Brunswick, N.J.; Tabor, Carolina State University Agricultural Experiment Iowa; Concordia, Kan.; Fort Collins, Colo.; Washing- Station, Raleigh, N.C. ton, D.C.; Richmond, Va.; Raleigh, N.C.; Pleasanton, 79 80 KLOOS, TORNABENE, AND SCHLEIFER INT. J. SYST. BACTERIOL. Calif.; La Jolla, Calif.; Mesa, Ariz.; Austin, Tex.; San DNA base composition. The mol% of guanine plus Antonio, Tex.; Birmingham, Ala.; and Bartow, Fla. cytosine (G+C) in DNA was estimated by the thermal Samples from people of the Raleigh longitudinal denaturation method of Marmur and Doty (27). study were taken from two separate sites on the Genetic compatability with M. luteus. Transforma- forehead and one site from one cheek, one anterior tion of the M. luteus strain ATCC 27141 auxotrophs, nare, each axilla, each upper and lower arm, and each purE (ISU) and trpC23, was tested with donor DNA upper and lower leg. Samples were taken from similar from each strain. The transformation procedures used sites on people of the second group, with the were previously described by Kloos and Rose (20). exception that the anterior nare and axillae were Colony morphology and pigment. Cells from each omitted. These sites only occasionally produced culture were streaked for isolation on one-half micrococci and then usually in small numbers. portions of P agar plates and incubated for 5 days. At Representative strains of M. lylae, M. sedentarius, this time, the diameters of five widely isolated and M. kristinae are listed in Tables 1, 2, and 3, colonies were measured. Colonial characteristics, in- respectively. Additional strains that were analyzed for cluding profile, edge, surface texture, and pigment, only certain of the characters listed in these tables were observed daily throughout the incubation period. included M. lylae strains RS 14, RS 23, CPE 21, Cell morphology. Gram-stained smears were pre- JMWA 3, CS 11, HG 22, EDP 14, RW 13, RW 14, CR pared from 36-h-old cultures and examined for cell 13, KHND 24, KHND 25, KHND 2, BB 25, BB 13, morphology, staining properties, size, and aggregation DA 22, KAH 14, KAH 24, KAH 25, PH 11, PH 14, SD patterns. Several strains of each species were also 1, EF 23, and TF 14; M. sedentarius strains CPE 15, examined at 4-h incubation intervals over a 36-h SMCA 21, PH 1, RG 27, DBM 274, DBM 349, SM 93, period to check possible changes in cell morphology. and SM 15; and M. kristinae strains JB 11, RS 15, Motility. Motility was checked by using standard JMWA 11, LM 21, SG 11, MH 12, TB 12,DP26, KE procedures recommended for the Difco motility test 20, AB 2, MW 1, SR 13, and RG 1. medium (1). Procedures for isolating micrococci. Samples were Acetylmethylcarbinol production. The appearance obtained by using the following swab technique. of acetylmethylcarbinol was tested by the procedure Sterile cotton swabs were first moistened with a sterile of Coblentz (7). A loopful of a culture was suspended detergent containing 0.1% Triton X-100 (Packard) in in 5 ml of MR-VP broth. The inoculated broth tubes 0.075 M phosphate buffer, pH 7.9 (45). One swab was were shaken vigorously in a 34 C water bath for 48 h rubbed vigorously over each site (approximately 8 and then examined. cm’) on the forehead, cheek, apex of the axilla, or Nitrate reduction. Nitrate reduction was tested by hairy portions of the arms and legs. The anterior nare the sulfanilic acid and a-naphthylamine method and was sampled by swabbing the lining of the mucous confirmed with zinc dust (9). A loopful of a culture membrane. The duration of rubbing varied from 5 to was suspended in 5 ml of nitrate broth (Difco). The 15 s depending on the expected aerobic bacterial inoculated broth tubes were shaken vigorously in a 34 density for each region. Immediately after sampling, C water bath for 48 h and then examined. each swab was used to inoculate the entire surface of a Oxidase. Oxidase activity was determined on 18- to standard isolation agar plate (100-mm diameter). 24-h-old cultures by a modification of the technique Inoculated plates were incubated at 34 C for 4 days of Kovacs (25) using N,Ndimethyl-p-phenyl- and then examined. If necessary, plates could be enediamine monohydrochloride. stored at 4 C for several weeks before the isolation of Salt tolerance. Growth at different NaCl concentra- strains. The above procedure was designed to produce tions of 0, 5, 7.5, and 10% in P agar was estimated by 100 to 700 colonies per plate for most samples. culture-streak development after incubation for 48 h. Isolation medium. The isolating medium (P agar) Streaks were made by lightly inoculating a lcm line (32) was nonselective and had the following composi- on the surface of an agar plate with a loopful of a tion: peptone (Difco), 10 g; yeast extract (Difco), 5 g; culture. Up to 16 streaks could be radially inoculated sodium chloride, 5 g; glucose, 1 g; agar (Difco), 15 g; on each plate. distilled water, 1,000 ml. P agar shipped to various Optimal growth temperature range. Growth on P collecting points was supplemented with the mold agar at different incubation temperatures between 15 inhibitor cy cloheximide (50 pg/ml). and 50 C was estimated by culture-streak development Culture conditions. P agar was used for the after incubation for 48 h. Streaks were prepared maintenance and propagation of all strains. Unless according to the procedure described above for salt otherwise noted, all cultures were maintained at 4 C tolerance determinations. and incubated at 34 C; inocula for tests were prepared Aerobic requirement. The aerobic requirement of from 24- to 48-h-old cultures. each strain was estimated by using the semisolid Catalase. A loopful of a culture was suspended in 2 thioglycolate medium described by Evans and Kloos ml of physiological saline.
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