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INTERNATIONALJOURNAL OF SYSTEMATIC
BACTERIOLOGY,
Apr. 1991, p. 284-289
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Copyright 0 1991, International Union of Microbiological Societies
Vol. 41, No. 2
Staphylococcus cohnii Subspecies: Staphylococcus cohnii subsp.
cohnii subsp. nov. and Staphylococcus cohnii subsp. urealyticum
subsp. nov.
WESLEY E. KLOOS” AND JANA F. WOLFSHOHL
Department of Genetics, North Carolina State University, Raleigh, North Carolina 27695
Two major subspecies of Staphylococcus cohnii, namely S . cohnii subsp. cohnii, from humans, and S . cohnii
subsp. urealyticum, from humans and other primates, are described on the basis of a study of 14 to 25 strains
and 18 to 33 strains, respectively. DNA-DNA hybridization studies conducted in our laboratory in 1983 (W. E.
Kloos and J. F. Wolfshohl, Curr. Microbiol. 8:115-121, 1983) demonstrated that strains representing the
different subspecies were significantly divergent. S . cohnii subsp. urealyticum can be distinguished from S .
cohnii subsp. cohnii on the basis of its greater colony size; pigmentation; positive urease, P-glucuronidase, and
P-galactosidase activities; delayed alkaline phosphatase activity; ability to produce acid aerobically from alactose; and fatty acid profile. The type strain of s. cohnii subsp. cohnii is ATCC 29974, the designated type
strain of S. cohnii Schleifer and Kloos 197513, 55. The type strain of S. cohnii subsp. urealyticum is ATCC
49330.
Early investigations of the systematics of Staphylococcus
cohnii have suggested that this species is composed of two
major subpopulations or subspecies on the basis of the
following characteristics: colony morphology (13, 15, 24);
configuration of lactate produced from glucose fermentation
(24); esterase and catalase zymograms (27, 28); amino acid
requirements (4); uracil requirements for anaerobic growth
(6); alkaline phosphatase, urease, P-glucuronidase, and P-galactosidase activities (19); gelatinase activity (23); and DNADNA hybridization (20). Furthermore, the host range of one
of the subspecies (designated subspecies 1) appeared to be
limited to humans, whereas the other subspecies (designated
subspecies 2) demonstrated a wider host range extending
from lower primates to humans (20). The original description
of S . cohnii by Schleifer and Kloos (24) was based on a total
of 42 strains isolated from humans, approximately 70% of
which would be included in S. cohnii subsp. 1 and the
remainder of which would be included in S . cohnii subsp. 2.
In this paper, we describe each of the S . cohnii subspecies
and designate their type strains. S. cohnii subsp. 1 is named
S. cohnii subsp. cohnii, and S. cohnii subsp. 2 is named S .
cohnii subsp. urealyticum.
MATERIALS AND METHODS
Bacterial strains. The strains selected for the description of
S . cohnii subspecies are listed in Table 1. All strains were
isolated from the skin of humans or nonhuman primates.
Characteristics. The following characteristics were determined in the present study by methods previously described:
colony morphology and pigmentation, anaerobic growth in
thioglycolate broth, catalase activity, acetylmethylcarbinol
(acetoin) production, nitrate reduction, coagulase activity,
hemolysis of bovine blood, carbohydrate reactions, and
susceptibility to various antibiotics (12, 14, 16, 17, 24).
Alkaline phosphatase, urease, P-galactosidase, P-glucosidase, and P-glucuronidase activity and arginine utilization
were determined with the API Staph-Ident system (Analytab
Products, Plainview, N.Y .) (19). Arginine arylamidase activ-
* Corresponding author.
ity and aerobic production of acid from N-acetylglucosamine
were determined with the ATB 32 Staph gallery (API System
S.A., La Balme-les-Grottes, France) (2). Pyrrolidonyl arylamidase activity and esculin hydrolysis were determined
with the ATB 32 Staph gallery and the Baxter-MicroScan
Pos Combo Type 5 panel (Baxter Healthcare Corp. [MicroScan Division], West Sacramento, Calif.) (8). Clumping
factor was detected by a conventional method and by using
Staphaurex (Wellcome Diagnostics, Dartford, England) (12).
Heat-stable nuclease activity was tested by using the thermonuclease agar (with toluidine blue) of Remel (Lenexa,
Kans .) by following the manufacturer’s instructions. The
oxidase test was performed by the method of Faller and
Schleifer (7). Ornithine decarboxylase activity was determined by using a modification of the test of Moeller (22) as
described by Kloos and Lambe (12) and by using the ATB 32
Staph gallery. The fatty acid profile was determined with the
Microbial Identification System (model H P 5890A; Microbial
ID Inc., Newark, Del.) (21).
RESULTS AND DISCUSSION
DNA-DNA hybridization studies. The genomic relationships of various S . cohnii strains were estimated on the basis
of relative DNA binding or reassociation under optimum
(55°C) and stringent (70°C) conditions and on the basis of the
thermal stability of DNA duplexes formed at the optimal
criterion in a previous study by Kloos and Wolfshohl (20).
Results are summarized in Table 2. As can be seen from the
data, each subspecies forms a separate DNA homology
group. Divergence of these homology groups was that appropriate for a separate subspecies status and insufficient for
species status despite a definite phenotypic distinction.
Fatty acid profile. The fatty acid analysis of S . cohnii
subsp. cohnii and S . cohnii subsp. urealyticum is shown in
Table 3. S . cohnii subsp. cohnii has a higher percentage of
anteiso-C,,,, and anteiso-C,,,, fatty acids and a lower percentage of (&:,and iso-C1s,o fatty acids compared with S.
cohnii subsp. ureafyticum. S . cohnii does not produce detectable quantities of iso-C,,,, fatty acids.
Description of Staphylococcus cohnii subsp. cohnii subsp.
nov. Staphylococcus cohnii subsp. cohnii (c0h’ni.i. M.L.
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STAPHYLOCOCCUS COHNII SUBSPECIES
285
TABLE 1. List of S . cohnii strains and their sources
Subspecies and strains
Source (host)
Reference(s)
S . cohnii subsp. cohnii
ATCC 29974= (DSM 20260)
ATCC 29972 (DSM 20262)
ATCC 29973 (DSM 20261)
DM 224
DM 272
RM 429
KH 201
RM 10
PM 244
LK 478
DBM 247
J L 321
JRM 24
BB3
SH161A
1368-4
1415-5
S033B
JLJ 8549
DLB 8534
MAW 8142
MAW 8452
MK 7-9
CB 7A-6
SM 60
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
6, 13, 20, 24, 27, 28
6, 20, 24
6, 20, 24
6, 13, 24
6, 24, 27, 28
6, 24
6, 20, 24, 27, 28
6, 20, 24, 27, 28
6, 20, 24, 27, 28
6, 20, 24, 27, 28
6, 24
6, 24
6, 24, 28
6, 20, 24, 27, 28
20
20
20
S . cohnii subsp. urealyticurn
ATCC 49330 (CK27)
ATCC 49328 (DBM 388)
ATCC 49329 (JL143)
ATCC 49331 (LK8172)
MK247
DM 154
CM 89
MAW 8453
MY 8456
DLB 8535
PAY9E6
PAY 10F4
PAY 1253
GOB18C8
POY8C1
MCY2A6
MCY4L7
CPB 10C4
CPB9C5
CCB13D2
ECB3B3
SS512
SS521
SS522
LANZP6C 1
LANZP6D2
LED 3104
LED 212
LED 182
MID 571
GAD 475
TUD 9C2
TUD 1C3
Human
Human
Human
Human
Human
Human
Human
Human
Human
Human
Chimpanzee
Chimpanzee
Chimpanzee
Gorilla
Orangutan
Rhesus monkey
Rhesus monkey
African green monkey
African green monkey
Cherry head mangabey
Patas monkey
Squirrel monkey
Squirrel monkey
Squirrel monkey
Brown woolly monkey
Brown woolly monkey
Yellow-whiskered lemur
Ring-tailed lemur
Ruffed lemur
Lesser mouse lemur
Grand galago
Common tree shrewa
Common tree shrewa
6, 20, 24, 26-28
6, 20, 24
6, 20, 24
~~~~
a
6, 13, 20, 24
6, 20, 24
6, 24, 27, 28
10
20
20
20
20
20
20
20
20
20
20
20
20
20
20
20
20
20
20
20
20
20
20
20
~
Questionable classification as a primate but may represent important evolutionary development toward this order (3).
gen. noun of Cohn, named for Ferdinand Cohn, a German
botanist and bacteriologist). The following description of S .
cohnii subsp. cohnii is based on testing of 14 to 25 strains.
Cells are gram-positive cocci, 0.5 to 1.2 pm in diameter,
nonmotile, and nonsporeforming; they occur predominantly
singly or in pairs. Colonies on P agar (17) are convex, entire,
circular, smooth, usually glistening or glossy, opaque, and
4.0 to 6.5 mm in diameter. Colonies are unpigmented or
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INT. J.
KLOOS AND WOLFSHOHL
286
SYST.
BACTERIOL.
TABLE 2. DNA relationships of S . cohnii subspecies"
AT,,,, of heterologous duplexes with
labeled DNA from:
% Relative binding of labeled DNA from:
Source of unlabeled DNAb
(no. of strains tested)
S . cohnii subsp.
urealvticum
S . cohnii subsp. cohnii
S . cohnii subsp. cohnii (11)
S. cohnii subsp. urealyticum (28)
s. xylosus (1)
S. saprophyticus (1)
S. aureus (1)
S . auricularis (1)
S. epidermidis species group (8)
Other Staphylococcus species (5)
55°C
70°C
55°C
70°C
93 2 3
78 2 4
40
44
31
32
26 -+ 2
20 -+ 3
94 -+ 3
65 k 5
19
19
14
9
9-+1
8 2 1
82 2 3
94 -c 4
49
44
31
34
27 -+ 3
20 k 1
68 k 3
92 ? 4
15
12
11
9
8+1
7 + 1
S . cohnii subsp.
cohnii
S. cohnii subsp.
urealyticum
0.5 0.1
6.7 -+ 0.2
17.4
*
5.7 + 0.4
0.4 2 0.1
15.2
19.4
18.0
'' According to Kloos and Wolfshohl (20).
Individual strains are listed in Table 2 of reference 20. Species of the S. epidermidis species group included S. epidermidis (relative binding and TmC,,data),
S. capitis, S. hominis, S . haemolytirus, and S . warneri. Other Staphylococcus species tested included S. simulans, S. intermedius, S . hyicus, S . sciuri, and S.
lentus.
occasionally have a slightly yellowish tint. Facultatively
anaerobic. Catalase produced. Oxidase not produced. Coagulase, clumping factor, heat-stable nuclease, pyrrolidonyl
arylamidase, ornithine decarboxylase, urease, P-glucosidase, P-glucuronidase, f3-galactosidase, arginine dihydrolase, and arginine arylamidase negative. No esculin hydrolysis. Acid is not produced aerobically from D-turanose,
D-xylose, D-cellobiose, L-arabinose, sucrose, L-rhamnose,
D-ribose, P-melibiose, or a-lactose. Acid is produced from
D-trehalose, p-D-fructose, D-glucose, and glycerol. No acid
is produced anaerobically from D-mannitol. The variable
characteristics of S. cohnii subsp. cohnii are listed in Table
4.
Antibiotic susceptibilities. Resistant to novobiocin (MIC,
3.1 to 12.5 pg/ml) and slightly resistant to lincomycin (MIC,
21.6 kg/ml), oxacillin (MIC, 0.5 to 4 pg/ml), and penicillin G
(MIC, 0.1 to 0.8 pg/ml). Forty-four percent of strains are
resistant to erythromycin, 8% are resistant to tetracycline,
and 4% are resistant to chloramphenicol. All strains tested
are susceptible to vancomycin, gentamicin, and kanamycin.
By disk diffusion methods, borderline resistance or resistance is noted for oxacillin and penicillin G.
Cell wall peptidoglycan and teichoic acid. The cell wall
peptidoglycan type is ~-Lys-Gly,-, (24). The cell wall teichoic acid type is poly(glycerolphosphate), with glucose and
N-acetylglucosamine as the main substituents (5, 24).
Additional characteristics. Predominantly L-lactic acid
(mean = 96%) and only a very small percentage of D-lactic
acid are produced following anaerobic growth in a yeast
extract-glucose broth (24). Supplementation of a basal casein
hydrolysate medium with uracil does not promote growth
under anaerobic conditions (6). Most strains (78%) require
both L-arginine and L-proline for growth on a defined medium (4). Esterase polymorphism and polytypism are characteristic for this subspecies (25). The type strain of S. cohnii
subsp. cohnii is ATCC 29974 (DSM 20260, originally designated GH137), the designated type strain of S. cohnii Schleifer and Kloos 1975b, 55 (24).
Description of the type strain. The type strain has all the
uniform characteristics of the subspecies. In addition, it has
TABLE 3. Fatty acid profile of S. cohnii subspecies and related Staphylococcus species
Avg % of total fatty acid content for:
Fatty acid type
Iso-c13:o
Iso-c,,,,
Cl,:,
Iso-c,,,,
Anteiso-C,,,,
Iso-Cl6,,
c16:0
Iso-C1,,,
Anteiso-C,,,,
Iso-c,,,,
Cl,:,
Iso-c,,,,
Anteiso-C,,,,
I so-c,,:,
c,,:,
Cm:1
a
S . cohnii subsp. cohnii
(8 strains tested)
S . cohnii subsp. urealyticum
(6 strains tested)
S. suprophyticus
(8 strains tested)
s. xylosus
(1 strain tested)"
0
4.3
0.7
12.4
42.3
5.3
3.4
3.9
7.6
1.1
7.6
1.2
0.4
0
9.8
0
0.5
4.8
4.3
22.4
30.0
3.2
5.6
4.8
3.3
0.5
8.1
1.5
0.1
tr
10.9
0
0
1.1
1.2
16.3
44.1
1.9
3.2
5.7
6.0
0.1
6.5
2.4
0.2
0
11.3
0
1.0
1.9
0.8
19.2
37.0
1.3
3 .O
7.0
3.7
0
6.9
3.9
0.8
0
11.4
2.0
Data from Schleifer and Kroppenstedt for the type strain (25).
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VOL. 41. 1991
STAPHYLOCOCCUS COHNII SUBSPECIES
TABLE 4. Variable characteristics of 25 S. cohnii
subsp. cohnii strains
Characteristic
287
TABLE 5. Variable characteristics of S . cohnii subsp.
urealyticum strains
% of
strains
positive"
Colony size 2 6 mm ....................................................
24
(12)
Colony pigment.. ........................................................
Hemolysis................................................................ .24 (28)
Alkaline phosphatase activity .......................................
(4)
Acetoin production ....................................................-48 (36)
Nitrate reduction.. ......................................................
(4)
Acid produced aerobically from:
D-Mannitol ............................................................ .24 (32)"
D-Mannose............................................................
.32 (20)
Maltose ................................................................ .24 (52)
Xylitol. ..................................................................
(24)
N-Acetylglucosamine ............................................... (4)
a The numbers in parentheses are the percentages of strains showing a weak
positive reaction.
the following properties (24). Cells are gram-positive cocci,
1.0 to 1.2 pm in diameter, occurring predominantly in pairs
and singly, occasionally in tetrads. Agar colonies are circular, entire, about 6.0 mm in diameter, convex to slightly
peaked with a flat edge, smooth with a glossy surface, white,
and opaque. Weak hemolysins are detected. Alkaline phosphatase negative. Acetylmethylcarbinol (acetoin) produced.
Nitrates are not reduced to nitrites. Weak acid produced
aerobically from maltose and D-mannitol. No acid produced
from D-mannose, xylitol, or N-acetylglucosamine. Resistant
to erythromycin (MIC, >150 pg/ml) and susceptible to
tetracycline. Guanine-plus-cytosine content of the DNA is
37.1 mol%.
Description of Staphylococcus cohnii subsp. urealyticum
subsp. nov. Staphylococcus cohnii subsp. urealyticum (u.re.a.ly'ti.cum. M.L. fem. n. urea urea; Gr. adj. lyticos dissolving; M.L. neut. adj. urealyticum urea dissolving). The following description of S. cohnii subsp. urealyticum is based
on testing of 18 to 33 strains.
Cells are gram-positive cocci, 0.6 to 1.2 pm in diameter,
nonmotile and nonsporeforming, occurring predominantly
singly or in pairs. Colonies on P agar are raised to slightly
convex, entire, circular, smooth, usually glistening or
glossy, translucent, and 5.5 to 8.0 mm in diameter. Colonies
have concentric ring patterns. Strains isolated from humans
are usually unpigmented, and colonies have gray and graywhite rings. Strains isolated from nonhuman primates are
usually pigmented , producing brilliantly colored colonies
with alternating yellow-orange, gray, gray-white, orange,
and gray rings or bands. Some strains from nonhuman
primates produce colonies with a yellow-green hue and only
a subtle ring pattern. On 1%maltose (purple agar base) agar,
colonies produce a distinct yellow ring pattern. Facultatively
anaerobic. Catalase produced. Oxidase not produced. Coagulase, clumping factor, heat-stable nuclease, ornithine decarboxylase, and arginine arylamidase negative. Urease,
P-glucuronidase, P-galactosidase, and alkaline phosphatase
positive. In many strains, alkaline phosphatase activity is
delayed. Acid is not produced aerobically from L-arabinose,
D-xylose, D-cellobiose, D-melezitose, raffinose, P-melibiose,
salicin, P-gentiobiose, D-ribose, or L-rhamnose. Acid is
produced from D-glucose, glycerol, D-trehalose, P-D-fructose, and D-mannose. No acid is produced anaerobically
from D-mannitol. The variable characteristics of S. cohnii
subsp. urealyticum are listed in Table 5.
Characteristic
Colony size 1 6 mm
Colony pigment
Hemolysis
Acetoin production
Nitrate reduction
Pyrrolidonyl arylamidase activity
p-Glucosidase
Arginine dihydrolase activity
Esculin hydrolysis
Acid produced aerobically from:
Sucrose
Maltose
a-Lactose
D-Mannitol
Xylitol
D-Turanose
N -Acetylglucosamine
No. of strains
positive/total
no. tested"
%positiveb
of strains
30133
21'133
(4133)
3/24 (6124)
(5133)
13/18 (3118)
(3118)
(5118)
(5118)
(1133)
24/33 (4133)
28/33 (2133)
30133
6120 (7120)
(2133)
14/18
(3)
73 (12)
85 (6)
91
30 (35)
(6)
78
a The numbers in parentheses are the numbers of strains showing a weak
positive reactionhotal number of strains tested.
The numbers in parentheses are the percentages of strains showing a weak
positive reaction.
Pigmented strains are from nonhuman primates.
Antibiotic susceptibilities. Resistances to novobiocin, oxacillin, and penicillin G are similar to those described above
for S. cohnii subsp. cohnii. Twenty-six percent of strains are
resistant to tetracycline, and 23% of strains are resistant to
erythromycin. All strains tested are susceptible to vancomycin, gentamicin , and kanamycin.
Cell wall peptidoglycan and teichoic acid. The cell wall
peptidoglycan type is L-LYs-GIY,,, and the cell wall teichoic
acid type is poly(glycerolphosphate), with glucose and
N-acetylglucosamine as the main substituents (24).
Additional characteristics. Both L- and D-lactic acid, in
nearly equal amounts, are produced following anaerobic
growth in a yeast extract-glucose broth (24). Supplementation of a basal casein hydrolysate medium with uracil promotes growth (change in optical density at 600 nm = 0.17 to
0.51) under anaerobic conditions (6). Only 8% of strains
require L-arginine and 25% of strains require L-proline for
growth on a defined medium (4). Proline auxotrophs revert
to proline independence at a high frequency and are then
able to grow on a medium containing (NH,),SO, as the sole
source of substrate nitrogen. The type strain of S . cohnii
subsp. urealyticum is ATCC 49330 (CK27).
Description of the type strain. The type strain has all the
uniform characteristics of the subspecies. In addition, it has
the following properties. Cells are gram-positive cocci, 1.0 to
1.2 pm in diameter, occurring predominantly in pairs and
singly. Agar colonies are circular, entire, 6.5 to 7 mm in
diameter, slightly convex, with a glossy surface, white with
a grayish concentric ring pattern, and opaque. Weak hemolysins are detected. Acetoin is produced. Nitrates are not
reduced to nitrites. Positive pyrrolidonyl arylamidase activity. P-Glucosidase and arginine dihydrolase negative. No
hydrolysis of esculin. Acid is produced aerobically from
maltose, a-lactose, D-mannitol, xylitol, and N-acetylglucosamine. No acid is produced from sucrose or D-turanose.
Susceptible to erythromycin and tetracycline. Guanine-pluscytosine content of the DNA is 37.0 mol% (26).
Distinguishing characteristics. S. cohnii subsp. urealyticum
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288
KLOOS AND WOLFSHOHL
INT.
TABLE 6. Characteristics useful for differentiating S. cohnii
subspecies from other members of the S. saprophyticus
species groupa
S . cohnii
S. cohnii
subsp.
subsp.
*'
"procohnii
urealyticum phyticus
Characteristic
Colony size 2 6 mm
Colony pigment
Nitrate reduction
Alkaline phosphatase
activity
Pyrrolidonyl arylamidase
activity
Urease activity
@-Glucosidaseactivity
p-Glucuronidase activity
9-Galactosidase activity
Acid produced aerobically
from:
D-Mannose
D-Turanose
D-xylose
a-Lactose
Sucrose
N-Acetylglucosamine
d
-
-
(d)
-
+
d
-
+
d
-
''
vlO-
+
d
d
d
(+)
-
d
-
d
+
+
+
+
+
+
+
+
-
+
d
d
-
+
+
+
+
d
+
+
+
+
-
d
d
d
a Data are from references 10-12 and 15. Symbols: +, 90% or more of
strains positive; -, less than 10% of strains positive; d, 11 to 89% of strains
positive. Symbols in parentheses indicated a delayed reaction.
can be distinguished from S. cohnii subsp. cohnii on the
basis of greater colony size; pigment or ring pattern; positive
urease, P-glucuronidase, and P-galactosidase activities; delayed alkaline phosphatase activity; DL-lactic acid isomers
produced anaerobically from glucose; ability to produce acid
aerobically from a-lactose; fatty acid profile; and DNA
relationship to S. cohnii subsp. cohnii. The major features
useful in distinguishing S. cohnii subspecies from each other
and from related members of the S. saprophyticus species
group are summarized in Table 6.
S. cohnii subsp. cohnii demonstrates significantly fewer
positive characteristics than S . cohnii subsp. urealyticum.
Other human host-adapted Staphylococcus subspecies, e.g.,
of S . capitis (lj, S . auricularis (9j, and S . warneri and S.
haemolyticus (18) also demonstrate fewer positive characteristics and have greater nutritional requirements compared
with their primate or nonhuman-primate-host-adapted counterparts. We can speculate that the human-host-adapted
subspecies are more advanced in their adaptation and,
therefore, have dispensed with numerous functions that are
no longer required for survival. They are, in effect, becoming
locked into their respective niches.
ACKNOWLEDGMENTS
We thank M. Sasser (Microbial ID Inc.) for identifying the cellular
fatty acids. We are also grateful to Barbara Leasure for typing the
manuscript.
This work was supported by Public Health Service grant 1ROI A1
21312 from the National Institute of Allergy and Infectious Diseases.
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