INTERNATIONALJOURNAL OF SYSTEMATIC BACTERIOLOGY, Jan. 1991, p. 1-5 Vol. 41, No.

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0020-7713/91/010001-05$02.OO/O
Copyright 0 1991, International Union of Microbiological Societies

Emended Descriptions and Recognition of Streptococcus

constellatus, Streptococcus intermedius, and
Streptococcus anginosus as Distinct Species
ROBERT A. WHILEY’” AND DAVID BEIGHTON2
Department of Oral Microbiology’ and Hunterian Dental Research Unit,2 The London Hospital
Medical College, Turner Street, Whitechapel, London, E l 2AD, United Kingdom

Strains currently classified as Streptococcus anginosus include strains previously identified as Streptococcus
constellatus (Prevot 1924) Holdeman and Moore 1974, Streptococcus intermedius (Prevot 1925), and “Strepto-
coccus millen“’ (Guthof 1956) because these specific epithets were argued to be later synonyms of Streptococcus
unginosus (Andrewes and Horder 1906) Smith and Sherman 1938 by Coykendall et al. (Int. J. Syst. Bacteriol.
37:222-228, 1987). However, recent data from DNA-DNA hybridization experiments, whole-cell-derived
polypeptide patterns determined by sodium dodecyl sulfate-polyacrylamidegel electrophoresis, and data from
phenotypic testing have demonstrated that Streptococcus anginosus strains represent three readily identifiable
taxa to which the previously assigned type strains of Streptococcus constellutus (strain NCDO 2226 [= ATCC
278231, Streptococcus intermedim (strain NCDO 2227 [ = ATCC 273351, and Streptococcus anginosus (strain
NCTC 10713 [= ATCC 333971 have been shown to belong. Therefore, we propose recognition of Streptococcus
constellatus (emend.) (type strain NCDO 2226 [= ATCC 27823]), Streptococcus intermedius (emend.) (type
strain NCDO 2227 [= ATCC 27335]), and Streptococcus anginosus (emend.) (type strain NCTC 10713 [=
ATCC 333971) as distinct species and propose an emended description of each of these taxa.

The species Streptococcus anginosus (1) as currently
recommended by Coykendall et al. (5) includes streptococ-
cal strains that have been referred to previously as the
“minute-colony-forming streptococci of Lancefield groups F
and G” (2, 21), “Streptococcus MG” (24), “Streptococcus
milleri” (15), the “Streptococcus milleri group” (14, 16),
Streptococcus constellatus (17), Streptococcus intermedius
(17), “Streptococcus MG-intermedius” (9) and “Streptococ-
cus anginosus-constellatus” (9). These strains have been
isolated from mouths, nasopharynges, gastrointestinal
tracts, and vaginas and are of clinical significance because of
their association with pyogenic infections involving the
central nervous system, chest, or abdomen (14, 28).
The taxonomy and nomenclature of the streptococci cur-
rently classified as S . anginosus have long been a source of
disagreement and confusion. Colman and Williams (3)
grouped the strains previously called “Streptococcus MG”
(24), the minute-colony-forming streptococci of Lancefield
groups F and G (2, 21), and the hemolytic and nonhemolytic
streptococci possessing the type antigens of Lancefield
group F (26) into “ S . milleri” because these organisms
closely resemble the nonhemolytic streptococci isolated
from oral abscesses and originally given that name by Guthof
(15). However, Facklam also noted a high degree of similar-
ity among “Streptococcus MG” (24), S . intermedius (17),
and S . constellatus (17) and divided these nonhemolytic
streptococci into lactose-fermenting strains, which he called
“S. MG-intermedius”, and strains that do not ferment
lactose, which he named “S. anginosus-constellatus” (9).
Subsequently, Facklam suggested that similar beta-hemo-
lytic strains, irrespective of their Lancefield group reaction,
should be called S. anginosus, with the nonhemolytic strains’
divided into S. intermedius (lactose fermenting) and S.
constellatus (lactose nonfermenting) (10).
Several studies of these streptococci have produced con-
* Corresponding author.
1
flicting results, with some workers reporting a high degree of
overall phenotypic similarity (12, 20, 22, 23) and other
workers demonstrating heterogeneity on the basis of fermen-
tation patterns (27, 29), antigenic compositions (3, 21, 26,
34), long-chain fatty acid compositions (4, 6), the results of
multilocus enzyme electrophoresis (13), and DNA base
compositions (guanine-plus-cytosine contents) (7).
DNA-DNA hybridization studies have also yielded con-
flicting data; some workers have concluded that these strains
form a single DNA homology group representing a single
species (5, 8, 11, 31), while other workers have identified
several groups (18,19). However, it has been acknowledged
that the different conclusions reached in some of these
studies may have been caused by inherent variations in the
experimental hybridization stringencies used ( 5 , 19). In
addition, the preselection (in some cases) of strains on the
basis of hemolytic reaction and the ability to produce acid
from lactose (8, 19) has prevented both full comparisons
between studies and taxonomic conclusions regarding this
group of streptococci as a whole. As a result of a study
involving DNA-DNA hybridization and phenotypic tests,
Coykendall et al. (5) reclassified strains of S. constellatus, S.
intermedius and “ S . rnilleri” as a single species, for which
they proposed the name S. anginosus on the basis that the
former names were later synonyms of the latter. However,
these authors speculated that the type strain of S. interme-
dius (strain ATCC 27335) may represent a separate species
after they observed relatively low levels of DNA homology
in experiments involving this strain.
A recent genetic analysis of strains currently classified as
S . anginosus revealed three DNA homology groups with, in
most cases, 69% or more DNA relatedness shared by the
strains within a group. The three DNA homology groups
observed were designated groups 1, 2, and 3 and contained
the type strains of S. constellatus (strain NCDO 2226), S.
intermedius (strain NCDO 2227), and S. anginosus (strain
NCTC 10713),respectively (Table 1)(33). Two strains in the
S. anginosus homology group (urine isolate KR 455 and

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2 WHILEY AND BEIGHTON
TABLE 1. Summary of levels of DNA homology among strains
of S. constellatus, S . interrnedius, and S . anginosusa
Avg % of DNA homology as determined
by using 3H-labeled DNA from:
Unlabeled DNA
from:
S. constellatus S. intermedius S.anginosus
NCDO 2226T NCDO 2227T NCTC 10713T
S. constellatus 95 (89)" 65 (30) 48 (23)
(5 strainslb
S. intermedius 36 ( N T ) ~ 103 (103) 38 (NT)
(5 strainslb
S. anginosus 49 (26) 41 (16) 76 (61)
(12 strains)b
~~~~~~
Data summarized from reference 33.
Including the type strain.
Values are the averages of the DNA homology values obtained under
optimum (60°C) conditions; the values in parentheses are the average DNA
homology values obtained under stringent (75°C) conditions.
NT, Not tested.
throat isolate ATCC 9895 [Table 21) exhibited 62 and 54%
DNA homology, respectively, with the type strain of S .
anginosus at the optimum hybridization temperature and 61
and 51% DNA homology, respectively, at the stringent
temperature. Similar results were obtained by Knight and
Shlaes (19) with strain ATCC 9895. These strains warrant
further examination. The lack of reciprocity observed in the
levels of DNA homology between S . intermedius and S .
constellatus strains when hybridization was carried out
under optimum (relaxed) conditions was not observed when
hybridization was carried out under stringent conditions
(Table 1). This indicated that the relatively high levels of
binding between 'H-labeled DNA from S . intermedius
NCDO 2227T (T = type strain) and DNAs from strains of S .
constellatus (average level of DNA homology, 65%) were
likely to have been due to the presence of mismatched
hybrids allowed to form only under optimum conditions.
This was possibly due to the condition of the labeled DNA
although the DNA from strain NCDO 2227T was pure as
measured by spectrophotometry and agarose gel electropho-
resis.
In addition to DNA homology data, DNA-homology-
group-specific polypeptide patterns at molecular weights of
25.5 x lo' to 34.0 x lo' were revealed by sodium dodecyl
sulfate-polyacrylamide gel electrophoresis. (32).
In this paper we consider the phenotypic differentiation of
S . constellatus, S . intermedius, and S . anginosus (32, 33)
together with DNA-DNA hybridization data (18, 33) and
propose emended descriptions and reinstatement of these
taxa as three distinct species.
MATERIALS AND METHODS
Bacterial strains. The 157 strains which we studied are
listed in Table 2 together with their clinical and laboratory
sources. All strains were stored frozen on glass beads at
-70°C and as freeze-dried stored cultures. Routine subcul-
turing was performed on Columbia agar (GIBCO Ltd.,
Paisley, Scotland) containing 5% (vol/vol) defibrinated horse
blood with incubation at 37°C in a 20% H,-lO% co,-70% N,
atmosphere.
Biochemical tests and cluster analysis. All biochemical
testing was carried out as previously described (32), and
cluster analysis was performed by using the average-linkage-
between-groups method in the SPSS package of statistical
programs (25).
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INT. J. SYST.BACTERIOL.
RESULTS AND DISCUSSION
As described previously, cluster analysis of the pheno-
typic data demonstrated the presence of three distinct clus-
ters (phena) (32); each cluster contained strains from only
one DNA homology group. The distinguishing characteris-
tics of the strains in each cluster are shown in Table 3.
Therefore, we believe that S . constellatus, S . intermedius,
and S . anginosus each deserve separate species status. The
descriptions below are based on data previously published
(32, 33).
Emended description of Streptococcus constellatus. Strep to-
coccus constellatus (Prevot 1924) Holdeman and Moore
1974 (emend.). Small (diameter 0.5 to 1.0 Fm), gram-posi-
tive, nonsporeforming, nonmotile cocci in short chains.
Catalase negative. Colonies on blood agar are 0.5 to 2.0 mm
in diameter, white or translucent, convex, and entire; some
strains produce colonies that are 0.5 to 1.0 mm in diameter,
white, and matte. Growth is reduced under aerobic condi-
tions and is frequently enhanced by the addition of CO,.
Some strains require anaerobic conditions for growth. Ace-
toin is produced. Arginine and esculin are hydrolyzed, but
urea is not. Hippurate is not split. Alkaline phosphatase and
leucine arylamidase are produced by all strains. Most strains
produce a-glucosidase, very few produce P-galactosidase,
and P-glucosidase. p-D-fucosidase, a-galactosidase , P-gluc-
uronidase , P-N-acetylglucosaminidase, pyrrolidonylarylami-
dase, and sialidase are not produced. Acid is produced from
glucose and frequently is produced from salicin and
trehalose. Lactose fermentation and amygdalin fermentation
are variable characteristics of this species. A few strains
produce acid from cellobiose, mannitol, melibiose, and
raffinose. Arabinose, glycerol, inulin, and sorbitol are not
fermented. Few strains produce hydrogen peroxide. Most
strains produce hyaluronidase. Strains are frequently both
hemolytic (beta) and members of Lancefield group F or are
nonhemolytic (alpha or gamma) and serologically ungroup-
able. A few strains react with Lancefield group A and C
antisera. Habitats are oral cavities and upper respiratory
tracts. Strains are isolated from human purulent infections,
including appendicitis. The DNA base composition is 37 to
38 mol% guanine plus cytosine. The type strain is strain
NCDO 2226 (= ATCC 27823).
Emended description of Streptococcus intermedius. Strepto-
coccus intermedius Prevot 1925 (emend.). Small (diameter
0.5 to 1.0 Fm), gram-positive, nonsporeforming, nonmotile
cocci in short chains. Catalase negative. Colonies on blood
agar are 0.5 to 2.0 mm in diameter, white or translucent,
convex, and entire; some strains also produce colonies that
are 0.5 to 1.0 mm in diameter, white, and matte. Growth is
reduced under aerobic conditions and is frequently enhanced
by the addition of CO,. Some strains require anaerobic
conditions for growth. Acetoin is produced. Arginine and
esculin are hydrolyzed, but urea is not. Hippurate is not
split. Alkaline phosphatase , P-D-fucosidase, P-galactosi-
dase, a-glucosidase, P-N-acetylgalactosaminidase, P-N-
acetylglucosaminidase, leucine arylamidase, and sialidase
are produced. The presence of P-glucosidase is a variable
characteristic of this species. a-Galactosidase, P-glucuroni-
dase, and pyrrolidonylarylamidase are not produced. All
strains produce acid from glucose and trehalose, and virtu-
ally all strains produce acid from lactose. The majority of
strains produce acid from amygdalin, cellobiose, and salicin,
and a few produce acid from mannitol, melibiose, and
raffinose. Arabinose, glycerol, inulin, and sorbitol are not
fermented. Hydrogen peroxide is not produced. Virtually all
VOL. 41, 1991 EMENDED DESCRIPTIONS OF STREPTOCOCCI 3

TABLE 2. Strain details

StraidsY' Received from": Clinical source

S . anginosus
NCTC 10713T (= ATCC 12395T = DSM20563T) NCTC Throat
NCTC 10707, NCTC 11062, NCTC 11065 NCTC Dental root canal
NCTC 8037 NCTC Respiratory tract
NCTC 11064 NCTC Materia alba
NCTC 11169 NCTC Palatal abscess
ATCC 9895 ATCC Throat
AC 9612, E F 222, H 117, PC 4890 LHMC Dental plaque
48 UNS Appendix
NMH 3 NMH Pelvic pus
NMH 5 NMH Perinephric swab
NMH 10 NMH Perforated ulcer
NMH 11 NMH Peritoneal swab
PHLS 430, PHLS 542, PHLS 549 PHLS Appendix
PHLS 457, PHLS 467 PHLS Vagina
PHLS 458 PHLS Pneumonectomy
KR 455, KR 461, KR 481, KR 485 KR Urine
KR 533 KR Rectal abscess
KR 580 KR Wound drain
KR 611 KR Hip sinus
KR 687 KR Axillary abscess
KR 757 KR Bartholin cyst
R8414972 GC Sputum
R8711657 GC Leg ulcer
R881111 GC Vagina
W554 LH Wound
W896 LH Vagina
CDC 1007-77 CDC Wound
CDC 2236-81, CDC 2405-81 CDC Blood
SL 34lW PH Subphrenic abscess
SL 36 PH Vagina
AGP-37lW MK Subgingival plaque
CR 245/G, CR 2451W D Palatal abscess
G5.3 M Dental plaque
B53 LH Blood
S . constellatus
NCDO 222fiT (= ATCC 27823T = NCTC 11325T = DSM 20575T) NCDO Purulent pleurisy
NCTC 10708, NCTC 10709 NCTC Dental abscess
NCTC 10714, NCTC 11063 NCTC Throat
NCTC 5389 NCTC Unknown
AC 3187, AM 699, AM 4261, E F 52, EF 5427, LHMC Dental plaque
E F 5249/R, EF 8941, EF 8958, GN 7307/R LHMC Dental plaque
GN 7307/W, GN 8096, PC 67, T269, T338 LHMC Dental plaque
34 UNS Liver disease
47, 50, 55 UNS Appendix
NMH 1 NMH Brain abscess
NMH 4 NMH Blood
NMH 6, NMH 7 NMH Inguinal abscess
NMH 9 NMH Bartholin gland
NMH 12 NMH Submandibular abscess
PHLS 432 PHLS Appendix
R861195 GC Throat
R8713795, R8713802 GC Blood
DP 10 LHMC Dental abscess
W207 LH Leg wound
W277 LH Tooth socket
W414 LH Abdominal mass
W862 LH Submandibular abscess
1340, 1391 WW Subgingival plaque
1769 WW Dental abscess
F77 LH Tooth socket
ACK LHMC Urinary tract infection
AGP-371G, WKP-2A/G, VJPl MK Subgingival plaque
FW73 GC Nasal swab
W2128 LH Tracheostomy
S . intermedius
NCDO 2227T (= ATCC 33397T = DSM 20573T) NCDO Unknown
AC 800, AC 1811, AC 4629, AC 4720, LHMC Dental plaque
AC 4730/R, AC 473O/S, AC4817, AC 5165, LHMC Dental plaque
Continued on following page

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4 WHILEY AND BEIGHTON INT. J. SYST.BACTERIOL.

TABLE ;?-Continued
Strain(s)“ Received froma: Clinical source

AC 5803, AC 6425, AC 7849, AM 47, LHMC Dental plaque

AM 1524, AM 2702, AM 4902, AM 5950, LHMC Dental plaque
AM 8276, AM 9256, EF491, EF1444, H251, LHMC Dental plaque
GN 72, GN 472/R, GN 472/S, GN 556, LHMC Dental plaque
GN 4633, GN 6146, GN 8364, PC 574/W, LHMC Dental plaque
PC 574/G, PC 594, PC 941, PC 1483/W, LHMC Dental plaque
PC 1483/G, PC 2392, PC 5631, PC 7466 LHMC Dental plaque
27s, 32, 39, 40, 42, 43, 45, 46 UNS Liver abscess
35, 36, 38 UNS Brain abscess
NMH 2 NMH Brain abscess
NMH 8 NMH Wound
PHLS 423 PHLS Appendix
I38713972 GC Blood
R88/114 GC Wound drain
DP101, DP102 LHMC Dental abscess
F44R LH Arm abscess
F458s LH Abdominal mass
ws 100s LH Bite wound
CDC 415-87 CDC Brain abscess
a ATCC, American Type Culture Collection, Rockville, Md; DSM, Deutsche Sammlung von Mikroorganismen, Gottingen, Federal Republic of Germany;
NCDO, National Collection of Dairy Organisms strains with this prefix are now included in the National Collection of Food Bacteria [NCFB], Agricultural and
Food Research Council Institute of Food Research, Norwich, United Kingdom); NCTC. National Collection of Type Cultures, Central Public Health Laboratory,
Colindale, London, United Kingdom; CDC, R. Facklam, Centers for Disease Control, Atlanta, Ga.; D, D. B. Drucker, University of Manchester, Manchester,
United Kingdom; GC, G. Colman, Central Public Health Laboratory, Colindale, London, United Kingdom; KR, K. Ruoff, Massachusetts General Hospital,
Boston, Mass.; LH, E. Shaw, The London Hospital, Whitechapel, London, United Kingdom; LHMC, Department of Oral Microbiology, The London Hospital
Medical College, Whitechapel, London, United Kingdom; M, B. Mkjare, University of Lund, Malmo, Sweden; MK, M. Kilian, Royal Dental College, Aarhus,
Denmark; NMH, M. W. D. Wren, North Middlesex Hospital, London, United Kingdom; PH, P. Handley, School of Biological Sciences, University of
Manchester, Manchester, United Kingdom; PHLS, P. Poole, Public Health Laboratory, Chester City Hospital, Chester, United Kingdom; UNS, P. Unsworth,
Central Public Health Laboratory, Colindale, London, United Kingdom; WW, W. Wade, College of Medicine, University of Wales, Cardiff, United Kingdom.

strains produce hyaluronidase. The majority of strains are mol% guanine plus cytosine. The type strain is strain NCDO
nonhemolytic (alpha or gamma), and virtually all strains are 2227 (= ATCC 27335).
serologically ungroupable with Lancefield grouping sera. Emended description of Streptococcus anginosus. Strepto-
Habitats are oral cavities and upper respiratory tracts, and COCCUS anginosus (Andrewes and Harder 1906) Smith and
this species has been reported to occur in feces. Strains are Sherman 1938 (emend.). Small (diameter, 0.5 to 1.0 km),
isolated from human purulent infections, notably liver and gram-positive, nonsporeforming, nonmotile cocci in short
brain abscesses- The DNA base ComPosition is 37 to 38 chains. Catalase negative. Colonies on blood agar are 0.5 to
2.0 mm in diameter, white or translucent, convex, and
entire; some strains produce colonies that are 0.5 to 1.0 mm
TABLE 3. Differential phenotypic characteristics of in diameter, white, and matte. Growth is reduced under
S. anginosus,S. constellatus, and S. intermedius aerobic conditions and is frequently enhanced by the addi-
Characteristic S. anginosus S.c o n s t e ~ ~ a t u s S. intermedius tion of co,. Some strains require anaerobic conditions for
( n = 47) (n = 49) (n = 61) growth. Acetoin is produced. Arginine and esculin are
Production of
hydrolyzed, but urea is not. Hippurate is not split. Alkaline
P-D-Fucosidase 0 100 (100) phosphatase and leucine arylamidase are produced by all
P-N-Acetylglu- 0 (0) 100 (100) strains, and P-glucosidase is produced by virtually all
cosaminidase strains, a-Galactosidase and a-glucosidase are sometimes
P-N-Acetylgalac- 0 (0) 100 (100) produced. Strains do not produce P-D-fucosidase, P-galac-
tosaminidase tosidase, P-glucuronidase, P-N-acetylglucosaminidase, pyr-
Sialidase 0 (0) 100 (100) rolidonylaminidase, or sialidase. Acid is produced from
P-Galactosidase 0 (0) 100 (100) amygdalin and glucose and is frequently produced from
P-Glucosidase 96 (86) 47 (0)
a-Glucosidase 19 (0) 100 (100) cellobiose, lactose, salicin, and trehalose. The majority of
H yaluronidase 4 (0) 98 (100) strains within the “ S . mifleri group’’ that ferment mannitol,
HZOZ 34 (57)b 0 (0) melibiose, and raffinose belong to this species, although only
Acid produced a small percentage of the strains that we have tested ferment
from: these substrates. Arabinose, glycerol, inulin, and sorbitol
Am ygdalin 100 (100) 78 (50) are not fermented. Hydrogen peroxide is sometimes pro-
Lactose 98 (100) 97 (100) duced. Very few strains produce hyaluronidase. Most
Manni to1 17 (14) 3 (0)
Raffinose 32 (29)b strains give partial hemolysis (alpha) or no hemolysis (gam-
5 (0)
ma). The majority are either serologically ungroupable or
” The values are the percentages of strains that were positive, while the belong to Lancefield group F although strains belonging to
values in parentheses are the percentages of DNA homology group strains (33)
that were positive.
Lancefield groups A, C, and G are also present. Habitats
The reaction of the type strain differs from that of the majority of the include oral cavities, upper respiratory tracts and vaginas.
strains tested. Strains of this species are isolated from a variety of human

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VOL.41, 1991
purulent infections. The DNA base composition is 38 to 40
mol% guanine plus cytosine. The type strain is strain NCTC
10713 (= ATCC 33397).
ACKNOWLEDGMENT
This study was supported in part by grant GB 8704557 from the
Medical Research Council.
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