INTERNATIONAL JOURNAL O F
SYSTEMATIC
BACTERIOLOGY
October 1970
Vol. 20, No. 4
Copyright 1970, Iowa State University P r e s s
pp. 483-490
THE RELATIONSHIP O F C E L L WALL COMPOSITION TO THE
CURRENT CLASSIFICATION O F STAPHYLOCOCCI
AND MICROCOCCI
A. C. Baird- P a r k e r
Unilever R e s e a r c h Laboratory, Colworth House
Sharnbrook, Bedford, England
ABSTRACT.
S t r u c t u r e a n d c o m p o s i t i o n s t u d i e s of c e l l
w a l l s of s t a p h y l o c o c c i a n d m i c r o c o c c i s u p p o r t s t h e
c l a s s i f i c a t i o n of t h e s e o r g a n i s m s b a s e d on p h y s i o l o g i c a l and biochemical characters. Staphylococcus aureus
a n d S. e p i d e r m i d i s a r e c l e a r l y s e p a r a t e d a s a l s o a r e
M i c r o c o c c u s l u t e u s a n d -~
M. r o s e u s .
The purpose of this contribution i s t o d i s c u s s the available information
concerning the composition and s t r u c t u r e of c e l l walls of staphylococci
and m i c r o c o c c i in relation t o the c u r r e n t classification of t h e s e o r g a n i s m s .
The Genus Staphylococcus
M e m b e r s of the genus Staphylococcus a r e s e p a r a t e d f r o m m e m b e r s of
the closely r e l a t e d genus Micrococcus by t h e i r ability to grow anaerobically and to f e r m e n t glucose (Evans, Bradford and Niven 1955; B a i r d P a r k e r 1963; Subcommittee 1965). Two s p e c i e s a r e c u r r e n t l y recognized
i n t h i s genus; t h e s e a r e Staphylococcus a u r e u s and S. e p i d e r m i d i s (Subc o m m i t t e e 1969). Biochemical and phy-cal .
cKaracters separating
t h e s e two s p e c i e s a r e shown in Table 1.
Staphylococcal c e l l walls contain two m a i n components namely the
m u l t i - l a y e r e d peptidoglycan and its a s s o c i a t e d teichoic a c i d s . S m a l l
amounts of serologically distinct proteins and polysaccharides m a y a l s o
be present. The peptidoglycan c o n s i s t s of l i n e a r s t r a n d s of a glycan consisting of repeating units of p - 1, 4 linked N-acetyl-glucosamine and Na c e t y l - m u r a m i c acid r e s i d u e s t h a t a r e linked through N- a c e t y l - m u r a m y l L-alanine linkages to peptide subunits consisting of Na-( L-alanyl- Disoglutamyl) - L-lysyl-D-alanine. T h e s e peptide subunits a r e c r o s s - l i n k e d
by peptide bridges containing solely o r mainly glycine t o f o r m a t h r e e dimensional s t r u c t u r e that i s responsible forthe s t r u c t u r a l integrity of
t h e c e l l wall. Where detailed studies have been done, t h e s e b r i d g e s have
b e e n shown t o extend f r o m the N E - l y s i n e r e s i d u e of one peptide subunit to
t h e C - t e r m i n a l D-alanine of a neighboring peptide subunit. Although only
a relatively few s t r a i n s of staphylococci have been studied i n sufficient
d e t a i l to d e t e r m i n e t h e composition and s t r u c t u r e of t h e peptide bridges
we a r e reasonably c e r t a i n that in all staphylococcal c e l l walls t h e s e
b r i d g e s contain glycyl-glycine linkages a s virtually a l l s t r a i n s a r e lysed
by lysostaphin endopeptidase (Klesius and Schuhardt 19 68) ; th’is enzyme
a c t s specifically on t h e glycyl-glycine linkages in the peptide bridges
( T i p p e r and Strominger 1966).
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484
Table 1.
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Some differential c h a r a c t e r i s t i c s of Staphylococcus s p e c i e s .
aureus
Coagulas e s
t
Mannitol: a c i d aerobically
acid anaerobically
t
t
Endonucleases ( h e a t r e s i s t a n t )
t
a toxin
t
epidermidis
Biotin for growth
d
t
d = s o m e s t r a i n s positive.
S t r u c t u r e and composition of Staphylococcus a u r e u s c e l l walls
Cell walls of r e p r e s e n t a t i v e s of t h i s s p e c i e s have been shown t o cont a i n organic phosphorus, ribitol, glucosamine, m u r a m i c ’ acid and the
amino acids, lysine, a s p a r t i c acid, s e r i n e , glycine, glutamic a c i d and
alanine together with s m a l l amounts of threonine, proline, valine and
leucine (Grove and Rude 1967a). T h e s e compounds can be accounted f o r
in the 3 m a i n components of t h e wall which a r e the peptidoglycan, t h e
ribitol teichoic acids and t h e s p e c i e s specific precipitinogen P r o t e i n A.
Small amounts of other p r o t e i n s and polysaccharides a r e a l s o p r e s e n t .
T h e s e c o r r e s p o n d t o t h e type specific agglutinogens and precipitinogens
used in t h e s e r o l o g i c a l typing of t h i s s p e c i e s (Oeding 1965).
Peptidoglycan. This p o s s e s s e s the following f e a t u r e s : 1) Approxim a t e l y 50% of t h e N - a c e t y l - m u r a m i c r e s i d u e s of t h e glycan a r e substituted with a n a c e t y l - g r o u p on the 6-Oposition ( T i p p e r and S t r o m i n g e r
1966), 2 ) All the N - a c e t y l - m u r a m i c r e s i d u e s a r e substituted by t h e t e t r a peptide subunits (Ghuysen and Strominger 1963), 3) T h e peptide subunits
a r e bridged by a s p e c i e s specific pentaglycine bridge.
Teichoic a c i d s . T W Oserologically distinct ribitol-containing teichoic
a c i d s m a y be p r e s e n t ; t h e s e a r e l i n e a r p o l y m e r s containing e i t h e r 4-0-(3
o r 4 - 0 - a - N - acetyl-D-glycosaminyl-D-ribitol bridged by 1 , 5 phosphodie s t e r linkages. In 2. a u r e u s s t r a i n Copenhagen the phosphodiester link
of the teichoic a c i d h a s been shown t o link the teichoic a c i d t o t h e peptidoglycan (Ghuysen, Tipper and Strominger 1965). It a p p e a r s t o be u n c e r t a i n whether the teichoic a c i d i s linked to the N-acetyl-glycosamine o r
N - a c e t y l - m u r a m i c a c i d p a r t of t h e glycan (Ghuysen 1968). The p-linked
teichoic acid c o r r e s p o n d s t o P o l y s a c c h a r i d e A and t h e a-u and (3-linked
teichoic a c i d s usually o c c u r together i n c e l l walls of a single s t r a t n a l though s o m e s t r a i n s contain only one o r other of t h e t e i c h o i c a c i d s ; t h e
t3-linked teichoic acid o c c u r s m o s t commonly and i s found i n s t r a i n s i s o lated f r o m both human and a n i m a l s o u r c e s (Marandon and Oeding 1967).
P r o t e i n A . T h i s s p e c i e s specific agglutinogen i s loosely bound t o
the c e l l wall and i s probably attached to t h e peptidoglycan; it contains a l l
the amino a c i d s found in S. -a u r e u s c e l l walls (Grove and Rude 1967b).
S t r u c t u r e and composition of Staphylococcus e p i d e r m i d i s c e l l w a l l s
C e l l walls of t h i s s p e c i e s a r e s i m i l a r in composition t o t h o s e of S.
a u r e u s but contain glycerol in place of ribitol and m o s t a l s o c o n t a i n g l u c o s e in addition ( B a i r d - P a r k e r 1965). T w o m a i n components have been
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SYSTEMATIC
48 5
BACTERIOLOGY
recognized, t h e s e a r e t h e peptidoglycan and t h e teichoic a c i d s ; P r o t e i n A
i s absent f r o m this species.
Peptidoglycan. The s t r u c t u r e and composition of the peptidoglycan
h a s only been studied in detail in a few s t r a i n s ( T i p p e r 1968; P e t i t , S t r o m i n g e r and S611 1968; Schleifer, Reid and Kandler 1968). The glycan and
peptide subunits a p p e a r t o be similar in s t r u c t u r e and composition t o
t h o s e of S. a u r e u s . The peptide bridges a r e different, a s they contain
s e r i n e o r L-alanine in addition t o glycyl-glycine r e s i d u e s ; s e r i n e can,
however, be substituted for glycine in the bridge of S. a u r e u s by growth
i n the p r e s e n c e of s e r i n e ( T i p p e r and B e r m a n 1969): T h e s e a r e v a r i a b l e
i n composition with r e s p e c t t o t h e amount of glycine and a m i n o a c i d s
t h e y contain
and a l s o the position of the amino a c i d s in t h e peptide
chains; t h e a v e r a g e chain length is 5 amino acids. The position of t h e
bridge in t h e two s t r a i n s studied i s t h e s a m e a s that i n S. -a u r e u s peptidog ly can.
Teichoic acids. All teichoic a c i d s that have been i s o l a t e d so f a r f r o m
c e l l walls of t h i s s p e c i e s contain glycerol. Depending on t h e linkage and
carbohydrate attachment of t h e glycerol, four types of teichoic a c i d s
have been described. In t h e s e glycerol is e i t h e r a - o r P-linked t o gluc o s e o r a - l i n k e d t o glucosamine; T h e teichoic a c i d s containing g l y c e r o l
a-linked to glucose m a y contain one o r two glycosyl r e s i d u e s (Davison
and Baddiley 1964; Davison Et al. 1964; Oeding, Myklestad and Davison
1967; Archibald, Baddiley and Shaukat 1968). The teichoic a c i d s a r e
serologically distinct and m a y f o r m a m e a n s of serologically typing t h i s
s p e c i e s . The a-linked glycosyl-glycerol teichoic acid probably c o r r e sponds t o Carbohydrate B of Julianelle and Wieghard ( L o s n e g a r d and
Oeding 19 63).
The Genus Micrococcus
M e m b e r s of the genus Micrococcus a r e s e p a r a t e d f r o m staphylococci
by t h e i r inability t o grow anaerobically and to f e r m e n t glucose ( B a i r d P a r k e r 1963). They a r e able t o oxidize glucose with the production of
a c i d o r carbon dioxide and w a t e r . F i v e s p e c i e s a r e c u r r e n t l y recognized
i n t h i s genus. See Table 2 for physiological and biochemical c h a r a c t e r s
s e p a r a t i n g t h e s e five s p e c i e s . The position of M. saprophyticus in the
genus Micrococcus i s c o n t r o v e r s i a l and on the F o u n d s of s i m i l a r i t y in
DNA composition t o the staphylococci the author h a s suggested that it
should be classified as a subgenus of t h e genus Staphylococcus (Subcomm i t t e e 1971).
Unfortunately studies on the s t r u c t u r e of c e l l walls of m i c r o c o c c i have
l u t e u s and
been l a r g e l y concentrated on the pigmented s t r a i n s , i. e. ,
M. r o s e u s . However, we can a s s u m e that t h e s t r u c t u r e and composition
of t h e glycan i s undoubtedly t h e s a m e a s that found in staphylococci. With
r o s e u s all s t r a i n s of m i c r o c o c c i that have
the exception of s t r a i n s of M. been examined contain glycine in t h e i r c e l l walls (Salton and Pavlik 1960;
M. luteus t h e glycine h a s been shown t o be p r e s e n t
B a i r d - P a r k e r 1965); i n in the peptide subunit. A l s o with the exception of the few s t r a i n s of M.
saprophyticus that have been studied, all m i c r o c o c c i that have so f a r b e e n
t e s t e d a r e r e s i s t a n t to lysostaphin (Klesius and Schuhardt 1968). T h e r e f o r e it is likely that peptide bridges containing glycyl-glycine links a r e
--
g.
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48 6
T a b l e 2.
INTERNATIONAL
JOURNAL
Some d i f f e r e n t i a l c h a r a c t e r s of Micrococcus s p e c i e s
saprophyticus
l a c t i s luteus roseus
-
t
Halophilic
t
Pigment: yellow
red
t
S
NT
R
R
Glucose: a c i d
a c et oin
t
t
t
d
t
d
Xylose: a c i d
>
<
S/R
t
Novobiocin sensitivity
R = MIC
S = MIC
m orrhuae
2.0 pg/ml
l.Opg/ml
a b s e n t f r o m c e l l w a l l s of m i c r o c o c c i o t h e r than t h o s e of M. saprophytic u s and that t h e glycine i s substituted i n the peptide s u b d t . O t h e r c o m -
ponents of t h e peptide subunit a r e probably identical t o t h o s e found i n t h e
staphylococcal peptidoglycan n a m e l y L- alanine, D -alanine, D- g l u t a m i c
a c i d and L-lysine.
It should be noted that a n u m b e r of t h e o r g a n i s m s t h a t have been misc l a s s i f i e d in the genus M i c r o c o c c u s contain the diamino a c i d s , D. A. P.
o r ornithine, i n t h e i r c e l l w a l l s . None of t h e s e o r g a n i s m s a r e now cons i d e r e d t o be m e m b e r s of t h i s genus. T h e r e a s o n s f o r t h e i r exclusion
have been d i s c u s s e d p r e v i o u s l y ( B a i r d - P a r k e r 1965). T h e s e o r g a n i s m s
include "M. c i n n a b a r i u s " and I'M. rhodochrous" ( C u m m i n s and H a r r i s
1956), " M. halodenitrificansll ( T a k a h a s h i and Gibbons 1959), "M. v a r i a n s "
(NCTC 7285) (Salton and P a v l i k 1960), "M. r a d i o d u r a n s " ( W o r k 1 9 6 4 ) ,
"M. d e n i t r i f i c a n s " and Abd-El-Malek a n d Gibson's g r o u p 3b m i c r o c o c c i
( G i r d - P a r k e r 1965).
S t r u c t u r e and composition of c e l l walls
of M i c r o c o c c u s s a p r o p h y t i c u s
----
C e l l w a l l s of t h i s s p e c i e s contain glucose, r i b i t o l o r g l y c e r o l , glucosa m i n e , m u r a m i c acid, g a l a c t o s a m i n e ( s o m e s t r a i n s ) , alanine, g l u t a m i c
acid, glycine, lysine, a s p a r t i c a c i d and s e r i n e (Salton and P a v l i k 1960;
B a i r d - P a r k e r 1965).
Peptidoglycan. Detailed s t u d i e s of t h e peptidoglycan have not been
done; t h e likely p r e s e n c e of glycine in t h e peptide b r i d g e s h a s been d i s c u s s e d above. It m a y be r e l e v a n t i n considering t h e taxonomic position
of t h i s s p e c i e s that it i s highly r e s i s t a n t t o novobiocin w h e r e a s s t r a i n s of
staphylococci with t h e exception of c e r t a i n hospital s t r a i n s of S. a u r e u s ,
a r e highly s e n s i t i v e to t h i s antibiotic (Mitchell and B a i r d - ParkerJ e f f r i e s 1968). Novobiocin a f f e c t s c e l l wall s y n t h e s i s although its p r i m a r y action i s probably not a g a i n s t c e l l w a l l s (Wishnow e t al. 1965).
Teichoic a c i d s . Two t y p e s of teichoic a c i d have b e e n r e p o r t e d in t h e
s m a l l n u m b e r of s t r a i n s of t h i s s p e c i e s that have been studied. C e l l w a l l s
of t h e type s t r a i n of t h e s p e c i e s (NCTC 7292) contain r i b i t o l t h a t is p r o b ably p -linked t o glucosamine; t h i s t e i c h o i c a c i d is s e r o l o g i c a l l y i d e n t i c a l
t o the ?-linked r i b i t o l glucosamine teichoic a c i d of S. a u r e u s ( P o l y s a c c h a r i d e A) (Davison e t a l . 1964). It i s of i n t e r e s t that s t r a i n s of M.
s a p r o p h y t i c u s containing r i b i t o l ( t h e s e m a i n l y c o r r e s p o n d t o B a i r z P a r k e r ' s
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SYSTEMATIC
BACT ERIO LOGY
48 7
Micrococcus subgroup 3) a r e able t o c a u s e infections of u r i n a r y t r a c t
( R o b e r t s 1967). The other type of teichoic a c i d contains g l y c e r o l linked
t o glucose.
S t r u c t u r e and composition of Micrococcus l a c t i s c e l l walls
C e l l walls a r e s i m i l a r i n composition t o t h o s e of M. saprophvticus
but
- -~
s o m e s t r a i n s contain two additional s u g a r s , i. e . , mannose and g a l a c t o s e
( B a i r d - P a r k e r 1965).
Peptidoglycan. T h e s t r u c t u r e of the peptidoglycan i s not known but it
is probably similar t o t h a t of M. luteus. C e l l s of t h i s s p e c i e s like t h o s e
of M. saprophyticus a r e highly r e s i s t a n t to novobiocin.
Teichoic acid. This s p e c i e s contains a v a r i e t y of g l y c e r o l o r r i b i t o l
teichoic a c i d s that a r e linked t o glucose, glucosamine ot galactosamine
(Davison and Baddiley 1963; Baddiley e t al. 1968). In one s t r a i n studied,
the teichoic a c i d was e x t r e m e l y c o m p g x a n d contained glucose, glucosamine, and galactosamine. C e r t a i n s t r a i n s of Micrococcus l a c t i s contain
p o l y s a c c h a r i d e s containing n e i t h e r r i b i t o l n o r g l y c e r o l (Baddiley e-t al.
1968).
S t r u c t u r e and composition of c e l l walls of Micrococcus 1 u E s
-
T h e composition of c e l l walls of t h i s s p e c i e s a p p e a r s t o be s i m i l a r t o
t h o s e of s t r a i n s of M. saprophyticus and M. l a c t i s except t h a t teichoic
a c i d s would a l w a y s a p p e a r t o be a b s e n t ( D l v i x n d Baddiley 1963;
B a i r d - P a r k e r 1965). Many s t r a i n s of t h i s s p e c i e s a r e s e n s i t i v e t o l y s o zyme and novobiocin but s o m e s t r a i n s a r e r e s i s t a n t ( J e f f r i e s 1968).
Peptidoglycan. T h e peptodiglycan of "M. lysodeikticus, ' I which is a
typical m e m b e r of t h i s s p e c i e s , h a s been s t u d i e d i n c o n s i d e r a b l e detail;
s e e Ghuysen (1968). The r e c e n t studies by Campbell, Leyh-Bouille and
Ghuysen (1969) on f u r t h e r r e p r e s e n t a t i v e s of the s p e c i e s , n a m e l y s t r a i n s
labelled -S a r c i n a lutea. Micrococcus flavus
t r e_u s show t h a t t h e s e
-and -M._ _c i _
o r g a n i s m s have t h e s a m e peptidoglycan s t r u c t u r e a s M. lysodeikticus.
T h i s p r o v i d e s f u r t h e r evidence t o support
t h e c u r r e n t v i e w t h a t all t h e s e
-~
o r g a n i s m s a r e m e m b e r s of t h e s a m e s p e c i e s (M.
l u t e u s ) . The peptide
- subunits of the glycan p o s s e s s t h e s t r u c t u r e Na-(L-alanyl-y (a-D-glutamylglycine)) - L-lysyl-D-alanine. T h i s i s identical in s t r u c t u r e t o the peptide
subunits of staphylococci except t h a t t h e a carboxyl group of t h e glutamic
a c i d r e s i d u e i s substituted with glycine. F u r t h e r differences f r o m c e l l
walls of staphylococci is t h a t not a l l the N - a c e t y l - m u r a m i c r e s i d u e s a r e
peptide substituted and 0 - a c e t y l substitution of the m u r a m i c a c i d is uncommon; s e e Ghuysen (1968). T h e question of t h e type of bridge between
the peptide subunits h a s been c o n t r o v e r s i a l f o r a n u m b e r of y e a r s although
it now a p p e a r s t h a t t h i s c o n t r o v e r s y h a s been finally resolved. It would
a p p e a r t h a t the peptide subunits a r e p o l y m e r i s e d by b r i d g e s f o r m e d by
d i r e c t bonding between the peptide subunits. Two types of c r o s s - l i n k i n g
a r e involved.
( 1 ) NE-(D-alany1)-L-lysine linkages between the E amino
group of the lysine molecule of one peptide subunit to the C - t e r m i n a l Dalanine of a neighbouring peptide unit and ( 2 ) D-alanyl- L-alanine linkages
between the N - t e r m i n a l alanine of one peptide subunit t o the C - t e r m i n a l
alanine of a neighbouring unit; in the o r g a n i s m s studied by Campbell e t al.
(1969) t h e l a t t e r type of linkage predominated.
P o l y s a c c h a r i d e s . In "M. lysodeikticus" (M. luteus) the polysaccharide
c o n s i s t s of a polymer containing glucose and7-acetamido-2-deoxymannuronic acid ( P e r k i n s 1963). Other polysaccharides o c c u r in o t h e r
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organisms of this species; s e e Baddiley et al. (1968). According t o
Campbell
$. (1969) it is probable thatth; glycan s t r a n d s consist of
8-18 disaccharide units linked through one m u r a m i c acid phosphate to a
polysaccharide consisting of 10 glucose residues together with the f u r t h e r
carbohydrates making up the polysaccharide.
et
Structure
-
and composition of cell walls of Micrococcus r o s e u s
The outstanding feature of the composition of cell walls of t h e s e organisms i s that both glycine and teichoic acids a r e absent.
Peptidoglycan. The glycan and peptide subunits of this molecule a r e
identical to those found in staphylococci. It differs, however, f r o m peptidoglycan of staphylococci in that the peptide bridge contains only Lalanine o r L-alanine and L-threonine. The proposed s t r u c t u r e of this
bridge is NE (L-alanyl-L-alanyl- L-alanyl- L-threonine)- L-lysine; in a
threonine negative mutant, threonine is absent f r o m the bridge (Petit,
Munoz and Ghuysen 1966).
Polysaccharides. Cell walls of this organism contain glucose, galact o s e and mannose ( B a i r d - P a r k e r 1965). The s t r u c t u r e of the polysaccharide has not been determined.
Micrococcus m o r r h u a e . No information i s available concerning the
composition o r s t r u c t u r e of cell walls of this organism.
CONCLUSIONS
C u r r e n t information relating t o t h e s t r u c t u r e and composition of c e l l
walls of staphylococci and micrococci mainly supports the classification
of t h e s e organisms based on physiological and biochemical c h a r a c t e r s .
Staphylococci p o s s e s s c e l l walls which a r e distinct f r o m t h o s e of m i c r o cocci. The two species currently recognized within the genus Staphylococcus a r e c l e a r l y separated by differences in their cell wall composition.
F u r t h e r work is required t o determine the composition and s t r u c t u r e
M. lactis and M.
of c e l l walls of micrococci. We have evidence that saprophyticus have distinct .cell wall peptidoglycans and we know that the
teichoic acids present in t h e s e s t r a i n s a r e extremely complex indicating
that further division of t h e s e two species may be possible on serological
grounds, T h e peptidoglycans of the two best defined species of m i c r o cocci, i. e. M. r o s e u s and _M. luteus (Evans 1965), a r e quite distinct.
I hope that further studies will be done on cell walls of the type s t r a i n s
of M. saprophyticus, M. lactis and M. m o r r h u a e as such studies would
b e T*remely valuable in finding furtxer information concerning the taxonomic position and validity of t h e s e species.
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