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INTERNATIONAL BULLETIN

OF
B A C T E RI 0 LOG1C A L NO M E N C L A T U R E
AND
TAXONOMY
Volume 11 October 15, 1961 No. 4

CLASSIFICATION O F THE KLEB SIELLA-AEROBAC TER


GROUP WITH SPECIAL R E F E R E N C E TO THE
COLD-TOLERANT MESOPHILIC AEROBACTER TYPES

Michae 1 G r i m e s

D a i r y and Food Microbiology Department


University College, Cork, I r e l a n d

SUMMARY: A C r o b a c t e r l i q u e f a c i e n s G r i m e s a n d
H e n n e r t y 1931 i s a l a t e r i l l e g i t i m a t e h o m o n y m
o f A,. l i q u e f a c i e n s B e i j e r i n c k 1 9 0 0 . .fl. l i p o -
l y t i c u s n o m . nov. i s p r o p o s e d i n i t s p l a c e . A
detailed description i s given. A.
lipolyticus
i s widely distributed in nature and is impor-
tant in dairy science. It usually fails to pro-
duce gas f r o m lactose a t 37"C, but produces
i t abundantly at 20-30°C. A.
aerogenes with
w h i c h i t m.ay b e c o n f u s e d , p r o d u c e s g a s f r o m
l a c t o s e a t 3 7 ° C . A. l i p o l y t i c u s d i f f e r s f r o m
-
A . h i b e r n i c u s by l i q u e f a c t i o n of g e l a t i n .

Since E s c h e r i c h (1885) published h i s p a p e r on "Intestinal


B a c t e r i a " and B e i j e r i n c k (1900) d e s c r i b e d a n d n a m e d A6ro-
b a c t e r a e r o g e n e s , the c l a s s i f i c a t i o n of the taxa of the f a m i l y
E n t e r o b a c t e r i a c e a e h a s been a subject f o r investigation, d i s -
c u s s i o n and review. The different viewpoints on the i n t e r -
r e l a t i o n s h i p s of the g e n e r a Klebsiella and A g r o b a c t e r a r e
d i s c u s s e d i n the 7th edition (1957) of B e r g e y ' s Manual of
De te r m i n a t i v e Bacteriology, the International Bulletin of
B a c t e r i o l o g i c a l Nomenclature and Taxonomy founded i n 1951
and in many p a p e r s published in the v a r i o u s j o u r n a l s dealing
with bacteriology, microbiology and public health.
The Ent e r o b a c t e r i a c e a e Sub c o m m i t t e e (0riginally The
Salmonella Subcommittee) and the J u d i c i a l C o m m i s s i o n and
t h e i r m e m b e r s collectively and individually have e x p r e s s e d
t h e i r viewpoints in a s e r i e s of p a p e r s i n the International
B u 1le tin.
( P a g e 111)

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Kauffmann and Edwards (1 952) emended the description


of Klebsiella to include nonmotile, nonliquefying, G r a m -
negative rods, fermenting lactose and mannitol, c i t r a t e
positive and u r e a negative, o r late and i r r e g u l a r l y poditive,
and n a m e d two species, K. pneumoniae a n d K . rhinosclero-
m a t i s . They stated:

"It i s r e a l i z e d that no provision i s made f o r the motile


f o r m s classified a s AErobacter. It i s felt that p r e s e n t
knowledge of these f o r m s i s insufficient to justify t h e i r
placement in a definite group."

Edwards and Fife (1955) studied 856 c u l t u r e s of Klebsiella


a n d A & r o b a c t e r and stated that no single biochemical t e s t o r
combination of t e s t s sufficed c l e a r l y to distinguish the genus
Klebsiella and A. a e r o g e n e s f r o m c u l t u r e s of 4, cloacae,
and that many a b e r r a n t and intermediate s t r a i n s o c c u r r e d .
It was suggested that the nonmotile f o r m s which do not
liquefy gelatin be placed in the genus Klebsiella, and that
Agrobacter be redefined a s a motile liquefying group with A.
cloacae a s the type. With r e g a r d to motility, Brooke (1953)
in his study of s t r a i n s of A. cloacae and Klebsiella (all i s o -
lated f r o m human s o u r c e s , most of them f r o m u r i n e ) noted
that while a l l the Klebsiellae w e r e nonmotile, a number of
A. cloacae s t r a i n s w e r e a l s o nonmotile.
Cowan (1954) reviewed t h e names of the coliform b a c t e r i a
and asked the Judicial Commission to consider whether ACro-
b a c t e r B e i j e r i n c k 1900 should be placed i n the list of nomina
g e n e r i c a rejicienda. The Commission should a l s o be asked
t o d e t e r m i n e whether a newly defined genus Aerobacter (not
ABrobacter Beijerinck) should be conserved with the type
A. cloacae Jordan, o r with a redefined (motile) s p e c i e s A.
aerogenes, o r whether the genus Cloaca Castellani and Chal-
m e r s 1919 should be c o n s e r v e d ?
The Editorial B o a r d (1954) published a p r e l i m i n a r y s t a t e -
ment on the status of the g e n e r i c n a m e s , Escherichia, Kleb-
-
siella, ABrobacter and Cloaca. The Enterobacteriaceae
Subcommittee (1954, 1958) r e p o r t e d on these genera. In the
1958 Report, the Subcommittee proposed to define Kleb siella
a s consisting of nonmotile, encapsulated b a c t e r i a that con-
f o r m to the definition of the family E n t e r o b a c t e r i a c e a e and
to define Cloaca (ACrobacter) a s consisting of motile b a c -
t e r i a that conform to t h e definition of the family Enterobac-

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t e r i a c e a e , and give typical biochemical reactions. The Sub-


committee pointed out that c u l t u r e s of Klebsiella which have
been typed w e r e derived largely f r o m r e s p i r a t o r y infections
and u r i n a r y infections in man and f r o m human f e c e s .
Winslow ",t a_l. (1919), Weldin (1927), Ruchhoft ",t a_l.
(1931), Ostermann e_t 2. (1941), Olsen (1942), and B o r m a n
-et - a l . (1944) a l l noted the difficulties experienced by w o r k e r s
in trying to classify the Klebsiella-Aerobacter group onbio-
chemical t e s t s , p a r t i c u l a r l y s u g a r fermentations. O s t e r -
mann z t aJ. state that they found no single t e s t o r group of
t e s t s that would distinguish many of their Klebsiella ( F r i e d -
l s n d e r ) c u l t u r e s f r o m those of the coli-aerogenes group and
s t a t e that i t s e e m s not unlikely that much of the confusion
still surrounding the Klebsiella ( F r i e d l s n d e r ) and coli-
'

aerogenes o r g a n i s m s i s due to f a i l u r e to recognize the full


significance of variation.
Edwards (1929) isolated s t r a i n s of AErobacter f r o m f e c e s ,
soil, water, and milk and noted that both the Aerobacter
s t r a i n s and the F r i e d l h d e r (Klebsiella) s t r a i n s w e r e r a t h e r
variable i n t h e i r fermentative c h a r a c t e r s ,
P a r r (1938) noted t h e difficulty of classifying the coli-
f o r m b a c t e r i a owing to the essentially intergrading n a t u r e
of the o r g a n i s m s in this group and defined i n t e r m e d i a t e s a s
coliform o r g a n i s m s which have one o r m o r e of t h e c h a r a c -
t e r i s t i c s of Escherichia &i and one o r m o r e of those a t t r i -
buted to Aerobacter a e r o g e n e s and notes "among the c o l i -
f o r m b a c t e r i a c h a r a c t e r s a r e f r o m time to t i m e lost o r those
in abeyance a r e regained." P a r r (1939) noted that t h e s e
intermediate f o r m s e i t h e r do not conform to the so-called
LMYiC pattern, o r lack power to f e r m e n t c e r t a i n c a r b o -
hydrates, o r produce only a c i d where the production of a c i d
and gas i s considered normal, o r display a combination of
fermentation c h a r a c t e r s the r e v e r s e of that which normally
o c c u r s . It i s to be noted that P a r r (1936) isolated s t r a i n s
of Agrobacter f r o m f e c e s which had been s t o r e d i n an i c e
box f o r a s long a s two months.
Stuart e t a l . (1938) noted that, with some of t h e i r 5, 200
c u l t u r e s i s o l a t e d f r o m human and bovine f e c e s , f r o m dust
of cowbarns, and f r o m milk, growth was m o r e luxuriant a t
room t e m p e r a t u r e than a t 37°C and that c u l t u r e s (grown i n
methyl r e d medium) that produced only acid when grown a t
37°C f o r 36 h o u r s p r o d u c e d acid a n d g a s whengrown a t r o o m
t e m p e r a t u r e f o r the s a m e period, and a l s o that . t h e methyl

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r e d reaction v a r i e d with t e m p e r a t u r e of incubation. These


i r r e g u l a r i t i e s in the methyl r e d reaction w e r e m o s t notice-
able i n the s t r a i n s which either failed to produce g a s f r o m
lactose a t 3 7 ° C o r produced gas a t r o o m t e m p e r a t u r e only.
Stuart zt a_l. (1940) proposed the t e r m "aberrant" coli-
f o r m s f o r c u l t u r e s not fermenting lactose, producing acid
only, o r requiring m o r e than 48 h o u r s f o r the production of
gas a t 37°C. These s t r a i n s were isolated f r o m water, soils
and c e r e a l s . Many of the so-called "aberrant" s t r a i n s
grew abundantly a t r o o m t e m p e r a t u r e but s p a r s e l y o r not
a t a l l when incubated a t 3 7 ° C (in other words they isolated
mesophilic s t r a i n s of A e r o b a c t e r ) .
The Enterobacteriaceae Subcommittee (1958) f i r s t gives
,the biochemical c h a r a c t e r i s t i c s of the Cloaca (Aerobacter)
group and then s t a t e s "Although these biochemical reactions
can be considered a s typical of the group, t h e r e a r e a b e r r a n t
cultures, not fermenting lactose, s u c r o s e , rhamnose, s o r -
bitol, raffinose, methyl r e d positive, Voges-Proskauer,
c i t r a t e , o r KCN negative. Anaerogenic s t r a i n s also exist."
My work on the coliform group a s a whole has convinced
m e that a s a t i s f a c t o r y classification of the KlebsieIla-AGro-
b a c t e r group cannot be based solely on sugar fermentations.
That this fact i s generally recognized i s shown by the many
qualifications found in the l i t e r a t u r e such a s "frequently do
not attack"; "may o r may not attack"; "many s t r a i n s f e r -
ment"; "usually do not f o r m acid and/or g a s . Using a pH
m e t e r one can state that fermentation h a s o c c u r r e d , but can-
not state that a coliform culture i s not capable of developing
the ability to f e r m e n t a given carbohydrate. In c a r r y i n g out
the methyl r e d and Voges-Proskauer reactions Fouad Et ~ 1 .
(1953) have shown the necessity f o r a chemically defined
glucose ammonium phosphate medium.
Some s t r a i n s of A6robacter do not produce gas i n lactose
broth a t 37°C but do so a t 1 5 - 3 0 ° C . Begue and Lichstein
(1958) have shown that i n Saccharomyces c e r e v i s e a e the r e -
quired synthesis of pantothenic acid i s accomplished a t 30 " C
but in s o m e m a n n e r i s prevented a t 3 7 " C , i . e . a n enzyme-
t e m p e r a t u r e s y s t e m i s postulated. Lichstein (-1960) notes
"it i s becoming increasingly apparent that antagonisms and
interactions among nutrients a s well a s the c h a r a c t e r of the
physical environment influence markedly the nutritional de-
mands of an organism" and "genetic expression is affected
by the environment and the p r e s e n c e of a p a r t i c u l a r gene

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does not n e c e s s a r i l y m e a n that the c o r r e s p o n d i n g c h a r a c t e r


will be e x p r e s s e d . "
The ability of non-lactose-fermenting o r g a n i s m s i s o l a t e d
f r o m f e c e s to f e r m e n t l a c t o s e a f t e r long cultivation i n l a c t o s e
media h a s been shown by a n u m b e r of w o r k e r s , p a r t i c u l a r l y
K r i e b e l (1934) who d r a w s the conclusion that t h e s e s t r a i n s
a r e closely r e l a t e d to t h e colon group, possibly a s v a r i a n t s ,
since they tend to d i s s o c i a t e 'into lactose-fermenting coli-
like o r g a n i s m s . Tregoning and P o e (1937) found that the
production of s u c r o s e - p o s i t i v e v a r i a n t s was r e a d i l y a c c o m -
plished i n s o m e s t r a i n s of E s c h e r i c h i a and Atirobacter. Di-
G i r o l a m o e,t a-l, (1958) have shown that s t r a i n s of g . &i
that did not u s e a r a b i n o s e a s the sole c a r b o n s o u r c e did so
i f seeded on a m i x t u r e of r h a m n o s e and a r a b o n i s e , a n d noted
t h a t the methytpentose i s a n i n d i c a t o r of the enzyme of a r a b -
i n o s e m e t a b o l i s m , which by itself h a s no inductive p r o p e r t y .
B r e e d (1957) in B e r g e y ' s Manual c o m m e n t s on the un-
s a t i s f a c t o r y position of the K l e b s i e l l a - A e r o b a c t e r group and
notes that no method h a s been found to differentiate the
m a j o r i t y of ,K. pneumoniae s t r a i n s f r o m u r i n a r y s t r a i n s
commonly c l a s s i f i e d a s fl. agrogenes. He concludes that
while awaiting a b e t t e r solution of the p r o b l e m i t was f e l t
advisable to continue to recognize_A. aErogenes (as a s p e c i e s
distinct f r o m 5. pneumoniae) and both g e n e r a AErdbacter
B e i j e r i n c k and Klebsiella. He pointed out that s p e c i e s of
A g r o b a c t e r that o c c u r i n d a i r y p r o d u c t s a r e frequently de-
r i v e d f r o m g r a i n and that they a r e found on p a n i c l e s of the
g r a s s family in open f i e l d s .
The E n t e r o b a c t e r i a c e a e Subcommittee (1958) r e c o m m e n d -
e d biochemical methods f o r differentiation of the g e n e r a of
the E n t e r o b a c t e r i a c e a e . Except f o r gelatin liquefaction a t
2 1 ° C , they suggested that t e s t s be c a r r i e d out a t 37°C f o r
2 d a y s . If negative, follow with f u r t h e r incubation a t 21 to
25°C f o r 5 d a y s . In o u r work on the cold-tolerant m e s o -
philic s t r a i n s of A e r o b a c t e r , the above m e t h o d s have been
followed since 1928 a t a n incubation t e m p e r a t u r e of 21 C, O

since t h e s e s t r a i n s grow p o o r l y o r not a t a l l a t 37°C. It i s


difficult to c o m p a r e o u r data with t h o s e of p r e v i o u s w o r k e r s
b e f o r e 1950, s i n c e o t h e r s usually worked with nonmotile
c u l t u r e s and c a r r i e d out t h e i r t e s t s a t 37°C. The methyl-
r e d t e s t p a r t i c u l a r l y i s influenced by the t e m p e r a t u r e of in-
cubation, s i n c e t e m p e r a t u r e influences the r a t e of production
of acid i n t h e m e d i u m .

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Schafler ",t +. (1959., 1960) obtained through "training"


on lactose media and by selection lactose-positive s t r a i n s of
Salmonella which also became cellobiose-positive. An in-
teresting finding was that the appearance of lactose-positive
v a r i a n t s f r o m cellobiose-positive v a r i a n t s of Salmonellae
was p a r t i c u l a r l y o r totally inhibited by succinate or gluta-
m a t e . Schema "_t 51. (1943) found increasing tolerance of
A. agrogenes to sodium pentachlorpentate and noted that i n
c e r t a i n c u l t u r e s g a s was no longer f o r m e d f r o m arabinose
o r rhamnose, and that i n such c u l t u r e s the methyl-red t e s t
became positive.
That t e m p e r a t u r e of chemicals can cause gene unstabil-
ization h a s been shown by Zamenhof and co-workers (1958,
1961). They used a typical s t r a i n of 5 . &i and a lactose
nonfermenting mutant of that s t r a i n . A s i m i l a r situation
may well apply to s t r a i n s of Klebsiella and AErobacter.
T h e r e i s a l s o the question of growth r e q u i r e m e n t s and I
suggest that mesophilic (plant) s t r a i n s of AErobacter i n -
gested i n the food of an animal (given t i m e ) would adapt
themselves to t h e i r habitat and that the ability to f e r m e n t
lactose o r other p r o p e r t i e s could be lost. Such a s t r a i n
l a t e r isolated f r o m the u r i n a r y t r a c t o r f r o m f e c e s might
well be identified a s Klebsiella o r a s a n intermediate s t r a i n .
Martinec e_t a_l. (1961) discussing the taxonomic status of
S e r r a t i a m a r c e s c e n s Bizio state that relatively g r e a t v a r i -
ability of s o m e s t r a i n s w e r e observed during the f e r m e n t a -
tion of carbohydrates and add "it i s interesting that the
m a j o r i t y of t h e s e anomalies was observed i n s t r a i n s isolated
f r o m different species of i n s e c t s . "
A s a d a i r y bacteriologist, I have been i n t e r e s t e d since
1925 i n s t r a i n s of Acrobacter that f e r m e n t e d lactose poorly
o r not a t a l l a t 3 7 ° C . T h e y w e r e f i r s t isolated f r o m c r e a m -
e r y water supplies contaminated by soil. Since in a c r e a m -
e r y water supply i t i s a s important to eliminate soil con-
tamination a s to detect f e c a l contamination, in routine exam-
ination f o r the coliform group lactose-broth tubes w e r e in-
oculated i n duplicate a t 2 1 ° C and a t 3 7 ° C . This procedure,
a l s o applied to milk and milk products, led to the isolation
f r o m w a t e r , milk, c r e a m , poor quality butter, g a s s y cheese,
a n d i c e c r e a m , of s t r a i n s of Agrobacter whose optimum
t e m p e r a t u r e r a n g e d f r o m 2 0 ° C to 3 0 " C , that grew well a t
1 5 ° C and grew slowly a t 4 ° C (1931).
G r i m e s (1934) concluded that while i t i s now usual to

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c a r r y out the t e s t f o r E s c h e r i c h i a and Agrobacter f r o m w a t e r


and d a i r y products a t 3 7 ° C the t e s t should a l s o be c a r r i e d
out a l s o a t . 21 "C, otherwise the AErobacter group, although
p r e s e n t , may not be identified. These cold-tolerant m e s o -
philic s t r a i n s of AErobacter have been isolated by many
w o r k e r s f r o m soil, g r a s s e s , e a r s and panicles of c e r e a l
c r o p s , milk, c r e a m , poor quality butter, gassy cheese, i c e
c r e a m , c r e a m e r y and f a r m water supplies and d a i r y f a r m
equipment, chilled m e a t and c r a b m e a t .
A c h a r a c t e r i s t i c of these s t r a i n s of ABrobacter i s t h e i r
poor growth o r lack of growth in lactose broth a t 3 7 ° C .
Thomas and co-workers (1958) s t a t e t h a t out of 1040 c u l t u r e s
isolated f r o m r a w milk and f a r m d a i r y equipment which f e r -
mented lactose with t h e formation of acid and g a s to 30°C,
4 7 3 (nearly 50700)failed to produce g a s f r o m lactose i n two
days a t 3 7 ° C .
Although t h i s paper is concerned mainly with mesophilic
s t r a i n s of Agrobacter I have a l s o worked on t h e s t r a i n s that
grow b e s t a t 37"CD likewise s t r a i n s of E s c h e r i c h i a and v a r -
ious intermediate s t r a i n s . I a m of the opinion t h a t while one
can s t a t e that a p a r t i c u l a r s t r a i n is capable of a p a r t i c u l a r
fermentation, i t cannot be said that i t is incapable of f e r -
menting that substance. Whether o r not fermentation o c c u r s
depends on the original environment, medium used, temp-
e r a t u r e of incubation and length of time of incubation.
The growth mediuim and the t e m p e r a t u r e of incubation
m a y a l s o influence motility. I find peptone broth the b e s t
medium f o r determining motility, the culture t o be incubated
f o r 2 4 h o u r s a t i t s optimum t e m p e r a t u r e . One does not get
a s good r e s u l t s with lactose broth, f o r the s t r a i n s of A6ro-
b a c t e r grow plumper and l a r g e r , and i n the motility t e s t
they a r e found to be sluggishly motile o r nonmotile.
I a m in a g r e e m e n t with Hormaeche and Edwards (1960)
that capsules and s l i m e formation a r e of no value i n differ-
entiation since the r e l a t e d s t r a i n s a r e not constant in these
properties. In o u r routine work (incubation t e m p e r a t u r e
2 1 " C ) , streaking o r plating on Levine media f r o m lactose
broth c u l t u r e s showing acid and gas a t 2 1 ° C i n 24 to 48
h o u r s the mucoid s t r a i n s a r e readily s e p a r a t e d f r o m the
nonmucoid s t r a i n s , but I have not found it possible defin-
itely to s e p a r a t e them by biochemical t e s t s . The mucoid
s t r a i n s will cause r o p i n e s s in milk and give s l i m i n e s s in
glucose, lactose, and s u c r o s e broth and-more o r l e s s s l i m i -

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n e s s i n galactose, raffinose, sorbitol, xylose and glucerol


broth. T h e r e i s no c o r r e l a t i o n between mucoid growth o r
nonmucoid growth and the liquefaction of gelatin.
In classifying Klebsiellae and A g r o b a c t e r e s one is b e -
tween Scylla and Charybdis, since on the one hand i t i s pos-
sible to simplify by r e s t r i c t i n g the number of t e s t s , e . g .
relying on IMViC and the fermentation of lactose and
glucose, o r on the other hand to complicate to the point of
absurdity by differentiating on numerous fermentation and
other t e s t s . T h e r e i s the f u r t h e r complication that the i n -
fluence of medium, growth t e m p e r a t u r e and length of time
of incubation h a s not always been fully recognized. Alford
(1960) and Schultze Et 51. (1960) support o u r contention of
the importance of incubation t e m p e r a t u r e when c a r r y i n g out
biochemical t e s t s . T a y l o r ' s question (1959) "Why C h r i s t e n
a Salmonella?" i s pertinent h e r e , and the same. question can
be asked a l s o regarding the Klebsiella-AErobacter group.
The cold-tolerant mesophilic s t r a i n s of AErobacter espe-
cially a r e to be r e g a r d e d a s an adaptable group capable of
changing to m e e t changes i n t h e i r environment (given t i m e )
whether i t b e biological o r biochemical.
In discussing the legitimacy of the generic name Kleb-
siella to include both Klebsiella and AErobacter, the r e p o r t
of the Coli-Aerogenes (1956) Subcommittee of' t h e Society
f o r Applied Bacteriology (1956) s t a t e s "since the generic
name Klebsiella h a s p r i o r i t y over Agrobacter, the aerogene s
o r g a n i s m not onlyfalls into the genus Klebsiella but, strictly,
a l s o l o s e s i t s specific name. However, if the Rules of the
Bacteriological Code (1948) a r e s t r i c t l y applied, the c o r -
r e c t n a m e s f o r many coli-aerogenes b a c t e r i a would be s o
unfamiliar a s to cause confusion and e r r o r , and i t will be
n e c e s s a r y to a s k for official opinions to conserve suitable
names against e a r l i e r . The views e x p e r s s e d by Cowan
(1954) concerning n a m e s f o r coliform o r g a n i s m s and his
paper "Nonconformism i n Nomenclature'' (1959) a r e a l s o
r e levant.
Hormaeche and Edwards (1960) have discussed the diffi-
culty of classifying the b a c t e r i a of the Klebsiella-Agrobacter
group, They proposed a new genus Enterobacter with the
type species Enterobacter cloacae based onBacillus cloacae
J o r d a n (1890) and requested that the t e r m Enterobacter
Hormaeche and Edwards be placed in the list of conserved
b a c t e r i a l generic names and that Enterobacter cloacae J o r -

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dan comb. nov. ( g . cloacae J o r d a n , 1890) be designated a s


i t s type s p e c i e s . This r e q u e s t of Hormaeche and Edwards
d e s e r v e s c a r e f u l consideration, but i t a c c e p t s i n g e n e r a l
only those s t r a i n s of AErobacter with an optimum t e m p e r a -
t u r e 37"C, and r e j e c t s the cold-tolerant me sophilic s t r a i n s
of Aerobacter of G r i m e s and Hennerty (1931). Ewing and
Edwards (1960) state "that a t p r e s e n t the A e r o b a c t e r group
i s divisible into t h r e e subgroups corresponding to the spe-
c i e s A. cloacae, 6 . a e r o g e n e s and A. liquefaciens G r i m e s
(1 931). ' I
Hormaeche and Edwards (1958) make a valuable contribu-
tion i n their observations on the genus A e r o b a c t e r with r e -
spect to the separation of A e r o b a c t e r f r o m Klebsiella on the
b a s i s of motility and the u r e a s e and ornithine decarboxylase
t e s t s . They note that nonmotile v a r i a n t s of otherwise typical
c u l t u r e s a r e known to o c c u r , likewise a b e r r a n t and i n t e r -
mediate s t r a i n s . They state that there a r e a t l e a s t two
well-defined species-&. aErogenes and A. cloacae-and l i s t
their biochemical c h a r a c t e r i s t i c s . I a m of the opinion that
s a n i t a r y and food bacteriologists would be i n a g r e e m e n t i n
d e s i r i n g that the g e n e r i c name AErobacter be retained even
though Klebsiella has precedence. Classification i s not i n -
tended to fit a concept of s t a t i c genera a n d s p e c i e s . With the
development of m o r e and b e t t e r taxonomic methods, p a r t i c -
u l a r ly serological methods, the i n t e r r e lation ships of the
s t r a i n s that c o m p r i s e the Klebsiella-Aerobacter group a r e
now somewhat b e t t e r r e a l i z e d . Can Klebsiella be differen-
tiated f r o m A e r o b a c t e r while acknowledging the adaptability
of the l a t t e r group t o a d j u s t i t s e l to i t s environment, r e s u l t -
ing i n a v a r i e t y of i n t e r m e d i a t e s t r a i n s , which may also b e
t e r m e d "variant" o r " a b e r r a n t " ?
The description of the genus Klebsiella, a s given by the
Enterobacteriaceae Subcommittee (1958) and i n B e r g e y ' s
Manual (1957), I would amend a s follows: Nonmotile s h o r t
rods, Gram-negative, encapsulated in the mucoid phase,
conforming to the definition of the family Enterobacteriaceae,
methyl-red negative, Voges-Proskauer positive, gelatin not
liquefied, c i t r a t e s utilized a s sole s o u r c e of carbon, n i t r i t e s
produced f r o m n i t r a t e s , sodium malonate positive, cap-
able of fermenting glucose, lactose, s u c r o s e , mannitol, s a l i -
cin, and growing inKCN medium. The type s p e c i e s i s Kleb-
siella pneumoniae. Encountered frequently in the r e s p i r a -
tory, intestinal and urogenital t r a c t s of m a n ' a n d recognized

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a s one of the c a u s e s of m a s t i t i s i n cattle (Barnes, 1953;


Buntain and Field, 1953; E s t e r b r o o k s and P l a s t r i d g e , 1956;
Guillot ",t 2. 1961; Smith a n d Henderson, 1934; White, 1957;
The type s p e c i e s r e p r e s e n t s the s t r a i n s of the group that
a r e adjusted to a human o r animal habitat, and may b e m o r e
o r l e s s pathogenic.
As to the value of biochemical t e s t s in distinguishing A_.
cloacae f r o m A. azrogenes, the Enterobacteriaceae Sub-
committee (1 958) give the biochemical c h a r a c t e r i s t i c s of
Cloaca (Azrobacter) and state "although these biochemical
c h a r a c t e r i s t i c s can be considered a s typical, t h e r e a r e
a b e r r a n t cultures not fermenting lactose, s u c r o s e , r h a m -
nose, sorbitol, raffinose, methyl-red positive, Voge s - P r o s -
k a u e r , c i t r a t e o r KCN negative, Two biochemical types
can be differentiated. Type A does not generally f e r m e n t
i n o s i t o l n o r glycerol, and when doing s o does not produce
gas in four d a y s ; i t i s arginine positive, lysine negative and
liquefies gelatin. Type B promptly f e r m e n t s with gas ino-
sitol and glycerol, i s arginine negative, lysine positive and
about hals the s t r a i n s do not liquefy gelatin."
B r e e d (1957) s t a t e s "usually motile" gelatin colonies-
"thin, c i r c u l a r , bluish, translucent" (no mention of lique-
faction). Gelatin stab--" slow liquefaction, liquefying power
s o m e t i m e s lost. "
I r e g a r d a nonmotile A. cloacae s t r a i n a s a v a r i a n t of
A. a z r o g e n e s Beijerinck, 1900, i . e . a Klebsiella s t r a i n ; a
motile A. cloacae that does not liquefy gelatin a s not p r o p e r l y
identified and the motile 4. cloacae s t r a i n that liquefies gela-
tin, m o r e o r l e s s slowly, a s a v a r i a n t .of A. lipolyticus nom.
nov. d e s c r i b e d below.
Aerobacter i s defined a s follows: motile, Gram-negative
rods, mucoid phase common in media containing lactose,
conforming to the definition of the family Ente robacteriaceae,
methyl-red negative, Voge s - P r o skauer positive, u r i c acid,
c i t r i c acid and c i t r a t e s utilized a s sole s o u r c e of carbon,
n i t r i t e s f o r m e d f r o m n i t r a t e s , fermenting with t h e produc-
tion of acid and gas-glucose, levulose, galactose, lactose,
s u c r o s e , maltose, cellobiose, mannitol, raffino e, sorbitol,
ino sitol, rhamno s e , a rabinos e, xylo s e, g lyc e r o 1, salicin,
aesculin, a-methyl glucoside; positive f o r arginine di-
hydrolase, lycine and ornithine decarboxylases; sodium
f o r m a t e and sodium malonate positive. Growth i n KCN
medium. Phenylalanine deaminase negative. Dulcitol,

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AND TAXONOMY

inulin, potato s t a r c h , d e s t r i n may o r may not be f e r m e n t e d .


Indole t e s t usually negative.
These biochemical reactions a r e typical f o r the s t r a i n s
that c o m p r i s e the cold-tolerant mesophilic s t r a i n s , optimum
t e m p e r a t u r e , 20°C t o 3 0 ° C ; good growth a t 1 5 ° C . growth
at 4 ° C ; poor o r no growth a t 37°C.
Soil and plant s t r a i n s , isolated f r o m soil, g r a s s e s , c e r -
e a l s , water, . m i l k and milk products, and cold-stored m e a t .
Cause of ropy milk. AErobacter lipolyticus nom. nov. lique-
f i e s gelatin, P e c t i n not liquefied.
A s t r a i n with the s a m e biochemical c h a r a c t e r i s t i c s , but
incapable of liquefying gelatin, h a s b e e n named AErobacter
hibe rnicum.
The name Aerobacter liquefaciens G r i m e s and Hennerty
1931 i s a l a t e r homonym of AErobacter liquefaciens B e i j e r -
inck 1900, hence illegitimate. The name A6robacter w o -
lyticus nom. nov. i s proposed to r e p l a c e A. liquefaciens
G r i m e s and Hennerty. A detailed description i s given h e r e -
with.

AErobacter lipolyticus nom. nov.

Synonym: AErobacter liquefaciens G r i m e s and Hennerty


~~

1931, not A. liquefaciens B eijerinck 1900,


Morphology: Rods, 0.75-1.0 x 1 . 0 - 2 y , motile, p o s s e s s i n g
~

p e r t r i c h o u s flagella, Gram-negative, aerobic, faculta-


tive, non spo r e -forming .
Nutrient gelatin: Two days at 21°C. Punctiform, e n t i r e
d i r t y g r e y i s h colonies, gelatin liquefied.
Nutrient gelatin stab: Two days a t 21°C. F i l i f o r m growth
with liquefaction. F i v e to seven days-above 10% lique-
faction, infundibuliform. Two to t h r e e weeks -around
40% liquefaction.
Tryptone d e x t r o s e a g a r : Two days-colonies, circular,
smooth, moi s t, g li s tening, g r eyi s h -whi t e , vi s cid ,
convex, opaque , r a i s e d , e n t i r e .
Tryptone dextrose a g a r slant: Two days-abundant greyish-
white growth, Smooth, moist, glistening, opaque, viscid.
Nutrient broth: Good growth i n 24 h o u r s , turbid.
Levine medium: One to two days- good, nonchromogenic
growth. Colonies o r streak-smooth, glistening, opaque,
vi s cid .

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Potato slope: Two to five days-good growth, smooth,


moist, glistening, opaque, viscid, muddy g r e y to brown-
ish g r e y colour.

Biochemical T e s t s a t 20-30°C

Methyl-red: Negative.
Voges-Proskauer test: Positive.
U r i c a c i d media: Two days-good growth. pH 4.4-5.0.
K o s e r ' s c i t r a t e medium: Two days-good growth.
Hydrogen sulfide: Lead a c e t a t e filter p a p e r strip-Negative.
Bismuth liquor technique. 1938. J. Bact. 35:183. Definite
blackening around the top of the medium and along the
line of the stab.
N i t r a t e s reduced to n i t r i t e s .
Indol: Usually negative (positive s t r a i n s found).
Catalase: Positive.
Diastatic action: Negative.
Milk: Acid coagulation, ropiness, pH 5 . 3 in two to t h r e e
d a y s , Acidity 0 . 5 to 0.6% lactic acid.
The following a r e fermented with production of acid and g a s ,
with pH dropping to 5.0 o r lower in two to four days:
Lactose, s u c r o s e , fructose, galactose, maltose,
rhamnose, arabino s e , c e llobiose, a e sculin .
pH dropping to l e s s than 5.5 but not lower than 5.1:
Mannitol, inositol, adonitol, xylose, raffinose,
a-methyl glucoside, salicin.
pH dropping to 6.6 but not lower than 5.6: Sorbitol,
glycerol, amygdalin.
Glucose: Drops to pH 5 . 5 i n two d a y s and i s around 7.0 i n
four days.
Dulcitol m a y o r m a y not be f e r m e n t e d ; when fermented,
pH v a r i e d f r o m 5 . 5 to 6.5.
Erythritol: Not fermented.
Mucoid phase common i n media containing glucose and
lactose.
Inulin: Usually fermented, pH 6 . 3 (average).
Dextrin: May o r may not be f e r m e n t e d ; when fermented,
pH 6.4 (average).
Starch: May o r may not be f e r m e n t e d ; when fermented,
pH 6.0 (average).
Sodium malonate: Positive, pH 8.4 (average). One
negative s t r a i n found.

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Sodium hippurate: May b e negative o r positive, pH 6. 2


(average).
Sodium f o r m a t e : P o s i t i v e , g a s production, pH 8 . 4 ( a v e r a g e ) .
KCN: P o s i t i v e .
A s p a r a g i n e : P o s i t i v e , pH 8 . 0 ( a v e r a g e ) .
Arginine dihydrolase : Usually positive.
Lysine d e c a r b o x y l a s e : P o s i t i v e .
Phenylalanine d e a m i n a s e : Negative.
Ornithine d e c a r b o x y l a s e : P o s i t i v e
. Growth in 7.570 sodium c h l o r i d e solution.

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