INTERNATIONAL JOURNAL of SYSTEMATIC BACTERIOLOGY
January 1971, p. 50-54.
Copyright 0 1971 International Journal of Microbiological Societies
Vol. 21, No. 1
Printed in U . S . A .
Studies on the Taxonomy of the Myxobacterdes
IV. M elit tangiu rn
HOWARD D. McCURDY
Department of Biology, Universityof Windsor, Windsor,Ontario
With the transfer of Podangium erectum, the type species of Podangium
Jahn, to the genus Stigmatella Berkeley and Curtis as an earlier, subjective
synonym of Stigmatella brunnea, it has become necessary to assign the
remaining species which were in the genus Podangium to another genus.
Included among these species is Podangium boletus (synonym:
Melittangium boletus), the type species of the genus Melittangium Jahn.
Because none of the other species is the type of a genus, the correct name
for the genus which includes the organisms under consideration is
Melittangium. In addition t o the type species, M. boletus, the genus
includes M. lechenicolum (Thaxter) comb. nov. and M. alboraceum
(Peterson) comb. nov.
The genus Podangium was erected by Jahn [P. gracilipes or P. lichenicolum; M74, M150,
(2) to contain myxobacters which were for- (ATCC 25945) M154, M155 (ATCC 25944) M164,
merly placed in the genus Chondromyces by M201 (ATCC 25946)l.
Herbarium specimens were as follows: (i) from the
Thaxter (13, 14) and which have fruiting bodies
Thaxter collection, Farlow Herbarium, Harvard Uniconsisting of a single sporangium borne on an versity : Melittangium lichenicolum (Chondromy ces
unbranched stalk. In it he placed Podangiurn
lichenicolus; acc. no. 4499, 4500, 4501,4502,5170),
erectum (the type species), P. gracilipes, Melittangium lichenicolum (Chondromyces gracilipes,
and P. 1ich en i co1u m. K rz e m ienie wsk a and acc. no. 45 14), and Melittangium boletus; (ii) from J .
Krzemieniewski ( 5 ) added, as the fourth E. Peterson, University of Missouri: Podangium cylinspecies, Podangium boletus, an organism which dricum (acc. no. 70) and Melittangium alboraceum
had been originally described by Jahn (2) as (Podangiumalboraceum; slide, acc. no. 72).
Melittangium boletus. Peterson (1 0 ) described
two additional species, Podangium alboraceum
RESULTS AND DISCUSSION
and Podangium cylindricum. More recently, a
There
is considerable difficulty in dissixth species, Podangium cellulosum, was recogtinguishing
between P. lichenicolum and P.
nized by Pronina (1 1).
McCurdy (8), concluding that P. erectum gracilipes. Thaxter (1 3, 14) had originally difthe type species of Podangium is a variant of ferentiated them chiefly on the basis of the
Stigmatella brunnea (synonym: Chondromyces short, squared stalks and irregular sporangia of
brunneus), changed the name of the latter t o P. lichenicolum compared t o the delicately
Stigmatella erecta. Podangium Jahn 1924 there- pointed sporangiophores and regularly rounded
fore is a later subjective synonym of Stigmatella sporangia of P. gracilipes. In other respects they
Berkeley and Curtis 1874. Thus, it is necessary seemed very similar. It is significant that P.
to establish a new genus for the other species gracilipes was observed on dung while P. lichenicolum was observed on lichen. In examining
previously placed in the genus Podangium.
Thaxter’s original specimens, the differences
observed between his two “species” appeared
MATERIALS AND METHODS
to be well within the range of variation exThe media employed and the procedures used were pected of a myxobacter growing on different
described in detail elsewhere (6).
Cultures and specimen material. The following were substrates. When his diagnostic criteria were
organisms examined in pure culture (strain designa- applied to our isolates, two (M154 and M155),
tions beginning with M are those of the University of both associated with lichen, corresponded t o P.
Windsor; ATCC indicates those from the American lichenicolum; the rest corresponded t o P. graType Culture Collection : Melittangium lichenicolum cilipes. In culture, however, no clear differences
50
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IV. MELITTANGIUM
VOL. 21, 1971
’
51
Peterson (10) himself commented on the
were found between them (Table 1). That only
one species (P. lichenicolum, the first de- close resemblance between P. cylindricum and
scribed) is involved is further supported by S. erecta (P. erecturn) (McCurdy, 1971). P.
observations such as those represented in Fig. 2. cylindricurn was considered t o differ from S .
The fruiting body shown, apparently a typical erecta on the basis of (i) the shape of its
representative of P. gracilipes, is in fact from sporangia, (ii) the presence of “oil droplets” in
Thaxter’s P. lichenicolum type specimen!
the sporangia, (iii) the presence of cells in the
Structures closely resembling the fruiting sporangiophore, and (iv) the slightly larger size
bodies of Archangium prirnigenium or Ar- of its microcysts. When Peterson’s type specichangium serpens (the published descriptions mens were compared t o Thaxter’s material and
do not permit a discrimination between the to our own specimen of S. erecta on bark, they
two) were frequently associated with P.licheni- were found to be remarkably similar. The
colum. Pure cultures obtained from the ar- cylindrical sporangia of Peterson’s organism fall
changium- and podangium-like fruiting bodies well within the range of variation in size and
proved t o be identical. Fruiting in pure culture shape of those of S. erecta. In fact, the
was rare in all cases but when it did occur (on sporangia of P. cylindricurn are not consistently
dung, Ca” - water agar) it was generally of the cylindrical but are frequently somewhat oval.
archangium type (Fig. 1). Only very rarely were Cells may or may not be present in the stalks of
podangium fruiting bodies obtained in culture S . erecta; they are not consistently present in
(Fig. 4). It is pertinent t o these observations those of P. cylindricurn. The “oil droplets”
that Thaxter mentioned that he had at first (probably derived from autolysis within the
regarded Chondromyces serpens (Archangiurn sporangium) are indeed observed in S. erecta as
serpens) as an abnormal form of P. licheni- they are in many myxobacters. Finally the
colum but was impressed by the constancy of microcyst dimensions of S . erecta (0.8 t o
the archangium morphology on continued culti- 1.5 pm by 1.5 to 3.5 pm) and P. cylindricurn
vation. This and similar observations reported (0.8 pm by 2.5 t o 3.5 pm) are not significantly
elsewhere (6, 7, 9) strongly suggest that mem- different. Because of these observations and the
bers of the genus Archangiurn may in many absence of any pure-culture data, the recogniinstances be degenerate forms of other myxo- tion of P. cylindricurn as a distinct species
would appedr unwarranted.
bacters.
An evaluation of P. alboraceum (10) is also
P. boletus (Fig. 9 and 10) was not encountered in spite of the observation of literally limited by the lack of pure-culture data. Furhundreds of myxobacters in our laboratory. thermore, the deliquescence of its fruiting
Consequently, our consideration of it is based bodies frustrated the conservation of even dry
on the study of a single specimen on dung from specimens. Its description, nevertheless, is reathe Thaxter collection and the available litera- sonably complete and accompanied by excelture (2, 5, 12). It appears to be a well defined lent photographs. Microscope slides form the
and easily identifiable species bearing some type material. The organism seems quite distinctive, but its relationship to other myxoresemblances t o Stigmatella.
TABLE 1. Cultural and biochemical characteristics of Melittangium lichenicolum
Strain
~~
M74
M150 (ATCC 25945)
M154
M155 (ATCC 25944)
M164
M201 (ATCC 25946)
~
~~
R
OR
OR
~~
R
0
0
OR
OR
R
R
R
R
+
+
-
-
-
+
+
+
-
-
-
-
+
+
+
+
+
+
+
+
+
+
- +
+ +
- +
+ +
a Abbreviations: 0 , orange; R, red; OR, orange-red.
b +, Antibiotic sensitive; -, antibiotic insensitive.
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+
+
+
+
+
+
+
+
+
+
+
+
- +
+ +
+ +
- +
+ +
- +
52
McCURDY
INT. J. SYST. BACTERIOL.
Fig. 1. Melittangium lichenicolum, archangium fruiting body on agar. X22. Fig. 2. M. lichenicolum, fruiting
body from Thaxter’s type material. X 150. Fig. 3 . M. lichenicolum, bark. X I O O . Fig. 4. M. lichenicolum, on agar
(contaminated). X 140. Fig. 5 . M. lichenicolum, microcysts. X30,OOO. Fig. 6. M. lichenicolum, rnicrocysts.
X 1,200. Fig. 7. M . lichenicolum, rnicrocysts. X 1,300. Fig. 8. M. lichenicolum, vegetative cells. X 1,300. Fig. 9. M.
boletus, fruiting bodies on dung. X 120. Fig. 10. M. boletus, microcysts. X 1,300.
bacters remains in doubt because of the statement by Peterson that the vegetative cells are
not tapered and have square ends.
The remaining organism proposed for inclusion in the genus Podangium, P. cellulosum
( 1 l), requires consideration if only in passing.
It was considered a podangium “in view of the
nature of the pseudoplasmodia,”-a criterion so
astoundingly inadequate in the absence of other
data as to be dismissed out of hand.
Of the three species, P. lichenicolum was the
first to be named and described, and there is
sufficient cytological and cultural evidence t o
assign it unambiguously t o the family Cystobacteraceae. It has the tapered vegetative cells
(Fig. 8 ) characteristic of the family, and elec-
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VOL. 21. 1971
IV. MELITTANGIUM
tron microscopy clearly demonstrates the presence of a slime capsule surrounding its myxospores (Fig. 5). It would be preferable if P.
Eichenicolum could be designated the type
species of the genus incorporating the species
considered here. However, because one of the
species, Podangium boletus (synonym: MeZittangium boletus), is the type species of Melittangium Jahn, Melittangium is the name which
must be used for this genus.
Genus Melittangium Jahn 1924.
Vegetative cells are tapered rods.
Sporangia borne singly on a stalk.
Microcysts rod-shaped, phasedense, or refract ile.
Vegetative colonies d o not etch or erode
agar media; Congo red is adsorbed.
Minimum nutritional requirements unknown
but cultivable on media containing enzymatically hydrolyzed protein.
Type species: Melittangium boletus Jahn
1924.
Melittangium boletus Jahn 1924.
[Objective synonym: Podangium boletus
Jahn (reference 5 ) l .
Vegetative rods are slightly tapered with
rounded ends (3), 0.7 pm t o 4.5 by 10.5 pm
(1 2).
Sporangia (Fig. 9 ) are spherical or flattened
and resemble a mushroom pileus, 45 p m t o 50
by 50 to 100 pm. At first whitish becoming
yellowish flesh-colored and finally yellowishbrown t o nut-brown; when dried, reddishbrown. Sporangiophore white or yellowish,
1 0 p m to 25 by u p t o 6 0 p m , occasionally
poorly developed or absent. The resting cells in
the sporangia stand at right angles to the
enclosing membrane in several layers, the membrane has a honeycomb structure because of
the impingement of the resting cells against it.
Myxospores rod shaped, 3.3 pm by 6.0 to
9.0 pm (Fig. lo).
Vegetative colonies not described.
Cultivated with good growth on 10% dung
decoction agar and potato agar (1 2).
Starch is hydrolyzed. Cellulose not digested
(12).
Aerobic (12).
pH range, 4.0 t o 8.5 (12).
Temperature range, 20 to 3 1 C (1 2).
Source and habitat: From dung of various
herbivores, also from wet bark (12).
M elit t engium lichenicolum (T hax t e r) comb.
nov.
[Objective synonyms: Chondromyces Zichenicolus Thaxter 1892, Podangium lichenicolum
(Thaxter) Jahn 19241.
53
[ Subjective synonyms: Chondromyces gracilipes Thaxter 1897, Pondangium gracilipes
(Thaxter) Jahn 1924, Chondromyces minor
Krzemieniewska and Krzemieniewski 1930,
2651.
Vegetative rods (Fig. 8) are tapered, 0.6 pm
to 0.9 by 7 t o 12 pm (exponential cells, 0.6 p m
by 6 t o 8 pm).
Fruiting bodies are of two types. One (Fig.
2-4) consists of a single orange-red t o bright
red, spherical, ellipsoidal, or pear-shaped
sporangium, 15 t o 35 pm by 25 t o 35 pm, o n a
white t o orange, rigid stalk, 5 t o 1 0 p m by 10
to 40 pm. When crowded, the sporangia may be
confluent. S porangio phore s occasionally lacking but, when well developed, tapering at the
tip, persistent; the sporangia caducous. The
second type of fruiting body (Fig. 1) often
accompanies the first and is more usual o n
artificial media. It consists of an orange t o
bright red irregular mass, up t o 1 mm diameter,
with a swollen padded surface. Internally the
microcysts and slime are oriented t o form
numerous, closely oppressed, intestine-like convoluted tubes with a diameter of about 50 t o
9 0 pm. This form appears very similar to
Archangium primigenium or A. serpens.
Microcysts irregularly rod-shaped, often bent
and narrowing at the ends, rigid, phase-dense or
refractile, with a slime capsule (Fig. 5-7).
Usually in sheaves (Fig. 6 ) and difficult t o
separate .
Vegetative colonies o n agar media spread
very rapidly; very thin, nearly transparent, with
occasional reddish-orange t o bright red radial
folds and accumulations. Characteristically extends on the walls of the culture vessel and
between agar-glass interfaces. Lysis on ECM (6)
is very extensive.
Growth in Sp broth ( 6 ) is poor, in the form
of compact red spheres; the medium remains
clear.
Cultivated o n ECM, dung pellet, and Sp
agars (6) but with only limited growth.
Nitrate not reduced. Catalase is produced.
Oxidase negative. Hydrolyzes starch, ribonucleic acid, deoxyribonucleic acid, and usually
aesculin. Urease negative. Does not digest
cellulose.
Temperature range, 18 t o 37 C; optimum,
25 t o 28 C .
Antibiotic sensitivity (discs): Inhibited by
10 pg of tetracycline, chloramphenicol, and
kanamycin, and 5 pg of erythromycin. Response to neomycin (10 pg) and penicillin (10
units) variable.
Source and habitat: Originally observed on
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54
McCURDY
rabbit dung in contact with soil and on lichens.
Very common on moist tree bark.
Type: Acc. No. 4500 and 5170, Thaxter
c o l l e c t i o n , F a r l o w Herbarium, Harvard
University.
R e f e r e n c e s t r a i n : Windsor M201
(ATCC 25946).
Melittangium alboraceum (Peterson) comb.
nov. (Objective synonym: Podangium alboraceum Peterson, 1959.)
Vegetative cells, 0.8 to l.Opm by 4.5 t o
5.0 pm,no tapering apparent, square ends.
Fruiting body a single sporangium on a long,
white, irregularly corkscrew-shaped sporangiophore, 2 0 p m by 82 to 2 5 0 p m (average,
125 pm). The sporangium is an irregular globe,
pale orange, cystalline, 35 p m in diameter,
bounded by an elastic membrane which is
difficult t o see.
Myxospores rod-shaped, 0.8 by 2.5 pm,
slightly curved, difficult to separate from the
sporangium and one another.
Not cultivated.
Source and habitat: Observed twice on elm
bark.
Type: Three microscope slides, Peterson 72,
University of Missouri herbarium.
ACKNOWLEDGMENT
This investigation was supported by National Research Council of Canada grant A 1022.
LITERATURE CITED
1. Berkeley, M. J., and Curtis. 1874. In M. J. Berkeley
(ed.), Notices of the North American fungi.
Grevillea 3: 1 - 17.
2. Jahn, E. 1924. Beitrige zur botanischen Protisto-
INT. J. SYST. BACTERIOL.
logie. I. Die Polyangiden, p. 1-107. Gebruder
Borntraeger, Leipz ig.
3. Krzemieniewska, H., and S. Krzemieniewski.
1928. Morfulogia Komorko miksobakterj (Zur
Morphologie der Myxobakterienzelle). Acta SOC.
Bot. Pol. 5:46-90.
4. Krzemieniewska, H., and S. Krzemieniewski.
1930. Miksobakterie Polski. C z e b Trzecia (Die
Myxobakterien von Polen 111 Teil). Acta SOC.
Bot. Pol. 7:250-273.
5. Krzemieniewska, H., and S. Krzemieniewski.
1946. Myxobacteria of the species Chondromyces Berkeley and Curtis. Bull. Int. Acad.
Cracovien (Acad. Pol. Sci.) Ser. B Sci. Nat.
1 :3 1-48.
6. McCurdy, H. D. 1969. Studies on the taxonomy
of the Myxobacterales. I. Record of Canadian
isolates and survey of methods. Can. J. Microbiol. 15 :145 3 -146 1.
7. McCurdy, H. D. 1970. Studies on the taxonomy
of the Myxobacterales. 11. Polyangium and the
demise of the Sorangiaceae. Int. J. Syst.
Bacteriol. 20:283-296.
8. McCurdy, H. D. 1971. Studies on the taxonomy
of the Myxobacterales. 111. Chondromyces and
Stigmatella. Tnt. J. Syst. Bacteriol. 21:40-49.
9. McCurdy, H. D., and B. T. Khouw. 1969. Studies
on Stigmatella brunnea. Can. J . Microbiol.
15:731-738.
10. Peterson, J. E. 1959. New species of Myxobacteria from the bark of living trees. Mycologia
51:163-172.
11. Pronina, N. I. 1962. Description of new species
and varieties of cellulose-decomposing myxobacteria. Mikrobiologiya 31:470-477.
12. Solntzeva, L. I. 1941. Biology of the Myxobacteria. 11. Genera Melittangium and Chondromyces. M ikrob iologiya 10:5 0 5 -524.
13. Thaxter, R. 1892. On the Myxobacteraceae, a
new order of Schizomycetes. Bot. Gaz.
17~389-406.
14. Thaxter, R. 1897. Further observations on the
Myxobacteraceae. Bot. Gaz. 23:395-411.
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