International Journal of Systematic and Evolutionary Microbiology (2015), 65, 4032–4042
DOI 10.1099/ijsem.0.000533
Reclassification of Angiococcus disciformis,
Cystobacter minus and Cystobacter violaceus
as Archangium disciforme comb. nov.,
Archangium minus comb. nov. and Archangium
violaceum comb. nov., unification of the families
Archangiaceae and Cystobacteraceae,
and emended descriptions of the families
Myxococcaceae and Archangiaceae
Elke Lang,1 Peter Schumann,1 Brian J. Tindall,1 Kathrin I. Mohr2
and Cathrin Spröer1
Correspondence
Elke Lang
[email protected]
1
Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures,
Inhoffenstrasse 7B, 38124 Braunschweig, Germany
2
Helmholtz Centre for Infection Research, Microbial Drugs, Inhoffenstrasse 7,
38124 Braunschweig, Germany
The species Archangium gephyra, Angiococcus disciformis, Cystobacter minus and
Cystobacter violaceus are currently classified in three different genera of the order
Myxococcales. The 16S rRNA gene sequences of the respective type strains show a similarity
higher than 98.4 % and form a tight phylogenetic group. A dendrogram calculating the similarity
of MALDI-TOF spectra confirmed the close relatedness of the four species that grouped in a
monophyletic cluster in the neighbourhood of other species of the genus Cystobacter. The type
strains shared similar fatty acid patterns of high complexity with iso-C15 : 0, C16 : 1v5c and isoC14 : 0 3-OH as the major components. The vegetative cells of these species are uniformly long
needle-shaped rods, and the myxospores are short rods, ovoid or irregularly spherical thus
differing from the myxospores of species related to Cystobacter fuscus, the type species of this
genus. Some enzymic and hydrolysing reactions of the type strains are described. As a result of
the high relatedness and similarity of the four species, it is proposed to place them into one
genus, and due to phylogenetic and morphological distinctness, the species should be
classified in a genus distinct from the genus Cystobacter as Archangium gephyra (type strain
M18T5DSM 2261T5ATCC 25201T5NBRC 100087T), Archangium disciforme comb. nov.
(type strain CMU 1T5DSM 52716T5ATCC 33172T), Archangium minus comb. nov. (proposed
neotype strain Cb m25DSM 147515JCM 12627) and Archangium violaceum comb. nov.
(type strain Cb vi61T5DSM 14727T5CIP 109131T5JCM 12629T). Since the family
Archangiaceae Jahn 1924 AL has priority over the family Cystobacteraceae McCurdy 1970 AL,
it is proposed to assign the genera Archangium, Anaeromyxobacter, Cystobacter, Hyalangium,
Melittangium and Stigmatella to the family Archangiaceae. Emended descriptions of the families
Myxococcaceae and Archangiaceae are also provided.
Abbreviations: AL, Approved Lists of Bacterial Names (Skerman et al.,
1980); ECL, equivalent chain-length; MALDI-TOF, matrix-assisted laser
desorption/ionization time-of-flight.
Four supplementary tables are available with the online Supplementary
Material.
4032
At times when morphology was the most important feature
in the taxonomy of myxobacteria, four species had been
assigned to three different genera. Archangium gephyra,
Angiococcus disciformis (listed as Myxococcus disciformis,
see below for details) and Cystobacter minus are listed in
the Approved Lists of Bacterial Names (AL) (Skerman
et al., 1980) and Cystobacter violaceus was described in
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+
+
+
2
+
2
2
+
W
W
W
W
W
W
+
+
+
+
2
2
*Sequences of different clones.
DDescription from Reichenbach (2005). The type strain of C. fuscus no longer produces fruiting bodies under the conditions applied.
Isolation Source
Isolation location
GenBank accession no. for
16S rRNA gene sequence
Shape of spores
Decomposition of:
Starch
Xylan
Aesculin
Chitin
Rather slender rods with pointed
ends, often C- or S-shapedD
Oval to short rods,
may be bean-shaped
Oval to short rods, may be
bean-shaped
Short rods, may be beanshaped
Soil
Arizona, USA
AJ233903
Soil
Canada
DQ768106
Cb vi61T5DSM
14727T5CIP 109131T5JCM
12629T
Soil with plant residues
Rajasthan, India
DQ768114
M18T5DSM 2261T5ATCC
25201T5NBRC 100087 T
Type strain
CMU 1T5DSM
52716T5ATCC
33172T
Unknown
Michigan, USA
M94374, HE582768–
HE582771*
Coccoid to oval
Cb m25DSM
147515JCM 12627
Cystobacter violaceus
Weak decomposition.
W,
Cystobacter minus
Archangium gephyra
Angiococcus
disciformis
Species
All strains used were from Leibniz Institute DSMZ –
German Collection of Microorganisms and Cell Cultures,
and were maintained on VY/2 agar composed of (per
litre): 1.36 g CaCl2 . 2H2O, 5 g baker’s yeast, 15 g agar,
0.5 mg vitamin B12; pH was adjusted to 7.2 with sterile
KOH after autoclaving. All incubations were carried out
at 28 8C. The 16S rRNA gene sequences of the strains of
the four studied species were retrieved from the European
Nucleotide Archive (http://www.ebi.ac.uk/ena/) (Table 1).
Pairwise similarities of the 16S rRNA gene sequence of
Archangium gephyra DSM 2261T to those of Angiococcus
disciformis DSM 52716T, C. minus DSM 14751 and C. violaceus DSM 14727T were 98.6 %, 98.4 % and 98.6 %,
respectively (http://www.ezbiocloud.net/eztaxon; Kim
et al., 2012). The 16S rRNA gene sequence similarity
of Angiococcus disciformis DSM 52716T versus C. minus
DSM 14751 and C. violaceus DSM 14727T were 98.8 %
The 16S rRNA gene sequences were determined from type strain cultures underlined in the table.
The type strain of C. minus has been lost, and for that
reason, strain Cb m2 (5DSM 14751) was proposed as
neotype strain (Lang & Reichenbach, 2013) and is
included as the representative of this species in this
study. It will be established as neotype strain in November
2015, two years after the publication of its proposal [Rule
18c of the Bacteriological Code (Lapage et al., 1992)].
Table 1. Species and type strains used in this study, and selected differential characteristics
When the first almost-comprehensive description of the
phylogenetic relationships of myxobacteria based on 16S
rRNA gene sequences appeared, the type strain of Archangium gephyra formed a branch distinct from other type
strains, confirming the existence of the species on a molecular basis (Spröer et al., 1999). However, two non-type
strains morphologically classified as Angiococcus disciformis grouped phylogenetically with the type strain of Archangium gephyra, demonstrating the high relationship of
these species. The (type) strains assigned to the four
species Archangium gephyra, Angiococcus disciformis,
Cystobacter minus and Cystobacter violaceus form one
monophyletic branch (Garcia et al., 2010). The aim of
the present study was to compare the morphological
and physiological characters of these species in order to
evaluate their assignment to one common genus. One
reason for the reassessment of the taxonomic position of
these species is their production of secondary metabolites
with perspectives in pharmaceutical application (Reichenbach & Höfle, 1993; Schäberle et al., 2014).
Cystobacter fuscus
Reichenbach (2005). A historical survey indicates that
three of the species experienced reclassification in different
genera over time, sometimes repeatedly (Table S1, available in the online Supplementary Material). This fact illustrates that there was no clear rationale to assign these
species to the one or the other genus, and that the classification systems rather depended on the importance that
the author allocated to specific morphological features.
In particular, recognition of members of the genus Archangium is described as problematic: ‘The borderline
between Archangium and the genera with sporangioles
is markedly fluid’ (Reichenbach, 2005).
M29T5DSM 2262T5ATCC
25194T5CECT 4287T5NBRC
100088T
Soil
Canada
DQ768109
New combinations in the genus Archangium
4033
E. Lang and others
and 98.7 %, respectively, and the similarity between those
of C. minus DSM 14751 and C. violaceus DSM 14727T
was 99.5 % (Table S2). Such high similarity values are generally expected among strains belonging to one genus or
even one species (Meier-Kolthoff et al., 2013). The 16S
rRNA gene sequence similarities of these four species
towards the four Cystobacter species sensu stricto, Cystobacter fuscus, Cystobacter ferrugineus, Cystobacter badius and
Cystobacter velatus, were lower than 98.2 %. The Cystobacter species sensu stricto are nearly indistinguishable from
each other by their 16S rRNA gene sequences. Phylogenetically, the four species studied here form a branch separate
from that including the Cystobacter species sensu stricto
(Garcia et al., 2010; Spröer et al., 1999).
The close phylogenetic relatedness and morphological
similarity of C. minus and C. violaceus prompted us to
determine whether the type strains belong to one species
by applying DNA–DNA hybridization. Cells were disrupted
by using a Constant Systems TS 0.75 kW (IUL Instruments) and the DNA in the crude lysate was purified by
chromatography on hydroxyapatite as described by Cashion et al. (1977). DNA–DNA hybridization was carried
out as described by De Ley et al. (1970) under consideration of the modifications described by Huss et al. (1983)
using a model Cary 100 Bio UV/VIS-spectrophotometer
equipped with a Peltier-thermostatted 666 multi-cell
changer and a temperature controller with in situ
temperature probe (Varian). The DNA–DNA relatedness
value (9.6 %) was far below the threshold of 70 % given
for membership within one species (Wayne et al., 1987).
Biomass for whole-cell fatty acid analyses and matrixassisted
laser
desorption/ionization
time-of-flight
(MALDI-TOF) mass spectra was cultivated on CY agar
(3.0 g casitone, 1.36 g CaCl2 . 2H2O, 1.0 g yeast extract
and 14 g agar per litre; pH 7.2) for approximately 2 days.
Cells were harvested as soon as enough biomass with as
few myxospores or fruiting bodies as possible became available. These plates had been inoculated with a suspension of
cells freshly grown on VY/2 agar. Sample preparation for
MALDI-TOF mass spectrometry was carried out according
to Protocol 3 in Schumann & Maier (2014). Instrumental
conditions for the measurement were used as described
by Tóth et al. (2008). The comparison of MALDI-TOF
mass spectra confirmed the close relatedness of the four
species. In a score-oriented dendrogram (average linkage,
distance measure: correlation), calculated from the spectra
of the type strains of the four species and related organisms
by using the Biotyper software (Bruker Daltonics; version
3.1), Archangium gephyra DSM 2261T, Angiococcus disciformis DSM 52716T, C. violaceus DSM 14727T and C. minus
DSM 14751 grouped together in a monophyletic cluster
in the neighbourhood of other species of the genus Cystobacter (Fig. 1). The type strain of Archangium gephyra was
the most distant strain among the four strains studied.
DSM 14698T Pyxidicoccus fallax
DSM 16525T Myxococcus fulvus
DSM 71T Nannocystis exedens
DSM 2261T Archangium gephyra
DSM 14727T Cystobacter violaceus
DSM 14751 Cystobacter minus
DSM 52716T Angiococcus disciformis
DSM 14712T Cystobacter miniatus
DSM 14718T Cystobacter velatus
DSM 2262T Cystobacter fuscus
DSM 14716T Cystobacter ferrugineus
DSM 14723T Cystobacter badius
1000
900
800
700
600
500
Distance Level
400
300
200
100
0
Fig. 1. Dendrogram of the MALDI-TOF spectra of type strains of the genus Cystobacter and other genera of the
Myxococcales.
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New combinations in the genus Archangium
Fatty acid methyl esters were obtained as described previously (Kämpfer & Kroppenstedt, 1996) and separated
by using a gas chromatograph (model 5898A; Hewlett
Packard). Peaks were automatically computed and assigned
using the Microbial Identification software package
(MIDI), TSBA40 method, Sherlock version 4.5. The fatty
acid patterns of the four strains were dominated by isoC15 : 0, iso-C14 : 0 3-OH and C16 : 1v5c, and contained
low amounts of C14 : 0, C15 : 0, iso-C16 : 0, C16 : 0, isoC17 : 0, substances with equivalent chain-lengths (ECLs)
of 13.565, 14.959, 15.687 and 17.875, and summed feature
4 (including anteiso-C17 : 1 B/iI), accompanied by trace
amounts (,1 %) of other compounds (Table 2). The culture age and most possibly intracellular prearrangements
accompanying myxospore and fruiting body formation
may affect the fatty acid composition. Taking into account
that these conditions cannot be adjusted (consistently)
among these strains, the fatty acid compositions of the
four strains were highly similar. The composition of Angiococcus disciformis displayed the highest complexity as already
stated by Garcia et al. (2011). Since the fatty acid pattern of
the type strain of C. fuscus also showed a high similarity,
fatty acid pattern determination seems not to be a suitable
tool for the discrimination of the studied species from
those of the core Cystobacter group. We did not confirm
the exceptionally high amount of C18 : 0 in Archangium
gephyra which was detected by Garcia et al. (2011). Possibly
the different growth conditions (liquid media versus agar
plates, different media composition) chosen in the two
studies resulted in the different outcomes.
Morphology of the spores and colour of the fruiting bodies
were observed in VY/2 cultures or in cultures grown on
streaks of dead or living cells of Escherichia coli as food bacteria on WAT agar (per litre: 1.0 g CaCl2 . 2H2O and 15 g
agar). The vegetative cells of all four species are uniformly
described as long slender, needle-shaped rods (Table S3).
The myxospores of the cultures studied were ovoid or irregularly spherical (Angiococcus disciformis) or short stout
rods with rounded ends, often a mixture of both. The
spores of Archangium gephyra DSM 2261T and C. violaceus
DSM 14727T were bean-shaped in part. None of the four
taxa developed the bent rods with pointed ends characteristic for the Cystobacter species sensu stricto. These are
demonstrated in Fig. 2 for a typical strain of C. fuscus
(see also Table S3).
The designated type strains for Archangium gephyra and C.
fuscus had been maintained in laboratories for decades and
did not develop fruiting bodies in our laboratory. However,
Archangium gephyra DSM 2261T formed small heaps, uniformly distributed over the surface of agar VY/2, similar to
the distribution of fruiting bodies of Corallococcus strains.
These heaps contained cells transformed to myxospores
(Fig. 2). The yellow fruiting bodies of C. minus DSM 14751
aggregated irregularly on the surface, were piled up or were
built on the tips of slime masses rising up from the agar
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Table 2. Cellular fatty acid compositions (%) of strains used
in this study and the type strain C. fuscus (type species of
genus)
Strains: 1, Archangium gephyra DSM 2261T; 2, Angiococcus disciformis
DSM 52716T; 3, Cystobacter minus DSM 14751; 4, Cystobacter violaceus DSM 14727T; 5, Cystobacter fuscus DSM 2262T.
Peak naming and calculation by method TSBA40. Only values
.0.2 % are listed. V , Traces detected only in one of duplicate
measurements.
Fatty acid
1
2
3
C10 : 0
iso-C11 : 0
C12 : 0
iso-C13 : 0
C13 : 1 AT 12-13
Unknown 13.565*
C14 : 1v5c
iso-C14 : 0
Unknown 13.945
Unknown 13.766
C14 : 0
Summed feature 1D
iso-C15 : 0
anteiso-C15 : 0
Unknown 14.959
C15 : 0
iso-C14 : 0 3-OH
Summed feature 2D
C16 : 1v7c alcohol
iso-C16 : 0
Unknown 15.687
C16 : 1v11c
C16 : 1v5c
C16 : 0
iso-C15 : 0 3-OH
Unknown 16.271
iso-C15 : 0 3-OH
iso-C17 : 1v10c
Summed feature 4D
iso-C17 : 0
C16 : 0 2-OH
C16 : 0 3-OH
Unknown 17.875
iso-C17 : 0 3-OH
Unknown 19.313
0.2
0.3
0.4
0.5
V
5
1.8
0.6
0.4
0.3
2.3
0.4
0.3
0.2
0.3
1.7
0.8
V
0.3
V
V
3.2
4
V
0.3
0.2
3.6
0.4
V
0.3
5.0
0.7
28.8
0.7
1.5
12.6
0.7
4.2
0.6
26.3
0.3
0.8
16.1
6.4
0.6
18.8
5.1
0.8
19.1
0.9
0.8
8.4
2.0
1.5
10.1
V
1.0
1.0
21.8
11.0
0.5
V
3.2
0.3
V
4.3
0.5
1.5
0.6
3.0
3.0
1.1
18.5
5.3
0.7
0.6
0.5
2.2
4.7
V
0.7
7.2
0.3
3.9
0.7
2.1
0.4
1.7
34.3
2.9
0.6
35.0
2.9
0.5
37.7
7.9
0.8
0.3
4.6
0.5
1.1
7.8
0.5
0.3
7.2
0.6
V
V
V
7.2
0.7
20.9
V
V
0.4
1.7
8.4
0.3
V
5.3
0.6
V
4.3
0.5
0.8
4.1
V
V
*Unknown fatty acid or alcohol with an equivalent chain-length
(ECL) of 13565.
DSummed features are groups of two or three fatty acids that are treated together for the purpose of evaluation in the MIDI system, and
include both peaks with discrete ECLs as well as those where the
ECLs are not reported separately [see Montero-Calasanz et al.
(2014)]. Summed feature 1 contained iso-C15 : 1 and/or C13 : 0 3OH; summed feature 2 contained iso-C16 : 1I and/or C14 : 0 3-OH;
summed feature 4 contained anteiso-C17 : 1 B/i I.
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E. Lang and others
(b)
(a)
(c)
(d)
(e)
Fig. 2. Myxospores of Angiococcus disciformis DSM 52716T (a), Archangium gephyra DSM 2261T (b), Cystobacter minus
DSM 14751 (c), Cystobacter violaceus DSM 14727T (d) and Cystobacter fuscus DSM 52657 (e). Bars, 10 mm (a–d), 5 mm (e).
(Fig. 3b, c, d). The sporangioles of the type strain of
Angiococcus disciformis appearing on streaks of E. coli
were composed of sporangioles clearly enclosed by
opaque envelopes and sitting singly on the agar surface
4036
in clusters, thus resembling those of members of the
genus Melittangium. The oblate form of the sporangioles
described earlier (Thaxter 1904; Hook et al., 1980) was
not clearly noticeable (Fig. 3a). The larger, dark
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New combinations in the genus Archangium
(a)
(b)
(c)
(d)
(e)
Fig. 3. Fruiting bodies of Angiococcus disciformis DSM 52716T (a), Cystobacter minus DSM 14751 [b, c, d (side view)]
and Cystobacter violaceus DSM 14727T (e). Bars, 100 mm (a, c), 200 mm (b, d, e).
sporangioles of C. violaceus DSM 14727T produced
meandering curves and lines on top of the agar surface.
These resembled most closely the fruiting bodies of the
core species of the genus Cystobacter (Fig. 3).
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Starch, xylan and aesculin hydrolysis, NaCl tolerance and
enzyme activities (API ZYM strips; bioMérieux) were
tested as described previously (Lang & Stackebrandt,
2009). Briefly, overlay agar plates containing 2 g potato
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E. Lang and others
starch or 5 g oat spelt xylan or 5 g colloidal chitin (Hsu &
Lockwood, 1975) per litre, respectively, were inoculated at
one spot and incubated for 4 or 5 days. Starch and xylan
degradation were detected after covering with Lugol’s solution. Clear halos larger than the swarm diameter were
scored positive. Aesculin hydrolysis was evaluated after
growth for up to 8 days on agar slants containing CY agar
plus aesculin, citrate and ferric citrate. Salt tolerance was
measured on CY agar plates containing 1.5 % NaCl. All
strains hydrolysed starch and xylan. Chitin was decomposed
by the strains assigned to the genus Cystobacter but not by
those of Archangium gephyra or Angiococcus disciformis
(Table 1). Aesculin was hydrolysed weakly by the strains of
C. minus and C. violaceus. Enzymic properties were tested
using the API ZYM strips displaying an individual enzyme
pattern for each of the strains. The strains of C. violaceus
and C. fuscus were the most active, while Angiococcus disciformis DSM 52716T was the least active strain showing only
alkaline and acid phosphatases, esterase, esterase-lipase and
naphthol-AS-BI-phosphohydrolase activities; these enzymes
were expressed in all strains (Table S4).
In the ‘Key to the species’ of the genus Cystobacter in Bergey’s Manual, two groups of species of the genus Cystobacter are distinguished. One group, including the type species
C. fuscus, forming ‘...myxospores relatively slender rods of
moderate length and with more or less tapering ends’, and
another group comprising the species C. minus, ‘Cystobacter disciformis’ (sic), C. violaceus and Cystobacter gracilis,
and forming ‘...myxospores very short fat rods to almost
spherical...’ (Reichenbach, 2005). While C. gracilis groups
with members of the genera Stigmatella and Hyalangium
in the 16S rRNA gene sequence tree (Garcia et al., 2010),
the species C. minus, Angiococcus/‘Cystobacter disciformis’
and C. violaceus cluster with Archangium gephyra. Thus,
the phylogenetic relatedness of these three species correlates with their morphological distinction.
The four type strains presently assigned to three different
genera displayed high similarities regarding cell and myxospore morphology, fatty acid pattern, 16S rRNA gene
sequence and MALDI-TOF mass spectra. Moreover, strains
of Archangium gephyra and C. violaceus produce chemically
similar polyketides, named archazolids, and strains of Angiococcus disciformis and Arcahgium gephyra produce peptides,
called tubulysins (Chai et al., 2010; Horstmann et al., 2011).
In conclusion, we propose to assign the four related species in
one genus distinct from the genus Cystobacter. This measure
will, based on a molecular basis, abandon an over-subdivison
of these taxa that was established at a time when the enthusiasm about morphological diversity and the developmental
capacities of the myxobacteria was culminating.
It is proposed to assign the four species to the genus Archangium, as Archangium gephyra, Archangium disciforme
comb. nov., Archangium minus comb. nov. and Archangium violaceum comb. nov. for the following reasons:
Rule 44 of the Bacteriological Code (Lapage et al., 1992)
reads: ‘If two or more species of different genera are
4038
brought together to form a genus, and if these species
include the type species of one or more genera, the name
of the genus is that associated with the type species
having the earliest legitimate generic name’. The genera
names Angiococcus and Archangium were described in the
same year, 1924, by Jahn (Tables S1 and S3). However,
only the genus name Archangium is listed on the AL
(Skerman et al., 1980) while the genus name Angiococcus
Jahn 1924 is not included. Although not proposed as
such, Angiococcus is a revived name (Rule 28a) and
should be cited as Angiococcus (ex Jahn 1924) Hook et al.
1980. Similarly, the species name Angiococcus disciformis
(Thaxter 1904) Jahn 1924 did not appear on the AL, but
an emended description was provided and a neotype
strain was designated by Hook et al. in 1980 on pages
135–142 of the Int J Syst Bacteriol (Hook et al. (1980).
However, on closer inspection of the strain history, the
type strain (CMU-1T5ATCC 33172T) of Angiococcus disciformis, as given by Hook et al. (1980), is listed under the
name Myxococcus disciformis Thaxter 1904 on the AL.
Thus the species combination Angiococcus disciformis is
both a homotypic synonym of Myxococcus disciformis
Thaxter 1904 AL, as well as a revival of a combination originally proposed by Jahn (1924), based on the species name
proposed by Thaxter (1904). Consequently, the species
combination should be cited as Angiococcus disciformis
(Thaxter 1904) Hook et al. 1980. This would be then consistent with the view that the genus and species names are
validly published as defined by Rules 23a and 24a (Lapage
et al., 1992). Based on these arguments, the genus name
Angiococcus, which does not appear on the AL must be
attributed to Hook et al. (1980) as a revived name. It therefore follows that the genus name Archangium Jahn 1924 AL
has priority over the genus name Angiococcus (ex Jahn
1924) Hook et al. 1980.
The different species had been assigned to three different
families, Angiococcus disciformis to the family Myxococcaceae by Jahn (1924) and Hook et al. (1980), Archangium
gephyra to the family Archangiaceae by Jahn (1924), and
C. minus and C. violaceus to the family Cystobacteraceae
by Reichenbach (2005). The unification of the species in
one genus demands the re-evaluation of the question in
which family the genus is allocated correctly. Based on
Rules 23b and 24b, the priority of family names placed
on the AL is determined by the date of effective publication
prior to the AL. Since both family names Cystobacteraceae
and Archangiaceae were included in the AL, the family
name Archangiaceae Jahn 1924 has priority over the
family name Cystobacteraceae McCurdy 1970.
In recognizing that Angiococcus disciformis should be placed
in the genus Archangium as Archangium disciforme Thaxter
1904 comb. nov., this species is also placed in the family
Archangiaceae - de facto removing the genus Angiococcus
(ex Jahn 1924) Hook et al. 1980 (treated here as a heterotypic synonym of Archangium Jahn 1924 AL), and the
species Angiococcus disciformis (ex Jahn 1924) Hook et al.
1980 [treated here as a homotypic synonym of Myxococcus
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New combinations in the genus Archangium
disciformis (Thaxter 1904)], from the family Myxococcaceae
Jahn 1924 AL. Phylogenetic studies (Garcia et al., 2010)
clearly exclude the classification of this species in the
family Myxococcaceae and support the inclusion in the
family Archangiaceae.
McCurdy (1970) treats the genera Archangium Jahn 1924
and Cystobacter Schroeter 1886 as belonging to the families
Archangiaceae Jahn 1924 and Cystobacteraceae McCurdy
1970, respectively. It is therefore appropriate to provide
emended descriptions of the families Archangiaceae Jahn
1924 and Myxococcaceae Jahn 1924.
Currently, the genera Anaeromyxobacter, Hyalangium and
Stigmatella are assigned to the family Cystobacteraceae
McCurdy 1970. Following the statement of the priority of
the genus name Archangiaceae, these species are grouped
correctly under the latter family name. However, phylogenetic analysis suggests that these three genera do not form
one branch with the other genera assigned to the family
Archangiaceae, namely Archangium, Cystobacter and Melittangium. Instead, members of the genera Hyalangium and
Stigmatella and the species Cystobacter gracilis phylogenetically group with members of the family Myxococcaceae
(Garcia et al., 2010). Members of the genus Anaeromyxobacter are the only known myxobacteria having a facultatively anaerobic lifestyle, using a wide range of unusual
electron acceptors (Sanford et al., 2002). This extraordinary
metabolism comes together with a deep-branching point in
the phylogenetic tree, at the suborder level. These facts
demand a re-evaluation of the taxonomic positions of
these genera in the future.
Emended description of the family
Myxococcaceae Jahn 1924 AL
Herewith contains currently the genera Myxococcus, Aggregicoccus, Corallococcus and Pyxidicoccus.
The characters of the family are described by Jahn (1924)
and Reichenbach (2005). ‘The rods contract to build
round spores in the fruiting bodies. During sporulation,
the spores elongate to rods without dropping an envelope’
[translated from German, Jahn 1924].
Vegetative cells are slender rods with tapering ends, 0.7–
0.8 mm|3–8 mm. Myxospores have a thick capsule, are
spherical or ellipsoidal, sometimes slightly deformed, 1.2–
2.5 mm in diameter, optically refractile when fully developed.
Nutrition is proteolytic–bacteriolytic (Reichenbach, 2005).
The type genus is Myxococcus Thaxter 1892.
Emended description of the family
Archangiaceae Jahn 1924 AL
Contains currently the genera Archangium Jahn 1924 AL,
Anaeromyxobacter Sanford et al. 2002 VL, Cystobacter
Schroeter 1886 AL, Hyalangium Reichenbach 2007 VL,
Melittangium Jahn 1924 AL and Stigmatella Berkeley and
Curtis 1875 AL.
http://ijs.microbiologyresearch.org
The family members may have the characters described by
Jahn (1924) for the family Archangiaceae ‘The swarms
build irregularly bulging or sidled fruiting bodies or columnar or finger-like extensions, mostly without clearly
discernable membrane’ [translated from German by
E. Lang]; and/or those described by McCurdy (1970) for
the family Cystobacteraceae ‘Vegetative cells tapered flexible
rods which are converted to refractile or phase-dense, rodshaped microcysts enclosed in sporangia of definite shape.
The sporangia may be sessile, occurring singly or in groups
and enclosed in a slime membrane or envelope; or borne
on stalks (sporangiophores) which may be simple or
branched. The sporangia may be solitary or in clusters at
the tips of the stalks. The vegetative colonies do not etch
or erode agar. Congo red is adsorbed by the vegetative
slime. All of the species examined grow well in media containing enzymatically hydrolyzed protein, starch and salts’;
or those characters described for the genus Anaeromyxobacter by Sanford et al. (2002) ‘...myxobacterial species
that are capable of facultative anaerobic growth using terminal electron acceptors such as nitrate, fumarate, and chlorophenolic compounds. Sulfur compounds are not reduced.
Oxygen is used but only at low concentrations. The morphological description of this genus is the same as that of
the type[...]and only species...’ and for the species Anaeromyxobacter dehalogenans ‘Cells are narrow rods 4 to 8 mm
long and 0.25 mm wide that exhibit gliding motility. Terminal ends of cells have pilus structures and form blebs periodically[...]Cysts are visible in older cultures’.
The type genus is Archangium Jahn 1924.
Emended description of the genus Archangium
Jahn 1924 AL
The descriptions of the genus by McCurdy (1974), and of
the species included - Angiococcus disciformis by Thaxter
(1904), Jahn (1924), McCurdy (1974) and Hook et al.
(1980); Cystobacter minus by Krzemieniewska & Krzemieniewski (1926) and McCurdy (1970); and Cystobacter violaceus by Kühlwein & Gallwitz (1958), Kühlwein &
Reichenbach (1964) and Reichenbach (2005) - can be summarized and emended as follows: Gram-negative, gliding
bacteria, undergoing development upon starving conditions. Vegetative cells are long slender rods with tapered
ends. The swarms form tough slime sheets with radial
veins. Does not engrave the agar. Congo red is adsorbed.
Myxospores are irregularly coccoid, oval or short rods
with blunt but never tapered ends, optically refractile
when fully developed. The fruiting bodies containing the
myxospores consist either of distinct oval to spherical sporangioles, somewhat oblate for one species, which are gathered in plaques, knobs, cones or ridges, sometimes forming
fingers, attached directly to the agar surface or occasionally
formed on a short slime cushion, or the fruiting bodies
consist of contorted interloped strings, sometimes subdivided by constrictions often resembling undetached sporangioles. Decomposes starch and xylan. May or may not
decompose aesculin or chitin. Whole-cell fatty acids are
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4039
E. Lang and others
dominated by iso-C15 : 0, iso-C14 : 0 3-OH and C16 : 1v5c,
and contain low amounts of C14 : 0, C15 : 0, iso-C16 : 0,
C16 : 0, iso-C17 : 0, substances with an ECL of 13.565,
14.959, 15.687 and 17.875, and summed feature 4
(including anteiso-C17 : 1 B/iI), accompanied by trace
amounts of other compounds. The G+C content of the
DNA of two species is concurrently 68 mol%.
3-OH, C16 : 0 and C16 : 1v5c (this study), or iso-C15 : 0,
C16 : 1v5c, iso-C17 : 0 and iso-C17 : 0 2-OH (Garcia et al.,
2011), respectively.
The type strain is CMU 1T (5DSM 52716T5ATCC
33172T). The GenBank accession numbers of the 16S
rRNA genes of different clones of the type strain are
HE582768–HE582771.
The type species is Archangium gephyra Jahn 1924.
Emended description of Archangium gephyra
Jahn 1924 AL
Synonyms: ‘Chondromyces serpens’ Quehl 1906, ‘Myxococcus cerebriformis’ Kofler 1913, ‘Chondrococcus cerebriformis’ (Kofler) Jahn 1924.
The characters of the species are described by Jahn (1924),
McDonald (1965, 1967), McCurdy (1974), Galván et al.
(1992) and Reichenbach (2005). Vegetative cells are slender
rods, 0.4–0.8|6–15 mm. Swarm colonies are thin with
radiating ridges and concentric folds, can be cut easily.
Myxospores are short fat rods with rounded ends, often
slightly bean-shaped, up to almost spherical, 1–2|1.5–
2.8 mm. Fruiting bodies consist of irregular bulges or
sidled ridges, up to 1 mm, reddish, without envelope;
inside contorted interlooped strings, 40–60 mm wide,
sometimes subdivided by irregular constrictions. The
fatty acid pattern may be dominated by C14 : 0, iso-C15 : 0,
iso-C14 : 0 3-OH, C16 : 0 and C16 : 1v5c (this study) or isoC15 : 0, C16 : 0, C16 : 1v5c, iso-C17 : 0 2-OH and C18 : 0
(Garcia et al., 2011), respectively.
The type strain is M18T (5DSM 2261T5ATCC
25201T5NBRC 100087T). The GenBank accession no. of
the 16S rRNA gene of the type strain is DQ768106.
Description of Archangium disciforme (Hook
et al. 1980) comb. nov.
Archangium disciforme (dis.ci.for9me. Gr. masc. n. diskos
disk; L. fem. n. forma form, shape; N.L. neut. adj. disciforme
disk-shaped).
Basonym: ¤ Myxococcus disciformis Thaxter 1904 AL.
Other synonym: Angiococcus disciformis (Thaxter 1904)
Hook et al. 1980, comb. nov. VP.
Shows the properties described by Thaxter (1904), Hook
et al. (1980) and (under the name ‘Cystobacter disciformis’)
Reichenbach (2005). Vegetative cells are slender, needlelike rods, 0.5–0.7|2–10 mm. Myxospores are ellipsoidal
or irregularly spherical, enclosed in a tenacious matrix,
1–1.9 mm in diameter, optically refractile. Fruiting bodies
are more or less disk-shaped, circular to oval, crowded, sessile or irregularly heaped, and pale dull orange–yellow
when mature. Sporangioles are enveloped by a thin but distinct wall, becoming very slightly wrinkled when ageing,
10–15|30–70 mm. Major components of the complex
whole-cell fatty acid pattern may be iso-C15 : 0, iso-C14 : 0
4040
Description of Archangium minus (McCurdy 1970)
comb. nov.
Archangium minus [min9us. L. neut. adj. minus (comparative of parvus small), smaller].
Basonym: Cystobacter minus (Krzemieniewska and Krzemieniewski 1926) McCurdy 1970 AL.
Other synonym: ‘Polyangium minus’ Krzemieniewska and
Krzemieniewski 1926.
The species characteristics are given by Krzemieniewska &
Krzemieniewski (1926), McCurdy (1970, 1974) and Reichenbach (2005). Vegetative cells are slender rods with
tapered ends, 0.4–0.7|3–11 mm. Myxospores are stout
short rods with blunt ends to almost spherical, 0.8–
1.4|1.0–2.7 mm. Fruiting bodies consist of spherical or
oval sporangioles, 20–50|20–80 mm, light rose or brownish, with a translucent wall, 0.5–1.0 mm thick, embedded in
a colourless translucent slime. Flat sori may cover surfaces
up to 0.5 mm, or sori may sometimes pile up forming
finger- or tree-like structures. Formation of secondary sporangioles within primary ones is observed. Major whole-cell
fatty acids may be iso-C15 : 0, iso-C14 : 0-3-OH, C16 : 1v5c,
iso-C17 : 0 and an unknown compound with an ECL of
17.875 (this study), or iso-C15 : 0, C16 : 0, C16 : 1v5c, isoC17 : 0 and iso-C17 : 0 2-OH (Garcia et al., 2011).
The proposed neotype strain is Cb m2 (5DSM
147515JCM 12627). The GenBank accession no. of the
16S rRNA gene of the proposed neotype strain is AJ233903.
Description of Archangium violaceum
(Reichenbach 2007) comb. nov.
Archangium violaceum (vi.o.la9ce.um. L. neut.adj. violaceum violet-coloured).
Basonym: Cystobacter violaceus (ex Kühlwein and Gallwitz
1958) Reichenbach 2007 VL.
Other synonyms: ‘Polyangium violaceum’ Kühlwein and
Gallwitz 1958, ‘Archangium violaceum’ Kühlwein and
Reichenbach 1964.
The species is as described by Kühlwein & Gallwitz (1958),
Kühlwein & Reichenbach (1964) and Reichenbach (2005).
Vegetative cells are slender rods with tapering ends, 0.5–
0.7|8–12 mm. Myxospores are short rods with rounded
ends, often bean- or S-shaped, 0.8–1.8|1.8–4.0 mm. Sporangioles are spherical to oval, large, 95–130|128–185 mm,
single or in groups, and dull brown to deep violet. Major
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New combinations in the genus Archangium
fatty acids are C14 : 0, iso-C15 : 0, iso-C14 : 0 3-OH, C16 : 1v5c,
iso-C17 : 0 and an unknown compound with an ECL of
17.875 (this study) or iso-C15 : 0, C16 : 1v5c and iso-C17 : 0
2-OH (Garcia et al., 2011).
The type strain is strain Cb vi61T (5DSM 14727T5CIP
109131T5JCM 12629T). The GenBank accession no. for
the 16S rRNA gene sequence of the type strain is DQ768114.
Polski (Die Myxobakterien von Polen). Acta Soc Bot Polon 4, 1–54
(in Polish with German abstract).
Kühlwein, H. & Gallwitz, E. (1958). Polyangium violaceum nov. spec.
Arch Mikrobiol 31, 139–145 (in German).
Kühlwein, H. & Reichenbach, H. (1964). Ein neuer Vertreter der
Myxobakteriengattung Archangium Jahn. Arch Mikrobiol 48,
179–184 (in German).
Lang, E. & Reichenbach, H. (2013). Designation of type strains for
Acknowledgements
We wish to thank C. Berg, G. Pötter, A. Wasner, W. Collisi and
B. Sträubler for excellent technical assistance. We appreciate the
readiness of members of the JCM and CIP to accept (proposed) myxobacterial type strains for deposit in the open collection notwithstanding extended efforts.
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