International Journal of Systematic and Evolutionary Microbiology (2015), 65, 778–783
DOI 10.1099/ijs.0.000012
Gemmobacter intermedius sp. nov., isolated from a
white stork (Ciconia ciconia)
Peter Kämpfer,1 Leszek Jerzak,2 Gottfried Wilharm,3 Jan Golke,4
Hans-Jürgen Busse4 and Stefanie P. Glaeser1
Correspondence
1
Peter Kämpfer
2
peter.kaempfer@umwelt.
uni-giessen.de
Institut für Angewandte Mikrobiologie, Universität Giessen, Giessen, Germany
Wydział Nauk Biologicznych, Uniwersytet Zielonogórski, Zielona Góra, Poland
3
Robert Koch-Institut, Bereich Wernigerode, Wernigerode, Germany
4
Institut für Bakteriologie, Mykologie und Hygiene, Veterinärmedizinische Universität, A-1210 Wien,
Austria
A cream-coloured, Gram-stain-negative, aerobic, non-motile, rod- to irregular shaped bacterium,
strain 119/4T, was isolated from a choana swab of a white stork nestling on sheep blood agar.
16S rRNA gene sequence analysis and subsequent comparisons showed that it was a member of
the family Rhodobacteraceae, showing 94.9 % similarity to the type strain of Gemmobacter
tilapiae and 94.6 % similarity to that of Gemmobacter nectariphilus, but also similarly low
sequence similarity to the type strains of Rhodobacter viridis (94.8 %), Rhodobacter veldkampii
(94.6 %) and Paenirhodobacter enshiensis (94.6 %). Reconstruction of phylogenetic trees
showed that strain 119/4T clustered close to species of the genus Gemmobacter. The quinone
system contained high amounts of ubiquinone Q-10 with traces of Q-8, Q-9 and Q-11, and the
fatty acid profile consisted mainly of C18 : 1v7c, C16 : 1v7c/iso-C15 : 0 2-OH and C10 : 0 3-OH. The
predominant polar lipids were diphosphatidylglycerol, phosphatidylethanolamine, phoshatidylglycerol and phosphatidylcholine. Major polyamines were putrescine and spermidine. On the basis of
16S rRNA gene sequence analysis and chemotaxonomic and physiological data, strain 119/4T
represents a novel species of the genus Gemmobacter, for which the name Gemmobacter
intermedius sp. nov. is proposed. The type strain is 119/4T (5CIP 110795T5LMG
28215T5CCM 8510T).
The genus Gemmobacter is grouped within the family
Rhodobacteraceae, which contains both photosynthetic and
non-photosynthetic genera. It was first proposed by Rothe
et al. (1987) and the description was later emended by Chen
et al. (2013). At the time of writing, the genus contained
ten recognized species from various habitats: Gemmobacter
aquatilis (Rothe et al., 1987; Chen et al., 2013), G. nectariphilus
(Tanaka et al., 2004; Chen et al., 2013), G. changlensis (Anil
Kumar et al., 2007; Zheng et al., 2011; Chen et al., 2013), G.
aquaticus (Liu et al., 2010; Chen et al., 2013), G. caeni
(Zheng et al., 2011; Chen et al., 2013), G. nanjingensis
(Zhang et al., 2012; Chen et al., 2013), G. fontiphilus (Chen
et al., 2013), G. tilapiae (Sheu et al., 2013a), G. lanyuensis
(Sheu et al., 2013b) and G. megaterium (Liu et al., 2014).
During investigations of the biodiversity of bacteria present
in white stork nestlings in 2013 in Poland, strain 119/4T
was isolated from a swap of a choana of a nestling. The
Abbreviation: LTP, ‘All-Species Living Tree’ project.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene
sequence of strain 119/4T is KM407667.
778
strain was cultured on sheep blood agar. The strain was
maintained and subcultured also on tryptone-soy agar
(TSA) at 28 uC. Good growth was obtained within 2 days.
Gram-staining was performed as described by Gerhardt
et al. (1994). Cell morphology was observed under a Zeiss
light microscope at 10006 magnification. The pH range
for growth was determined in nutrient broth (Oxoid),
which was adjusted prior to sterilization to pH 3–11 (at 0.5
pH unit intervals), and the temperature range for growth
was determined by testing growth at 10, 15, 20, 25, 30, 35
and 35–60 uC (5 uC intervals) on nutrient agar. Morphological, physiological and biochemical characteristics of
strain 119/4T are listed in the species description and in
Table 1. Biochemical characteristics were investigated as
described by Kämpfer et al. (1991). The results are given
in the species description. In addition, strain 119/4T was
tested by using the API 20NE system (bioMérieux)
according to the instructions of the manufacturer. These
results are given in comparison with the results of other
species of the genus Gemmobacter in Table 1.
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Table 1. Characteristics that differentiate strain 119/4T from members of the genus Gemmobacter
Strains: 1, 119/4T; 2, G. tilapiae Ruye-53T; 3, G. aquatilis DSM 3857T; 4, G. fontiphilus JS43T; 5, G. changlensis JA139T; 6, G. caeni DCA-1T; 7, G. nectariphilus AST4T (5DSM 15620T); 8, G. aquaticus
A1-9T; 9, G. nanjingensis Y12T. Data for the reference type strains are from Sheu et al. (2013a). All strains are Gram-reaction-negative, mesophilic, non-spore-forming, and positive for oxidase and
catalase. All strains are negative for DNase, urease, arginine dihydrolase, trypsin, a-galactosidase and b-glucuronidase activities, glucose acidification, assimilation of caprate, adipate and
phenylacetate, and hydrolysis of starch, gelatin and Tweens 40 and 80.
Characteristic
2
3
White to beige Creamy white
2
2
2
2
2
2
0–1.0 (0)
0–1.0 (0)
Colourless
2
2
+
0–2.0 (0)
4
Light yellow
2
2
+
0–0.5 (0)
7–10 (7–8)
6–9 (8–9)
6–7 (6)
7–10 (7–8)
15–45 (20–30) 10–37 (20–25) 10–40 (20–30) 10–30 (25)
5
6
7
Yellowish brown Pale yellow White to beige
2
2
2
+
2
2
+
2
2
0–6.0 (0–1.0) 0–5.0 (0–3.0) 0–2.0 (1.0)
6–9 (6–7)
10–37 (30)
4–8 (4–6)
6–8 (7–8)
15–40 (30–35) 15–40 (30)
8
9
Transparent
+
2
2
0–1.0 (0–0.5)
White to beige
2
2
+
0–5.0 (0)
4–10 (7–8)
20–30 (25–30)
7–9 (7)
10–40 (20–25)
2
2
2
2
+
+
+
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
+
2
+
2
2
+
2
2
2
2
2
+
+
+
2
+
2
2
2
+
+
2
2
2
2
2
+
2
+
2
+
2
2
+
2
+
2
2
2
2
+
2
2
2
+
+
+
+
+
+
+
+
2
2
+
2
+
2
+
2
+
2
+
2
+
2
2
+
+
+
+
+
+
2
+
+
2
2
2
2
2
2
2
+
2
+
2
2
+
2
2
2
2
2
2
2
2
2
2
2
2
2
2
+
2
+
+
+
+
2
2
2
+
+
+
+
+
+
+
+
2
+
+
+
+
2
+
+
+
+
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
+
2
+
+
+
+
2
+
2
779
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Gemmobacter intermedius sp. nov.
Colony pigmentation
Motility
Photoheterotrophic growth
Facultatively anaerobic growth
NaCl range for growth (%, w/v)
(optimum)
pH range for growth (optimum)
Temperature range for growth (uC)
(optimum)
Nitrate reduction
Indole production
Hydrolysis of:
Aesculin
Skimmed milk
Corn oil
Tween 20
Tween 60
Enzyme activities:
Alkaline phosphatase
b-Galactosidase
a-Glucosidase
b-Glucosidase
Assimilation of:
Glucose
Arabinose
Mannose
Mannitol
N-Acetyl-D-glucosamine
Maltose
Gluconate
Malate
Citrate
1
P. Kämpfer and others
For 16S rRNA gene-based phylogenetic analysis, the nearly
full-length 16S rRNA gene of strain 119/4T was PCRamplified and sequenced with the Sanger method using
universal primers 27F and 1492R (Lane, 1991). Phylogenetic analysis was performed using the software tool ARB
release 5.2 (Ludwig et al., 2004) and the ‘All-Species Living
Tree’ project (LTP; Yarza et al., 2008) database release
LTPs115 (March 2014). Sequences not included in the
database were aligned with the SILVA Incremental Aligner
(SINA; version 1.2.11; Pruesse et al., 2012) according to
the SILVA seed alignment and imported into the LTP
database. The alignment of sequences included in the
phylogenetic analysis was controlled manually including
secondary structure information. Sequence similarities
were calculated without evolutionary substitution models
using the ARB neighbour-joining tool. Phylogenetic trees
were reconstructed with the maximum-likelihood method
using RAxML version 7.04 (Stamatakis, 2006) with GTRGAMMA and rapid bootstrap analysis and the maximumparsimony method using PhyML with 100 bootstraps.
First phylogenetic placement was performed using 276 type
strains of the Rhodobacterales. Based on the obtained
phylogenetic resolution, further trees were reconstructed
including 24 type strains of the closest related genera.
Analyses were based on 16S rRNA gene sequences between
Escherichia coli positions 60 and 1466 (E. coli numbering
according to Brosius et al., 1978).
The sequenced fragment of the 16S rRNA gene of strain
119/4T represents a continuous stretch of 1344 bp spanning
E. coli positions 49–1471. Phylogenetic analysis placed
strain 119/4T in the family Rhodobacteraceae, clustering as
an outlier species to the genus Gemmobacter not supported
by high bootstrap values (Fig. 1). Highest sequence similarities were obtained with the type strains of G. tilapiae
(94.9 %) and G. nectariphilus (94.6 %), but also with those of
Rhodobacter viridis (94.8 %), Rhodobacter veldkampii (94.6 %)
and Paenirhodobacter enshiensis (94.6 %), although the latter
group were more distant in phylogenetic trees including all
Rhodobacteraceae (data not shown).
For analysis of polyamines, respiratory quinones and
polar lipids, strain 119/4T was grown on 3.3xPYE medium
(1.0 % w/v peptone from casein, 1.0 % (w/v) yeast extract,
pH 7.2). For polyamine analysis, cells were harvested at the
late exponential growth phase and polyamines were
extracted as described by Busse & Auling (1988). HPLC
analysis was carried out as described by Busse et al. (1997)
applying the equipment reported by Stolz et al. (2007).
Major polyamines were putrescine [29.7 mmol (g dry
weight)21] and spermidine [17.0 mmol (g dry weight)21].
Minor amounts of cadaverine [0.1 mmol (g dry weight)21]
and spermine [1.0 mmol (g dry weight)21] were detected as
well. This polyamine pattern closely matches those of other
members of the family Rhodobacteraceae, including species
of the genera Catellibacterium, Jannaschia, Paracoccus,
Pelagibaca, Pseudorhodobacter, Pseudovibrio, Rhodobacter,
Rhodovulum, Roseibium, Roseibacterium, Roseovarius and
Yangia (Busse & Auling, 1988; Hamana & Matsuzaki, 1990;
Hamana & Takeuchi, 1998; Hamana et al., 2003, 2006).
However, representatives of the genera Roseobacter and
Pseudovibrio were reported to contain only a single major
polyamine, namely spermidine (Hamana & Takeuchi,
1998). Quinones and polar lipids were extracted from
biomass harvested at the stationary growth phase and
analysed applying the integrated procedure reported by
Tindall (1990a, b) and Altenburger et al. (1996). The
quinone system was composed exclusively of ubiquinones
(98.7 % Q-10, 0.8 % Q-9, 0.4 % Q-11 and 0.1 % Q-8). The
presence of Q-10 is widespread among members of the
Alphaproteobacteria, including the genus Gemmobacter
(Chen et al., 2013). The polar lipid profile was composed
100 Gemmobacter caeni DCA-1T (FJ386516)
** Gemmobacter nanjingensis Y12T (EU289803)
84
100 * Gemmobacter lanyuensis Orc-4T (JN104393)
* Gemmobacter aquaticus A1-9T (EU313813)
99 72* Gemmobacter fontiphilus JS43T (FJ906694)
88 **Gemmobacter aquatilis DSM 3857T (FR733676)
76 * *
Gemmobacter changlensis JA139T (AM399030)
Gemmobacter tilapiae Ruye-53T (HQ111526)
Gemmobacter nectariphilus AST4T (AB101543)
* Gemmobacter megaterium CF17T (JN620361)
98
Gemmobacter intermedius 119/4T (KM407667)
100 Haematobacter massiliensis FramboiseT (AF452106)
** Haematobacter missouriensis CCUG 52307T (DQ342315)
* 97
Rhodobacter blasticus ATCC 33485T (DQ342322)
** Tabrizicola aquatica RCRI19T (HQ392507)
Pseudorhodobacter wandonensis WT-MW11T (JN247434)
79
Pseudorhodobacter antarcticus ZS3-33T (FJ196030)
97
Pseudorhodobacter ferrugineus IAM 12616T (D88522)
Pseudorhodobacter aquimaris HDW-19T (GU086365)
Rhodobacter sphaeroides 2.4.1T (X53853)
88 Rhodobacter megalophilus JA194T (AM421024)
Rhodobacter johrii JA192T (AM398152)
100
Rhodobacter azotoformans KA25T (D70846)
** Falsirhodobacter halotolerans JA744T (HE662814)
100
4
Amaricoccus
0.10
780
Fig. 1. Maximum-likelihood tree based on 16S
rRNA gene sequences showing the phylogenetic relationship of strain 119/4T among
closest related species of the family
Rhodobacteraceae including all species of
the genus Gemmobacter. The tree was generated in ARB using RAxML (GTR-GAMMA,
rapid bootstrap analysis, 100 bootstraps).
Only bootstrap values .70 % are depicted.
The calculations are based on 16S rRNA gene
sequences between E. coli positions 49 and
1471 (E. coli numbering according to Brosius
et al., 1978). Nodes marked with asterisks
were also obtained by the maximum-parsimony
analysis, where two asterisks indicate nodes
that also had a high bootstrap value in the
maximum-parsimony tree. Type strains of the
genus Amaricoccus were used as the outgroup. Bar, 0.1 substitutions per site.
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Gemmobacter intermedius sp. nov.
of the major lipids diphosphatidylglycerol, phosphatidylethanolamine, phoshatidylglycerol and phosphatidylcholine and
moderate to minor amounts of phosphatidylmonomethylethanolamine, three unidentified aminolipids and five
lipids not containing an amino, a phosphate or a sugar
residue (Fig. 2). This polar lipid profile includes the
characteristics listed in the emended description of the
genus Gemmobacter but the presence of diphosphatidylglycerol distinguishes strain 119/4T from the majority of species
of the genus Gemmobacter (Chen et al., 2013). It also
contains several components reported to be present in
G. megaterium (Liu et al., 2014), G. tilapiae (Sheu et al.,
2013a) and G. lanyuensis (Sheu et al., 2013b), including
phosphatidylethanolamine, phosphatidylglycerol and phosphatidylcholine, but the presence of diphosphatidylglycerol
and two unidentified aminolipids (AL2, AL3) distinguishes
strain 119/4T from the latter three species. Additionally,
the absence of any glycolipid present in G. megaterium
distinguishes the novel strain from this species.
Fatty acid methyl esters were obtained from cells cultivated on R2A agar for 48 h at 28 uC by saponification,
methylation and extraction as described by Kämpfer &
Kroppenstedt (1996) and separated using a gas chromatograph (model 5898A; Hewlett Packard). Peaks were automatically integrated and fatty acid names and percentages
were determined using the Microbial Identification standard software package MIDI. The fatty acid profile of strain
L1
DPG
L2
L3
PME
AL1
PE
PG
2nd dimension
PC
↑
AL3
AL2
L4
L5
→ 1st dimension
Fig. 2. Polar lipid profile of strain 119/4T after two-dimensional TLC
and detection with molybdatophosphoric acid. PE, phosphatidylethanolamine; PME, phosphatidylmonomethylethanolamine; PG,
phosphatidylglycerol; DPG, diphosphatidylglycerol; PC, phosphatidylcholine; AL1–3, unidentified aminolipids; L1–5, unidentified
lipids.
http://ijs.sgmjournals.org
119/4T was characterized by a large amount of unsaturated
(C18 : 1v7c) fatty acids. In addition, minor amounts of C16 : 0
and small amounts of the hydroxylated fatty acid C10 : 0
3-OH were detected. Strain 119/4T contained C17 : 0 in
moderate amounts, a component not found in other species
of the genus Gemmobacter. The detailed fatty acid pattern is
given in Table 2.
The genomic DNA G+C content of strain 119/4T was
determined as described previously (Glaeser et al., 2013)
based on the DNA melting temperature methods established
by Gonzalez & Saiz-Jimenez (2002) and was 64 mol%. This
value is close to the G+C content determined for the type
species of the genus Gemmobacter, G. aquatilis (63 mol%;
Rothe et al., 1987) and in the range given for all species of the
genus Gemmobacter (62.5–69.4 mol%; Chen et al., 2013).
Despite problems with phylogenetic allocation, the present
data demonstrate that strain 119/4T exhibits traits that
are typical characteristics of the genus Gemmobacter.
Therefore, we suggest that strain 119/4T represents a novel
species of the genus Gemmobacter, for which the name
Gemmobacter intermedius sp. nov. is proposed.
Description of Gemmobacter intermedius
sp. nov.
Gemmobacter intermedius (in.ter.me9di.us. L. masc. adj.
intermedius in the middle, referring to the fact that the
species is grouped between Gemmobacter and Rhodobacter
and Roseinatronobacter and Roseibaca on the basis of 16S
rRNA gene sequence similarities).
Cells are Gram-stain-negative, non-motile, aerobic, nonspore-forming irregular rods, 1.0–1.2 mm in width and 2.0–
5.0 mm in length. Some cells are irregularly rod-shaped.
Growth is visible after 24 h of incubation on TSA at 37 uC.
Colonies on nutrient agar are cream-coloured, circular
with spreading edge. Good growth occurs on TSA and
yeast extract agar. Growth occurs at 15–55 uC (optimum,
37–45 uC), but not at 10 or 60 uC. Growth occurs at
pH 5.0–10.0 (optimum, pH 8.0) and in the presence of 1–
4 % (w/v) NaCl (optimum, 1–2 %). The fatty acid profile is
characterized by a large amount of unsaturated (C18 : 1v7c)
fatty acids. Minor amounts of C16 : 0 and low amounts of
the hydroxylated fatty acid C10 : 0 3-OH are present. The
polyamine profile contains major amounts of putrescine
and spermidine. The quinone system is ubiquinone Q-10.
Major polar lipids are diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine and phosphatidylcholine. Additionally, several unidentified lipids are
present, including three unidentified aminolipids and five
polar lipids not containing an amino residue, a phosphate
group or a sugar moiety. Oxidase- and catalase-positive.
Utilizes only a few compounds, among them DL-lactate and
L-malate. The following compounds are not utilized as sole
source of carbon: acetate, propionate, N-acetyl-D-glucosamine, N-acetylgalactosamine, L-arabinose, arbutin, cellobiose, gluconate, glycerol, maltose, D-mannitol, maltitol,
a-melibiose, L-rhamnose, D-ribose, sucrose, salicin, D-xylose,
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781
P. Kämpfer and others
Table 2. Fatty acid compositions of strain 119/4T and reference strains of the genus Gemmobacter
Strains: 1, 119/4T; 2, G. tilapiae Ruye-53T; 3, G. aquatilis DSM 3857T; 4, G. fontiphilus JS43T; 5, G. changlensis JA139T; 6, G. caeni DCA-1T; 7, G.
nectariphilus DSM 15620T; 8, G. aquaticus A1-9T; 9, G. nanjingensis Y12T. Data for the reference type strains are from Sheu et al. (2013a). Methods
of extraction and analyses were exactly the same. Values are percentages of the total fatty acids. TR, Trace amount (,1 %); 2, not detected; ECL,
equivalent chain-length.
Fatty acid
C16 : 0
C17 : 0
C18 : 0
C10 : 0 3-OH
C18 : 0 3-OH
C16 : 1v7c/iso-C15 : 0 2-OH*
C18 : 1v9c
C18 : 1v7c
11-Methyl C18 : 1v7c
Unknown ECL 11.799
1
2
3
4
5
6
7
8
9
3.0
3.7
–
3.1
–
6.6
–
80.9
–
2.8
3.3
2
4.0
2.5
3.8
–
–
73.4
7.7
–
2.5
–
2.5
3.3
1.0
5.8
–
74.0
5.3
–
1.7
–
3.8
3.0
2.4
1.0
1.1
76.7
5.0
–
1.5
–
4.3
3.0
–
5.9
–
73.6
3.0
–
3.2
–
4.6
2.4
1.9
1.0
–
82.4
–
–
1.6
–
8.2
2.9
1.2
–
1.6
74.3
3.5
–
2.0
–
5.7
3.9
1.3
–
2.5
70.3
4.6
–
1.2
–
2.2
3.1
–
1.3
–
81.2
2.7
–
*C16 : 1v7c/C16 : 1v6c in Sheu et al. (2013a).
adonitol, i-inositol, D-sorbitol, putrescine, cis-aconitic
acid, trans-aconitic acid, 4-aminobutyrate, adipate, azelate,
fumarate, glutarate, DL-3-hydroxybutyrate, itaconate, 2oxoglutarate, pyruvate, suberate, citrate, mesaconate, Lalanine, b-alanine, L-ornithine, L-phenylalanine, L-serine,
L-aspartate, L-histidine, L-leucine, L-proline, L-tryptophan,
3-hydroxybenzoate, 4-hydroxybenzoate and phenylacetate.
The chromogenic substrates bis-p-nitrophenyl-phosphate,
bis-p-nitrophenyl-phenyl-phosphonate and bis-p-nitrophenylphosphoryl-choline (weakly) are hydrolysed. The substrates
p-nitrophenyl-a-D-glucopyranoside, p-nitrophenyl-b-D-galactopyranoside, p-nitrophenyl-b-D-xylopyranoside, p-nitrophenyl-b-D-glucopyranoside, p-nitrophenyl-b-D-glucuronide,
2-deoxythymidine-29-p-nitrophenyl-phosphate, L-alanine-pnitroanilide, c-L-glutamate-p-nitroanilide and L-proline-pnitroanilide are not hydrolysed.
The type strain, 119/4T (5CIP 110795T5LMG 28215T5
CCM 8510T), was isolated from a choana swab of a white
stork nestling sampled in Poland. The G+C content of the
genomic DNA of the type strain is 64 mol%.
Brosius, J., Palmer, M. L., Kennedy, P. J. & Noller, H. F. (1978).
Complete nucleotide sequence of a 16S ribosomal RNA gene from
Escherichia coli. Proc Natl Acad Sci U S A 75, 4801–4805.
Busse, H.-J. & Auling, G. (1988). Polyamine pattern as a chemotaxo-
nomic marker within the Proteobacteria. Syst Appl Microbiol 11, 1–8.
Busse, H. J., Bunka, S., Hensel, A. & Lubitz, W. (1997). Discrimination
of members of the family Pasteurellaceae based on polyamine patterns.
Int J Syst Bacteriol 47, 698–708.
Chen, W. M., Cho, N. T., Huang, W. C., Young, C. C. & Sheu, S. Y.
(2013). Description of Gemmobacter fontiphilus sp. nov., isolated
from a freshwater spring, reclassification of Catellibacterium nectariphilum as Gemmobacter nectariphilus comb. nov., Catellibacterium
changlense as Gemmobacter changlensis comb. nov., Catellibacterium
aquatile as Gemmobacter aquaticus nom. nov., Catellibacterium caeni
as Gemmobacter caeni comb. nov., Catellibacterium nanjingense as
Gemmobacter nanjingensis comb. nov., and emended description of
the genus Gemmobacter and of Gemmobacter aquatilis. Int J Syst Evol
Microbiol 63, 470–478.
Gerhardt, P., Murray, R. G. E., Wood, W. A. & Krieg, N. R. (editors)
(1994). Methods for General and Molecular Bacteriology. Washington,
DC: American Society for Microbiology.
Glaeser, S. P., Galatis, H., Martin, K. & Kämpfer, P. (2013). Niabella
hirudinis and Niabella drilacis sp. nov., isolated from the medicinal
leech Hirudo verbana. Int J Syst Evol Microbiol 63, 3487–3493.
Acknowledgements
Gonzalez, J. M. & Saiz-Jimenez, C. (2002). A fluorimetric method for
We thank Drs Marcin Bochenski and Mariusz Kasprzak for sample
drawing. We also thank Evelyn Skiebe, Gundula Will, Katja Grebing
and Maria Sowinsky for excellent technical assistance.
the estimation of G+C mol% content in microorganisms by thermal
denaturation temperature. Environ Microbiol 4, 770–773.
Hamana, K. & Matsuzaki, S. (1990). Polyamines and their
biosynthetic activities in nonphytopathogenic marine agrobacteria.
Can J Microbiol 36, 567–572.
References
Hamana, K. & Takeuchi, M. (1998). Polyamine profiles as chemo-
painting. J Biotechnol 47, 39–52.
taxonomic marker within alpha, beta, gamma, delta and epsilon
subclasses of class Proteobacteria: distribution of 2-hydroxyputrescine
and homospermidine. Microbiol Cult Collect 14, 1–14.
Anil Kumar, P., Srinivas, T. N. R., Sasikala, Ch. & Ramana, Ch. V.
(2007). Rhodobacter changlensis sp. nov., a psychrotolerant, photo-
Hamana, K., Sakamoto, A., Tachiyanagi, S., Terauchi, E. & Takeuchi,
M. (2003). Polyamine profiles of some members of the alpha subclass
trophic alphaproteobacterium from the Himalayas of India. Int J Syst
Evol Microbiol 57, 2568–2571.
of the class Proteobacteria: polyamine analysis of twenty recently
described genera. Microbiol Cult Collect 19, 13–21.
Altenburger, P., Kämpfer, P., Makristathis, A., Lubitz, W. & Busse,
H.-J. (1996). Classification of bacteria isolated from a medieval wall
782
Downloaded from www.microbiologyresearch.org by
International Journal of Systematic and Evolutionary Microbiology 65
IP: 88.99.165.207
On: Fri, 16 Jun 2017 06:20:59
Gemmobacter intermedius sp. nov.
Hamana, K., Sato, W., Gouma, K., Yu, J., Ino, Y., Umemura, Y.,
Mochizuki, C., Takatsuka, K., Kigure, Y. & other authors (2006). Cellular
Sheu, S. Y., Sheu, D. S., Sheu, F. S. & Chen, W. M. (2013a).
Gemmobacter tilapiae sp. nov., a poly-b-hydroxybutyrate-accumulat-
polyamine catalogues of the five classes of the phylum Proteobacteria:
distributions of homospermidine within the class Alphaproteobacteria,
hydroxyputrescine within the class Betaproteobacteria, norspermidine
within the class Gammaproteobacteria, and spermidine within the classes
Deltaproteobacteria and Epsilonproteobacteria. Ann Gunma Health Sci 27,
1–16.
ing bacterium isolated from a freshwater pond. Int J Syst Evol
Microbiol 63, 1550–1556.
Kämpfer, P. & Kroppenstedt, R. M. (1996). Numerical analysis of
fatty acid patterns of coryneform bacteria and related taxa. Can J
Microbiol 42, 989–1005.
Kämpfer, P., Steiof, M. & Dott, W. (1991). Microbiological
characterization of a fuel-oil contaminated site including numerical
identification of heterotrophic water and soil bacteria. Microb Ecol 21,
227–251.
Lane, D. J. (1991). 16S/23S rRNA sequencing. In Nucleic Acid
Techniques in Bacterial Systematics, pp. 115–175. Edited by
E. Stackebrandt & M. Goodfellow. London: Wiley.
Liu, Y., Xu, C. J., Jiang, J. T., Liu, Y. H., Song, X. F., Li, H. & Liu, Z. P.
(2010). Catellibacterium aquatile sp. nov., isolated from fresh water,
and emended description of the genus Catellibacterium Tanaka et al.
2004. Int J Syst Evol Microbiol 60, 2027–2031.
Sheu, S.-Y., Shiau, Y.-W., Wei, Y.-T. & Chen, W.-M. (2013b).
Gemmobacter lanyuensis sp. nov., isolated from a freshwater spring.
Int J Syst Evol Microbiol 63, 4039–4045.
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based
phylogenetic analyses with thousands of taxa and mixed models.
Bioinformatics 22, 2688–2690.
Stolz, A., Busse, H.-J. & Kämpfer, P. (2007). Pseudomonas
knackmussii sp. nov. Int J Syst Evol Microbiol 57, 572–576.
Tanaka, Y., Hanada, S., Manome, A., Tsuchida, T., Kurane, R.,
Nakamura, K. & Kamagata, Y. (2004). Catellibacterium nectariphilum
gen. nov., sp. nov., which requires a diffusible compound from a
strain related to the genus Sphingomonas for vigorous growth. Int J
Syst Evol Microbiol 54, 955–959.
Tindall, B. J. (1990a). A comparative study of the lipid composition
of Halobacterium saccharovorum from various sources. Syst Appl
Microbiol 13, 128–130.
Liu, J.-J., Zhang, X. Q., Chi, F.-T., Pan, J., Sun, C. & Wu, M. (2014).
Tindall, B. J. (1990b). Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66, 199–202.
Gemmobacter megaterium sp. nov., isolated from coastal planktonic
seaweeds. Int J Syst Evol Microbiol 64, 66–71.
Yarza, P., Richter, M., Peplies, J., Euzeby, J., Amann, R., Schleifer,
K. H., Ludwig, W., Glöckner, F. O. & Rosselló-Móra, R. (2008). The
Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H.,
Yadhukumar, Buchner, A., Lai, T., Steppi, S. & other authors
(2004). ARB: a software environment for sequence data. Nucleic Acids
All-Species Living Tree project: a 16S rRNA-based phylogenetic tree
of all sequenced type strains. Syst Appl Microbiol 31, 241–250.
Res 32, 1363–1371.
Zhang, J., Chen, S. A., Zheng, J. W., Cai, S., Hang, B. J., He, J. & Li, S. P.
(2012). Catellibacterium nanjingense sp. nov., a propanil-degrading
Pruesse, E., Peplies, J. & Glöckner, F. O. (2012). SINA: accurate
bacterium isolated from activated sludge, and emended description of
the genus Catellibacterium. Int J Syst Evol Microbiol 62, 495–499.
high-throughput multiple sequence alignment of ribosomal RNA
genes. Bioinformatics 28, 1823–1829.
Rothe, B., Fischer, A., Hirsch, P., Sittig, M. & Stackebrandt, E. (1987).
Zheng, J. W., Chen, Y. G., Zhang, J., Ni, Y. Y., Li, W. J., He, J. & Li, S. P.
(2011). Description of Catellibacterium caeni sp. nov., reclassification
The phylogenetic position of the budding bacteria Blastobacter aggregatus
and Gemmobacter aquatilis gen. nov., sp. nov. Arch Microbiol 147, 92–
99.
of Rhodobacter changlensis Anil Kumar et al. 2007 as Catellibacterium
changlense comb. nov. and emended description of the genus
Catellibacterium. Int J Syst Evol Microbiol 61, 1921–1926.
http://ijs.sgmjournals.org
Downloaded from www.microbiologyresearch.org by
IP: 88.99.165.207
On: Fri, 16 Jun 2017 06:20:59
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