Archives of Microbiology (2020) 202:2655–2661

https://doi.org/10.1007/s00203-020-01988-8

ORIGINAL PAPER

Aureimonas fodinaquatilis sp. nov., isolated from coal mine wastewater

Jihye Baek1 · Jong‑Hwa Kim1 · Jung‑Sook Lee2 · Ampaitip Sukhoom3 · Wonyong Kim1 

Received: 4 March 2020 / Revised: 9 July 2020 / Accepted: 14 July 2020 / Published online: 26 July 2020
© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract
A Gram stain-negative, aerobic, non-motile, short, rod-shaped bacterial strain CAU 1­ 482T was isolated from coal mine
wastewater in Hongcheon, Korea. It grew well at 30 °C, pH 8.5, 2% NaCl (w/v). 16S rRNA-based phylogeny indicated that
CAU ­1482T forms a distinct lineage within Aureimonas with high similarity to Aureimonas frigidaquae ­CW5T (98.2%),
Aureimonas altamirensis ­S21BT (98.0%), and Aureimonas glaciei B5-2T (96.3%). The predominant cellular fatty acids were
­C18:1 2-OH, C ­ 16:0, ­C18:1 ω7c, and/or C
­ 18:1 ω6c (summed feature 8), with Q-10 as the major isoprenoid quinone. The polar
lipid profile comprised diphosphatidylglycerol, phosphatidylglycerol, phosphatidylethanolamine, phosphatidylcholine, two
unidentified aminolipids, and three unidentified lipids. The 3.9-Mb genome included 8 contigs and 3599 protein-coding genes
with a 56.7 mol% G + C content. Average nucleotide identity (ANI) and digital DNA–DNA hybridization (dDDH) values
between strain CAU ­1482T and closely related strains of A. frigidaquae ­CW5T and A. altamirensis ­S21BT were 72.2‒72.4%
and 18.7‒18.8%, respectively. These phenotypic, chemotaxonomic, and phylogenetic data support CAU 1­ 482T as a novel
Aureimonas species, for which the name Aureimonas fodinaquatilis sp. nov. is proposed. The type strain is CAU ­1482T
(=  KCTC ­62995T = NBRC ­113692T).

Keywords  Aureimonas fodinaquatilis · Aurantimonadaceae · Coal mine · Wastewater · Genome · 16S rRNA · Novel
species

Introduction Aureimonas frigidaquae. At the time of writing, the genus

currently comprises 14 species with validly published names
The genus Aureimonas in the family Aurantimonadaceae (https​://www.lpsn.dsmz.de/genus​/aurei​monas​), which have
was proposed by Rathsack et  al. (2011). Aurantimonas been isolated from various sources, including a water-cool-
altamirensis, Aurantimonas ureilytica and Aurantimonas ing system (Kim et al. 2008; Rathsack et al. 2011), Altamira
frigidaquae of the genus Aurantimonas were transferred Cave (Jurado et al. 2006; Rathsack et al. 2011), a rusty iron
as Aureimonas altamirensis, Aureimonas ureilytica and plate (Lin et al. 2013), an air (Weon et al. 2007; Rathsack
et al. 2011), plants (Madhaiyan et al. 2013; Aydogan et al.
2016; Li et al. 2017, 2018), an ice core (Guo et al. 2017),
Communicated by Erko Stackebrandt. and a pond (Cho et al. 2015). In the course of investigating
novel bacteria, strain CAU ­1482T was isolated from a coal
Electronic supplementary material  The online version of this mine wastewater sample collected in the Republic of Korea,
article (https​://doi.org/10.1007/s0020​3-020-01988​-8) contains
supplementary material, which is available to authorized users. and was identified as a novel bacterium based on its unique
taxonomic position using a polyphasic approach, including
* Wonyong Kim the determination of phenotypic, genomic, and chemotaxo-
kimwy@cau.ac.kr nomic characteristics.
1
Department of Microbiology, Chung-Ang University College
of Medicine, Seoul, Republic of Korea
2
Korean Collection for Type Cultures, Korea Research
Institute of Bioscience and Biotechnology, Jeongeup,
Republic of Korea
3
Department of Microbiology, Faculty of Science, Prince
of Songkla University, Songkhla, Thailand

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Materials and methods
Bacterial isolation
A coal mine sewage sample was collected from
Hongcheon, Gangwon-do (37° 39′ 29.0″ N 127° 34′ 50.6″
E) in the Republic of Korea as described by Kim et al.
(2019). 100-µl aliquots of serial dilutions of the sewage
sample was spread on marine agar (MA) 2216 plates (BD
Difco, Sparks, MD, USA) under aerobic conditions at
30 °C for 7 days. Strain CAU ­1482T was one of the iso-
lates that appeared on MA. Pure cultures were preserved
in marine broth (MB) 2216 (BD Difco) supplemented with
25% (v/v) glycerol stocks at − 70 °C.
Physiological, morphological, and biochemical
characterization
Direct comparative analyses of the new strain were per-
formed with reference to A. frigidaquae KCTC ­12893T, A.
altamirensis KCTC ­22106T, and A. glaciei KCTC ­52395T
from the Korean Collection for Type Cultures (Jeongeup,
Korea). The reference strains were cultivated under the
same conditions for morphological, physiological, and bio-
chemical characteristic analysis. For morphological analy-
sis, cell morphology was examined under a DM 1000 light
microscope (Leica, Wetzlar, Germany) using cells grown
on MA at 30 °C for 2 days. Gram staining was performed
using a Gram staining kit (bioMérieux, Craponne, France).
The presence of flagella was observed under a JEM 1010
transmission electron microscope (JEOL, Tokyo, Japan)
using cells growing at the exponential phase. Motility was
investigated by stabbing material from strain CAU 1­ 482T
into a semisolid agar tube (Wolfe and Berg 1989). Colo-
nies were observed for detection of morphological features
such as appearance, pigmentation, size, shape, and texture
on MA plates incubated at 30 °C.
To determine the optimum growth conditions, strain
CAU ­1482T growing in MB was incubated at various tem-
peratures (4, 10, 20, 30, 37, and 45 °C), pH (4.5, 5.0, 5.5,
6.0, 6.5, 7.0, 7.5, 8.0, 8.5, 9.0, 9.5, 10.0, 10.5, 11.0, and
11.5; adjusted with 1 M HCl or 1 M NaOH), and NaCl
concentrations (0, 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14,
and 15%, w/v), and the turbidity of the broth was measured
after 48 h.
Catalase activity was tested by bubble production in
3% (v/v) H ­ 2O2 solution. Oxidase activity was tested by
the oxidation of 1% (w/v) tetramethyl-p-phenylenediamine
(Cappuccino and Sherman 2010). Hydrolysis of casein,
starch, gelatine, and urease, and reduction of nitrate were
examined according to the protocol of Smibert and Krieg
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Archives of Microbiology (2020) 202:2655–2661
(1994). Biochemical properties and enzyme activities were
determined using API 50CH, API 20E, API 20NE, and
API ZYM kits (bioMérieux). The values on the API 50CH,
API 20E, and API 20NE systems were read after incuba-
tion for 48 h at 30 °C, whereas those obtained on the API
ZYM system were read after incubation for 24 h at 37 °C.
16S rRNA gene sequence analysis
Genomic DNA extraction of strain CAU 1­ 482T was per-
formed using a genomic DNA extraction kit (iNtRON,
Seongnam, Korea). Fragments of the 16S rRNA gene were
amplified by polymerase chain reaction as described pre-
viously (Nam et  al. 2004), and the sequence was deter-
mined using the BigDye Terminator Cycle Sequencing Kit
(Applied Biosystems, Foster City, CA, USA) and the 3730
automatic DNA sequencer (Applied Biosystems). The 16S
rRNA gene sequence of strain CAU ­1482T was directly com-
pared with sequences obtained from the GenBank database.
Multiple alignments and calculation of 16S rRNA gene
sequence similarity between strain CAU ­1482T and the most
closely related strains were performed using EzTaxon-e—
EzBioCloud.net (https​://www.ezbio​cloud​.net/eztax​on) and
CLUSTAL_X 2.1 software (Larkin et al. 2007). A phy-
logenetic tree was constructed using algorithms from the
PHYLIP 3.66 package (Felsenstein 1989), including neigh-
bour-joining (Saitou and Nei 1987), maximum-likelihood
(Felsenstein 1981), and maximum-parsimony (Fitch 1971)
approaches for distance analysis. Evolutionary distance
matrices were generated by the neighbour-joining method
described by Jukes and Cantor (1969). Branch support in
the neighbour-joining tree was estimated by the bootstrap
resampling method with 1000 replicates (Felsenstein 1985).
Whole‑genome sequence analysis
The genomic DNA of strain CAU ­1482T was extracted using
TruSeq DNA PCR-Free kit (Illumina, San Diego, CA, USA)
and sequenced using an Illumina Hiseq sequencer by Macro-
gen (Seoul, Korea). De novo assembly of the sequence data
was performed with SPAdes version 3.13.0 (https​://www.
cab.spbu.ru/softwa​ re/spades​ ). K-mer analysis was performed
with Jellyfish (version 2.2.3) (https:​ //www.genome​ .umd.edu/
jellyfi
​ sh.html) and GenomeScope (https:​ //qb.cshl.edu/genom​
escop​e). The G + C content was calculated based on the
whole-genome sequence of CAU ­1482T. Average nucleotide
identity (OrthoANI) and the digital DNA–DNA hybrid val-
ues were calculated using the ANI calculator (https​://www.
ezbio​cloud​.net/tools​/ani) and Genome-to-Genome Distance
Calculator (https​://www.ggdc.dsmz.de/ggdc.php). Annota-
tion of the genome with predicted functional genes was per-
formed by Rapid Annotation using Subsystem Technology
(Aziz et al. 2008).
Archives of Microbiology (2020) 202:2655–2661 2657

Chemotaxonomic characterization
Respiratory quinones were extracted with chloroform/meth-
anol (2:1, v/v), evaporated under vacuum conditions, and
analysed by reverse-phase high-performance liquid chro-
matography as previously described (Hiraishi et al. 1996).
Polar lipids were extracted as described by Minnikin et al.
(1984) and separated by two-dimensional thin-layer chroma-
tography using chloroform: methanol: water (65:25:3.8, by
volume) for the first dimension and chloroform: methanol:
acetic acid: water (40:7.5:6:1.8, by volume) for the second
dimension as described by Embley and Wait (1994).
For cellular fatty acid analysis, strain CAU 1­ 482T and
reference strains were cultured under the same conditions
as described above, and then the biomass was harvested.
Fatty acids were saponified, methylated, and extracted using
standard Microbial Identification System (MIDI, version
6.1) methods. Cellular fatty acids were analysed by gas chro-
matography as described previously (Sasser 2006).
Results and discussion
Morphological, physiological, and biochemical
characteristics
Cells of strain CAU ­1482T were non-motile, rod-shaped
(Online Resource 1). The characteristics of strain CAU
­1482T demonstrating clear differences from the reference
strains of the genus Aureimonas are summarized in Table 1.

Table 1  Differential properties Characteristic 1 2 3 4

of strain CAU 1­ 482T and the
type strains of the most closely Temperature (°C)
related Aureimonas species
 Range 10–40 4–40 4–40 4–35
 Optimum 30 25–30 37 30
pH
 Range 5.5–9.0 6.5–10.0a 6.0–9.5b 5.0–8.0c
 Optimum 8.5 7.5–9.0a 7.0–9.0b 6.0c
NaCl (%, w/v)
 Range 0–7 0–9a 0–8b 0–8c
 Optimum 2 2 3 2
Enzyme activities
 Esterase lipase (C8) − + − −
 Trypsin − − + −
 Naphthol-AS-BI-phosphohydrolase + − + −
 β-Galactosidase + + − −
Assimilation
 Glucose fermentation − − + −
 d-Mannose − + + +
 d-Maltose − − + +
 l-Arabinose + − − −
 Potassium gluconate w + + +
 Malic acid − + + +
Acid production
 Erythritol − + + +
 d-Ribose − − + +
 l-Fucose +
DNA G + C content (mol %) 56.7 63.9a 71.8b 69.3c

+  positive, w weakly positive, − negative

Strains: 1, CAU ­1482T; 2, A. frigidaquae KCTC 1­ 2893T; 3, A. altamirensis KCTC 2­ 2106T; 4, A. glaciei
KCTC ­52395T. All data were obtained in the present study unless otherwise indicated. All strains were
positive for the hydrolysis of aesculin
a
 Kim et al. (2008)
b
 Jurado et al. (2006)
c
 Guo et al. (2017)

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Strain CAU ­148T differed from closely related species,
namely, A. frigidaquae ­CW5T, based on negative reactions
for d-mannitol, d-glucose, leucine arylamidase, and trypsin.
In addition, strain CAU 1­ 482T differed from A. frigidaq-
uae ­CW5T based on positive reactions for esterase (C4) and
lipase (C14). Based on the comparison of phenotypic char-
acteristics, strain CAU 1­ 482T could be distinguished from
recognized species of the genus Aureimonas. All negative
traits of commercial kits are given in Online Resource 4.
Phylogenetic and whole‑genome sequencing
characterization
The 16S rRNA gene sequence analysis revealed that strain
CAU ­1482T was a novel strain belonging to the genus Aurei-
monas with 98.2%, 98.0%, and 96.3% pairwise similarities
to A. frigidaquae ­CW5T, A. altamirensis ­S21BT, and A. gla-
ciei B5-2T, respectively. The neighbour-joining phylogenetic
tree (Fig. 1) indicated that strain CAU 1­ 482T clustered with
members of the genus Aureimonas.
The draft genome of strain CAU ­1482T comprises 8 con-
tigs (average length 492,122 bp) with a total genome size
of 3.9 Mb. The K-mer coverage was 165.4 × , and the N50
value was 1,264,131 bp. In the draft genome, 3599 protein-
coding genes with 3621 coding sequences, 3 rRNAs (5, 16,
and 23S), and 46 tRNAs were annotated. According to the
whole-genome sequence, the DNA G + C content of CAU
­1482T was 56.7 mol%, this value is lower than that of closely
related members of the genus Aureimonas (Table  1 and
Online Resource 5).
The detailed characteristics of the genome of members of
Aureimonas are summarized in Online Resource 2. RAST
analysis of strain CAU 1­ 482T showed the major categories
with a threshold of > 7%. Annotated gene functions included
“Amino Acids and Derivatives” (303 genes), “Carbohy-
drates” (245 genes), “Respiration” (100 genes), and “Cofac-
tors, Vitamins, Prosthetic Groups, Pigments” (133 genes).
The average nucleotide identity (OrthoANI) values of A.
frigidaquae ­CW5T and A. altamirensis ­S21BT were 72.4%
and 72.2%, respectively. The digital DNA–DNA hybridi-
zation values with closely related strains A. frigidaquae
­CW5T and A. altamirensis ­S21BT were 18.8% and 18.7%,
respectively, which are also significantly lower than the 70%
threshold (Goris et al. 2007).
Chemotaxonomic characterization
Comparison of the cellular fatty acids present in strain CAU
­1482T and other members of the genus Aureimonas is out-
lined in Table 2. The major fatty acids of strain CAU ­1482T
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Archives of Microbiology (2020) 202:2655–2661
were ­C18:1 2-OH, C­ 16:0 and C­ 18:1 ω7c, and/or C ­ 18:1 ω6c
(summed feature 8). Strain CAU ­1482T and A. altamirensis
­S21BT showed similar fatty acid profiles but did not con-
tain cyclo-C19:0 ω8c, ­C16:1 ω6c, and/or C­ 16:1 ω7c (summed
feature 3), which differed from the fatty acid profiles of A.
frigidaquae ­CW5T and A. glaciei B5-2T. The polar lipid
components included diphosphatidylglycerol, phosphatidyl-
glycerol, phosphatidylethanolamine, phosphatidylcholine,
two unidentified aminolipids, and three unidentified lipids
(Online Resource 3). The polar lipid profile of strain CAU
­1482T was similar to that of other species of the genus Aurei-
monas (Rathsack et al. 2011; Guo et al. 2017).
Taxonomic conclusion
The phylogenetic tree based on the 16S rRNA sequence indi-
cated that strain CAU 1­ 482T and A. frigidaquae ­CW5T and
A. altamirensis ­S21BT formed a separate branch with the
Aureimonas lineage. The phenetic inference was supported
by the combination of chemotaxonomic and biochemical
characteristics. Therefore, it can be concluded that strain
CAU ­1482T represents a novel species of the genus Aurei-
monas, for which the name Aureimonas fodinaquatilis sp.
nov. is proposed.
Description of Aureimonas fodinaquatilis sp. nov.
Aureimonas fodinaquatilis sp. nov. (fo.din.a.qua’ti.lis. L.
fem. n. fodina mine; L. masc. or fem. adj. aquatilis aquatic;
N.L. fem. adj. fodinaquatilis living in mine water).
Gram stain-negative, aerobic, short, and rod-shaped with
a size of approximately 0.7–0.9 µm in width and 0.8–1.9 µm
in length. Motility was not observed. Colonies are circular,
yellow-coloured, opaque, slightly convex, smooth, glisten-
ing, with entire margins and 0.8–1.0 mm in diameter on
MA after incubation at 30 °C for 24 h. Optimal growth
occurred at 37 °C and pH 8.5 with 2% (w/v) NaCl. Cata-
lase, gelatinase, urease, and protease activities are present,
but oxidase activity is absent. Acetoin production positive.
Enzyme activities are positive for alkaline phosphatase,
esterase (C4), leucine arylamidase, acid phosphatase, and
naphthol-AS-BI-phosphohydrolase. The strain can assimi-
late d-glucose, l-arabinose, d-mannitol, and potassium glu-
conate. The major polar lipids are diphosphatidylglycerol,
phosphatidylglycerol, phosphatidylethanolamine, phosphati-
dylcholine, two unidentified aminolipids, and three unidenti-
fied lipids. Q-10 is the predominant respiratory quinone, and
­C18:1 2-OH, ­C16:0 and C­ 18:1 ω7c, and/or ­C18:1 ω6c (summed
Archives of Microbiology (2020) 202:2655–2661 2659
Fig. 1  Neighbour-joining phylogenetic tree based on nearly complete
16S rRNA gene sequences showing the relationships between strain
CAU ­1482T and the type strains of reference Aureimonas species.
Dots indicate that the corresponding nodes were also recovered in the
trees created with the maximum-likelihood and maximum-parsimony
feature 8) are the major fatty acids. The DNA G + C con-
tent is 56.7 mol%. The type strain is CAU ­1482T (= KCTC
­62995T = NBRC ­113692T), which was isolated from coal
mine wastewater collected from Hongcheon, Gangwon-
do in the Republic of Korea. The GenBank/EMBL/DDBJ
algorithms (NJ/ML/MP). Bootstrap values (> 70%) are indicated
as percentages of 1000 resampled datasets of maximum-parsimony,
neighbour-joining, and maximum-parsimony analysis, respectively.
Bars represent 0.1 substitutions per nucleotide position. Escherichia
coli ­NCTC9001T (LN831047) was used as the outgroup strain
accession number for the 16S rRNA gene sequence of
Aureimonas fodinaquatilis CAU ­1482T is MH889112 and
the Whole Genome Shotgun project accession number is
VTWH00000000.
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Table 2  Cellular fatty acid compositions (%) of strain CAU 1­ 482T RAST Server: rapid annotations using subsystems technology.
and the type strains of the most closely related Aureimonas species BMC Genom 9:75
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Acknowledgements  This work was supported by a grant from 56:2583–2585
the National Institute of Biological Resources (NIBR), funded Kim MS, Hoa KTQ, Baik KS, Park SC, Seong CN (2008) Auranti-
by the Ministry of Environment (MOE) of the Republic of Korea monas frigidaquae sp. nov., isolated from a water-cooling sys-
(NIBR201902203), and the Chung-Ang University Research Grants tem. Int J Syst Evol Microbiol 58:1142–1146
in 2018. Kim JH, Kanjanasuntree R, Kim DH, Lee JS, Sukhoom A, Kanta-
chote D, Kim W (2019) Arenibacillus arenosus gen. nov., sp.
nov., a member of the family Rhodobacteraceae isolated from
Compliance with ethical standards  sea sand. Int J Syst Evol Microbiol 69:153–158
Larkin MA, Blackshields G, Brown NP, Chenn R, McGettigan PA,
Conflict of interest  The authors declare no competing interests. McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R,
Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and
Availability of data and material  The GenBank/EMBL/DDBJ acces- Clustal X version 2.0. Bioinformatics 23:2947–2948
sion number for the 16S rRNA gene sequence of Aureimonas fodina- Li FN, Tuo L, Pan Z, Guo M, Lee SMY, Chen L, Lin H, Sun CH
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project accession number is VTWH00000000. bacterium isolated from Aegiceras corniculatum. Int J Syst Evol
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Li Y, Xu G, Lin C, Wang X, Piao C (2018) Aureimonas populi sp.
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