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International Journal of Systematic and Evolutionary Microbiology (2014), 64, 3503–3507
DOI 10.1099/ijs.0.065003-0
Permianibacter aggregans gen. nov., sp. nov.,
a bacterium of the family Pseudomonadaceae
capable of aggregating potential biofuel-producing
microalgae
Hui Wang,1,2,3 Tianling Zheng,2 Russell T. Hill3 and Xiaoke Hu1
Correspondence
Xiaoke Hu
1
[email protected]
2
Yantai Institute of Costal Zone Research, Chinese Academy of Sciences, Yantai 264003,
PR China
Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, PR China
3
Institute of Marine and Environmental Technology, University of Maryland Center for Environmental
Science, Baltimore, MD 21202, USA
A novel bacterial strain, capable of aggregating potential biofuel-producing microalgae, was
isolated from the phycosphere of an algal culture and designated HW001T. The novel bacterial
strain was identified on the basis of its phylogenetic, genotypic, chemotaxonomic and phenotypic
characteristics in this study. Cells were aerobic, Gram-negative rods. 16S rRNA genebased phylogenetic analysis revealed that strain HW001T is affiliated with the family
Pseudomonadaceae in the phylum Proteobacteria, but forms a distinct clade within this family.
The DNA G+C content of strain HW001T was 55.4 mol%. The predominant cellular fatty acids
were iso-C15 : 0, summed feature 9 (iso-C17 : 1v9c), C16 : 0 and summed feature 3 (C16 : 1v7c/
C16 : 1v6c). Q-8 was the main respiratory quinone. The polar lipid profile contained
phosphatidylethanolamine, an unidentified aminophospholipid and some unidentified lipids. Based
on the extensive polyphasic analysis, strain HW001T represents a novel species of a new genus in
the family Pseudomonadaceae, for which the name Permianibacter aggregans gen. nov., sp. nov.,
is proposed. The type strain of the type species is HW001T (5CICC 10856T5KCTC 32485T).
The family Pseudomonadaceae comprises 12 different
genera at the time of writing, Azomonas, Azomonotrichon,
Azorhizophilus, Azotobacter, Chryseomonas, Cellvibrio,
Flavimonas, Mesophilobacter, Pseudomonas, Rhizobacter,
Rugamonas and Serpens (Parte, 2014; Rediers et al., 2004;
Skerman et al., 1980). Although the type genus Pseudomonas, and other two genera, Chryseomonas and Flavimonas, in this family are known as emerging opportunistic
pathogens (Carmeli et al., 1999; Holmes et al., 1987; Hugh
& Leifson, 1964), the family is well-acknowledged to
perform important functions in the rhizosphere by fixing
nitrogen in the atmosphere to ammonium which supports
and enhances plant growth. (De Smedt et al., 1980; Suarez
et al., 2014; Young & Park, 2007). Micro-organisms
performing this function are termed as plant growthpromoting rhizobacteria (PGPRs) (Vessey, 2003). Here, a
bacterial strain, affiliated into the family Pseudomonadaceae
and showing a distinct function is described. The strain,
designated HW001T was isolated from the phycosphere of
the potential biofuel-producing microalgae Nannochloropsis
oceanica IMET1 in a study investigating the diversity and
functions of the bacterial communities associated with this
microalga (Wang et al., 2012). Strain HW001T showed a
remarkable ability to aggregate N. oceanica IMET1, which
could be a novel approach to harvest biofuel-producing
microalgae. Results indicated that the strain originated
from the Permian groundwater, which was used for
cultivating N. oceanica IMET1. Polyphasic taxonomic tests
including phylogenetic, genotypic, chemotaxonomic and
phenotypic assays were performed to characterize the novel
strain in this study and indicated that strain HW001T
represents a novel species of a new genus in the family
Pseudomonadaceae.
Abbreviations: PE, phosphatidylethanolamine; UAPL, unidentified aminophospholipid.
Permian groundwater used for cultivating the microalga
was collected from the Pecos Cenozoic Trough in Imperial,
TX, USA (31u 169 16.930 N 102u 409 48.350 W). Photobioreactors (PBR) were constructed to investigate the diversity
and functions of bacteria in the phycosphere at different
temperatures (15, 25 and 30 uC). The functional bacterium
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene
sequence of strain HW001T is KJ721800.
Two supplementary figures and three supplementary tables are available
with the online version of this paper.
065003 G 2014 IUMS
Printed in Great Britain
3503
H. Wang and others
HW001T was successfully isolated on Difco marine agar
2216 plates (BD Bioscience) at 30 uC and cryopreserved at
280 uC in marine broth 2216 (BD Bioscience) supplemented with 30 % (v/v) glycerol. After 72 h incubation
on marine agar, the aerobic bacterium strain formed
circular, flat, yellow colonies. Gram staining was performed
according to the method described by Gerhardt et al.
(1994). Scanning electron microscopy (SEM) was used to
observe the morphology of strain HW001T. The results
indicated that strain HW001T was a Gram-stain-negative,
rod-shaped (0.461.6–2.7 mm) bacterium (Fig. S1, available in the online Supplementary Material).
Genomic DNA was extracted using an Ultra-Clean
microbial DNA isolation kit (MoBio Laboratories). PCR
amplification and 16S rRNA gene sequencing was performed as described previously (Enticknap et al., 2006).
The almost full-length 16S rRNA gene was analysed using
the EzTaxon-e server (Kim et al., 2012). 16S rRNA gene
sequences were aligned with representative members of
selected genera belonging to the family Pseudomonadaceae
in the phylum Proteobacteria. Phylogenetic analysis was
conducted using the MEGA 4 software package (Tamura
et al., 2007). A phylogenetic tree was reconstructed using
the neighbour-joining (Jukes–Cantor correction) algorithm. The robustness of the inferred tree topologies was
evaluated after 1000 bootstrap replicates of the neighbourjoining data.
The taxonomic analysis by using EzTaxon-e shows that
strain HW001T is only 88.31 % similar to any previously
identified type strain. The closest cultured bacterium was
Pseudomonas protegens CHA0T, affiliated into the genus
Pseudomonas in the family Pseudomonadaceae. Similarities
65
0.01
of strain HW001T with the type species of each genus in the
family Pseudomonadaceae ranged from 82.99 % to 87.45 %
(Table S1). Phylogenetic analysis of strain HW001T and
all type strains in the family indicated that the novel
bacterium does not affiliate into any existing genus and
forms a distinct lineage in the family Pseudomonadaceae
(Fig. 1, Fig. S2).
Temperature, pH, and salinity suitable for the growth
of strain HW001T and the reference strain Pseudomonas
aeruginosa ATCC 10145T were tested according to previously described methods (Nedashkovskaya et al., 2004a; Yi
& Chun, 2004). Physiological and biochemical characterizations were conducted using API ZYM, API 50 CH,
API 20NE, API 20E and API 50CHB strips (bioMérieux),
while some media used for tests were prepared as previously
described (Yi et al., 2003). Sensitivity to antibiotics was
tested by adding antibiotic discs (Oxoid) onto marine agar
plates spread with fresh HW001T cultures. The antibiotics
and their minimum inhibitory concentration (MIC; mg
ml21) determined in this experiment were as follows:
kanamycin (0.5), ceftazidime (0.125), norfloxacin (,0.016),
tetracycline (0.38), nitrofurantoin (3), gentamicin (0.125)
and chloramphenicol (0.032). The effect of antibiotics on
the growth of cells was assessed after 48 h based on the
methods described as CLSI/NCCLS M100-S21 (CLSI, 2011).
The results of physiological and biochemical tests are given
in the species description and in Table 1 and Table S2.
Simultaneous tests of all parameters mentioned above were
conducted on the reference strain.
The DNA G+C content of strain HW001T was determined
by using the thermal denaturation method (Mandel &
Marmur, 1968). The results showed that the DNA G+C
Azorhizophilus paspali ATCC 23833T (AJ308318)
Pseudomonas aeruginosa ATCC 10145T (HE978271)
57
100 66
Azomonotrichon macrocytogenes ATCC 12335T (AB175654)
Azotobacter chroococcum ATCC 9043T (AB175653)
Serpens flexibilis ATCC 29606T (GU269546)
Azomonas agilis ATCC 7494T (AB175652)
99
Chryseomonas polytricha ATCC 43330T (D84003)
53
99
Flavimonas oryzihabitans ATCC 43272T (D84004)
Cellvibrio mixtus UQM 2601T (AF448515)
Permianibacter aggregans HW001T (KJ721800)
100
Rhizobacter dauci ATCC 43778T (AB297965)
Rugamonas rubra ATCC 43154T (HM038005)
Roseobacter litoralis ATCC 49566T (X78312)
Fig. 1. Rooted neighbour-joining tree of partial 16S rRNA gene sequences of strain HW001T and representative members of
selected genera belong to the family Pseudomonadaceae in the phylum Proteobacteria. The tree was reconstructed using MEGA
software. Roseobacter litoralis ATCC 49566T (GenBank accession no. X78312) was used as the outgroup. Numbers at nodes
are bootstrap values (%) based on 1000 replicates. Bar, 0.01 substitutions per nucleotide position.
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International Journal of Systematic and Evolutionary Microbiology 64
Permianibacter aggregans gen. nov., sp. nov.
Table 1. Differential characteristics of strain HW001T and reference strains in the family Pseudomonadaceae
Strains: 1, HW001T, 2, Pseudomonas aeruginosa ATCC 10145T (data from this study), 3, Azomonotrichon macrocytogenes ATCC 12335T (De Ley &
Park, 1966), 4, Cellvibrio mixtus UQM 2601T (Blackall et al., 1985), 5, Chryseomonas polytricha ATCC 43330T (Holmes et al., 1986), 6, Flavimonas
oryzihabitans ATCC 43272T (Holmes et al., 1987), 7, Mesophilobacter marinus IAM 13185T (Nishimura et al., 1989), 8, Rhizobacter dauci ATCC
43778T (Goto & Kuwata, 1988), 9, Rugamonas rubra ATCC 43154T (Austin & Moss, 1986), 10, Serpens flexibilis ATCC 29606T (Hespell, 1977). +,
Positive; 2, negative; NA, no data available.
Characteristic
pH range for growth
Salinity for growth (%, w/v)
Acid production from:
(2)-D-Arabinose
(2)-L-Xylose
(+)-L-Arabinose
D-Fructose
D-Mannose
(+)-Cellobiose
(+)-Maltose
Starch
Gluconate
Enzymic activities
Urease
Catalase
Oxidase
Hydrolysis of:
Maltose
Malic acid
Sodium citrate
Mannitol
1
2
3
4
5
6
7
8
9
10
6–10
2–8
5–10
0–6
5.2–6.9
Neutral and alkaline pH
5–10
NA
NA
NA
7.6
7–20
NA
NA
0–0.7
5–9
0–5
5.8–7.2
5.85
2
2
2
2
2
+
+
+
+
+
+
+
+
+
2
2
2
2
2
2
2
2
2
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
2
+
2
2
+
+
+
2
+
+
+
+
+
+
+
+
2
+
2
2
2
2
+
+
+
NA
NA
NA
2
2
NA
NA
2
+
+
2
2
2
+
+
2
2
2
NA
NA
content of the strain HW001T was 55.4 mol%. This value is
lower than those associated with members of the genus
Pseudomonas, which range from 58–70 mol% (Palleroni,
1984).
The Sherlock Microbial Identification System (MIDI) was
applied for measuring cellular fatty acids of strain HW001T
and the reference strain Pseudomonas aeruginosa ATCC
10145T. Strain HW001T and the reference strain were
cultured to late exponential phase in marine broth 2216 at
30 uC for 48 h and Luria broth (LB; Life Technologies)
at 37 uC for 48 h, respectively. The predominant cellular
fatty acids of strain HW001T were iso-C15 : 0 (29.15 %), isoC15 : 0, summed feature 9 (iso-C17 : 1v9c, 22.25 %), C16 : 0
(7.0 %) and summed feature 3 (C16 : 1v7c/C16 : 1v6c,
6.44 %) (Table S3), while the principal cellular fatty acids
for the reference strain were C16 : 0 (31.1 %) and C18 : 1v7c/
C18 : 1v6c (31.86 %). Quinone composition was characterized by HPLC as described previously (Nedashkovskaya
et al., 2004b). The main isoprenoid quinone of strain
HW001T was Q-8 (ca. 100 %) which was consistent with
type species of genera Rhizobacter and Mesophilobacter. Polar
lipids were determined using TLC following the method of
Minnikin et al. (1984): methanol/water (100 : 10, v/v) and
petroleum ether (b.p. 60–80 uC) extraction was applied
followed by chloroform/methanol/water (90 : 100 : 30, by
vol.) extraction, chloroform/methanol/water (50 : 100 : 40,
http://ijs.sgmjournals.org
NA
2
NA
2
2
NA
+
2
NA
+
+
+
2
2
+
2
2
2
+
2
NA
NA
NA
+
NA
+
+
NA
NA
NA
NA
+
2
+
+
NA
+
NA
+
+
+
+
+
+
+
+
NA
NA
NA
NA
NA
NA
+
+
+
+
+
2
+
+
NA
NA
2
2
by vol.) extraction twice, and chloroform/water (1 : 1,
v/v) extraction subsequently. Polar lipids were harvested
after evaporation of the lower layer with N2 (,37 uC).
Chromatography was conducted by using chloroform/
methanol/water (65 : 25 : 4, by vol.), followed by chloroform/acetic acid/methanol/water (40 : 7.5 : 6.2, by vol.).
Ethanolic molybdophosphoric acid (5 %) was applied to
detect the presence of all lipids. Ninhydrin (0.2 % in watersaturated butanol) was used for revealing the presence of
phospholipids. a-Naphthol/sulphuric acid was sprayed to
reveal the presence of glycolipids. The results indicated
that the polar lipid profile was composed of phosphatidylethanolamine (PE), an unidentified aminophospholipid
(UAPL), and some other unidentified lipids (Fig. 2).
However, diphosphatidylglycerol, phosphatidylglycerol and
phosphatidylcholine, three common polar lipids in the
genus Pseudomonas were not detected.
The great differences shown by phylogenetic, genotypic,
chemotaxonomic and phenotypic analyses distinguished
the novel bacterium HW001T from the closest reference
strain, Pseudomonas aeruginosa ATCC 10145T. Based
on polyphasic analysis in this taxonomic study, strain
HW001T represents a novel species of a new genus
affiliated with the family Pseudomonadaceae, for which
the name Permianibacter aggregans gen. nov., sp. nov. is
proposed.
3505
H. Wang and others
The type strain is HW001T (5CICC 10856T5KCTC
32485T), isolated from Permian ground water, from the
Pecos Cenozoic Trough in Imperial, TX, USA. The DNA
G+C content of the type strain is 55.4 mol%.
UL
UL
UAPL
Acknowledgements
UL
PE
UL
Fig. 2. Polar lipids of strain HW001T separated by twodimensional TLC and detected by spraying with molybdatophosphoric acid reagent. PE, Phosphatidylethanolamine; UAPL,
unidentified aminophospholipid; UL, unknown lipid.
We acknowledge the China Center of Industrial Culture Collection
for assistance in identifying the novel strain. Aidan Parte is thanked
for nomenclatural advice. Funding for this research was provided by
the Hundred Talents Program of Chinese Academy of Sciences
awarded to X. H., the Science and Technology Program of Shandong
Province (2013GHY11534) and the State Key Laboratory of Marine
Environmental Science (Xiamen University) visiting fellowship
(MELRS1211). The Permian groundwater was kindly provided by
Bart Reid, Organic Aquaculture Institute, Imperial, TX, USA.
Funding for H. W. was generously provided by the China
Scholarship Council.
References
Description of Permianibacter gen. nov.
Permianibacter (Per.mi.a.ni.bac9ter. N.L. adj. permianus
referring to the Permian era; N.L. masc. n. bacter a rod.;
N.L. masc. n. Permianibacter the Permian rod, referring
to the isolation of the type species from Permian
groundwater).
Cells are aerobic, Gram-stain-negative rods. Endospores
are not formed. Urease-negative, catalase-negative and
oxidase-positive. The predominant cellular fatty acids are
iso-C15 : 0, summed feature 9 (iso-C17 : 1v9c), C16 : 0 and
summed feature 3 (C16 : 1v7c/C16 : 1v6c). The main respiratory quinone is Q-8. The polar lipid profile contains
phosphatidylethanolamine, an unidentified aminophospholipid, and some other unidentified lipids. 16S rRNA
gene-based phylogenetic analysis indicates the genus
Permianibacter is affiliated with the family Pseudomonadaceae
and distinct from all known genera.
The type species is Permianibacter aggregans.
Description of Permianibacter aggregans sp. nov.
Permianibacter aggregans (ag9gre.gans. L. part. adj. aggregans aggregating).
Displays the following characteristics in addition to those
given in the genus description. Cells are ca. 1.6–2.7 mm long
and 0.4 mm wide and non-motile. Colonies are circular, flat
and yellow on marine agar after 72 h cultivation. The
temperature suitable for growth ranges from 25 uC to 45 uC.
The pH suitable for growth ranges from pH 6–10. Optimal
salinity for growth ranges from 2 % to 8 % (w/v). Capable of
hydrolysing maltose, glucose, gluconate, and Adipic acid
(API 20 NE assay). By applying API 50 CHB, acids are
produced from the substrates (+)-cellobiose, (+)-sucrose,
(+)-maltose, starch, 5-keto-D-gluconic acid and potassium
salt gluconate.
3506
Austin, D. A. & Moss, M. O. (1986). Numerical taxonomy of red-
pigmented bacteria isolated from a Lowland river, with the description
of a new taxon, Rugamonas rubra gen. nov., sp. nov. J Gen Microbiol
132, 1899–1909.
Blackall, L. L., Hayward, A. C. & Sly, L. I. (1985). Cellulolytic and
dextranolytic Gram-negative bacteria: revival of the genus Cellvibrio.
J Appl Bacteriol 59, 81–97.
Carmeli, Y., Troillet, N., Eliopoulos, G. M. & Samore, M. H. (1999).
Emergence of antibiotic-resistant Pseudomonas aeruginosa: comparison
of risks associated with different antipseudomonal agents. Antimicrob
Agents Chemother 43, 1379–1382.
CLSI (2011). Performance Standards for Antimicrobial Susceptibility
Testing; 21st Informational Supplement M100-S21. Wayne, PA:
Clinical and Laboratory Standards Institute.
De Ley, J. & Park, I. W. (1966). Molecular biological taxonomy of
some free-living nitrogen-fixing bacteria. Antonie van Leeuwenhoek
32, 6–16.
De Smedt, J., Bauwens, M., Tytgat, R. & De Ley, J. (1980). Intra-
and intergeneric similarities of ribosomal ribonucleic acid cistrons
of free-living, nitrogen-fixing bacteria. Int J Syst Bacteriol 30, 106–
122.
Enticknap, J. J., Kelly, M., Peraud, O. & Hill, R. T. (2006).
Characterization of a culturable alphaproteobacterial symbiont common to many marine sponges and evidence for vertical transmission via
sponge larvae. Appl Environ Microbiol 72, 3724–3732.
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.
Goto, M. & Kuwata, H. (1988). Rhizobacter daucus gen. nov., sp. nov.,
the causal agent of carrot bacterial gall. Int J Syst Bacteriol 38, 233–
239.
Hespell, R. B. (1977). Serpens flexibilis gen. nov., sp. nov., an unusually
flexible, lactate-oxidizing bacterium. Int J Syst Bacteriol 27, 371–381.
Holmes, B., Steigerwalt, A. G., Weaver, R. E. & Brenner, D. J.
(1986). Chryseomonas polytricha gen. nov., sp. nov., a Pseudomonas-
like organism from human clinical specimens and formerly known as
group Ve-1. Int J Syst Bacteriol 36, 161–165.
Holmes, B., Steigerwalt, A. G., Weaver, R. E. & Brenner, D. J.
(1987). Chryseomonas luteola comb. nov. and Flavimonas oryzihabi-
tans gen. nov., comb. nov., Pseudomonas-like species from human
Downloaded from www.microbiologyresearch.org by
International Journal of Systematic and Evolutionary Microbiology 64
IP: 124.16.240.197
On: Thu, 17 Dec 2015 06:17:36
Permianibacter aggregans gen. nov., sp. nov.
clinical specimens and formerly known, respectively, as groups Ve-1
and Ve-2. Int J Syst Bacteriol 37, 245–250.
Hugh, R. & Leifson, E. (1964). The proposed neotype strains of
Pseudomonas aeruginosa (Schroeter 1872) Migula 1900. Int Bull
Bacteriol Nomencl Taxon 14, 69–84.
Kim, O. S., Cho, Y. J., Lee, K., Yoon, S. H., Kim, M., Na, H., Park, S. C.,
Jeon, Y. S., Lee, J. H. & other authors (2012). Introducing EzTaxon-
Palleroni, N. J. (1984). Genus I. Pseudomonas Migula 1894, 237AL
(nom. cons. Opin. 5, Jud. Comm. 1952, 237). In Bergey’s Manual of
Systematic Bacteriology, vol. 1, pp. 141–199. Edited by N. R. Krieg &
J. G. Holt. Baltimore: Williams & Wilkins.
Parte, A. C. (2014). LPSN–list of prokaryotic names with standing in
nomenclature. Nucleic Acids Res 42 (Database issue), D613–D616.
Rediers, H., Vanderleyden, J. & De Mot, R. (2004). Azotobacter
e: a prokaryotic 16S rRNA gene sequence database with phylotypes
that represent uncultured species. Int J Syst Evol Microbiol 62, 716–
721.
Skerman, V. B. D., McGowan, V. & Sneath, P. H. A. (1980). Approved
Mandel, M. & Marmur, J. (1968). Use of ultraviolet absorbance-
Suarez, C., Ratering, S., Kramer, I. & Schnell, S. (2014). Cellvibrio
temperature profile for determining the guanine plus cytosine content
of DNA. Methods Enzymol 12B, 195–206.
Minnikin, D. E., O’Donnell, A. G., Goodfellow, M., Alderson, G.,
Athalye, M., Schaal, A. & Parlett, J. H. (1984). An integrated
procedure for the extraction of bacterial isoprenoid quinones and
polar lipids. J Microbiol Methods 2, 233–241.
Nedashkovskaya, O. I., Kim, S. B., Han, S. K., Rhee, M. S., Lysenko,
A. M., Falsen, E., Frolova, G. M., Mikhailov, V. V. & Bae, K. S. (2004a).
Ulvibacter litoralis gen. nov., sp. nov., a novel member of the family
Flavobacteriaceae isolated from the green alga Ulva fenestrata. Int J
Syst Evol Microbiol 54, 119–123.
Nedashkovskaya, O. I., Vancanneyt, M., Van Trappen, S.,
Vandemeulebroecke, K., Lysenko, A. M., Rohde, M., Falsen, E.,
Frolova, G. M., Mikhailov, V. V. & Swings, J. (2004b). Description of
Algoriphagus aquimarinus sp. nov., Algoriphagus chordae sp. nov. and
Algoriphagus winogradskyi sp. nov., from sea water and algae, transfer
of Hongiella halophila Yi and Chun 2004 to the genus Algoriphagus as
Algoriphagus halophilus comb. nov. and emended descriptions of the
genera Algoriphagus Bowman et al. 2003 and Hongiella Yi and Chun
2004. Int J Syst Evol Microbiol 54, 1757–1764.
vinelandii: a Pseudomonas in disguise? Microbiology 150, 1117–1119.
lists of bacterial names. Int J Syst Bacteriol 30, 225–420.
diazotrophicus sp. nov., a nitrogen-fixing bacteria isolated from the
rhizosphere of salt meadow plants and emended description of the
genus Cellvibrio. Int J Syst Evol Microbiol 64, 481–486.
MEGA4: molecular
evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol
Evol 24, 1596–1599.
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007).
Vessey, J. K. (2003). Plant growth promoting rhizobacteria as
biofertilizers. Plant Soil 255, 571–586.
Wang, H., Laughinghouse, H. D., IV, Anderson, M. A., Chen, F.,
Willliams, E., Place, A. R., Zmora, O., Zohar, Y., Zheng, T. & Hill, R. T.
(2012). Novel bacterial isolate from Permian groundwater, capable of
aggregating potential biofuel-producing microalga Nannochloropsis
oceanica IMET1. Appl Environ Microbiol 78, 1445–1453.
Yi, H. & Chun, J. (2004). Hongiella mannitolivorans gen. nov., sp. nov.,
Hongiella halophila sp. nov. and Hongiella ornithinivorans sp. nov.,
isolated from tidal flat sediment. Int J Syst Evol Microbiol 54, 157–162.
Yi, H., Chang, Y.-H., Oh, H. W., Bae, K. S. & Chun, J. (2003).
Zooshikella ganghwensis gen. nov., sp. nov., isolated from tidal flat
sediments. Int J Syst Evol Microbiol 53, 1013–1018.
Nishimura, Y., Kinpara, M. & Iizuka, H. (1989). Mesophilobacter
Young, J. M. & Park, D.-C. (2007). Probable synonymy of the
marinus gen. nov., sp. nov.: an aerobic coccobacillus isolated from
seawater. Int J Syst Bacteriol 39, 378–381.
nitrogen-fixing genus Azotobacter and the genus Pseudomonas. Int J
Syst Evol Microbiol 57, 2894–2901.
http://ijs.sgmjournals.org
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