Streptomyces baliensis sp. nov., isolated from Balinese soil

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DOI 10.1099/ijs.0.007179-0

International Journal of Systematic and Evolutionary Microbiology (2009), 59, 2158-2161

Streptomyces ba/iensis sp. nov., isolated from
Balinese soil
Misa Otoguro, 1 Shanti Ratnakomala,2 Yulin Lestari,3 Ratih D. Hastuti, 4
Evi Triana,5 Yantyati Widyastuti 2 and Katsuhiko Ando 1
Correspondence

1

NITE Biological Resource Center (NBRC), Department of Biotechnology, National Institute of
Technology and Evaluation (NITE), 2-5-8 Kazusakamatari, Kisarazu, Chiba 292-0818, Japan

Misa Otoguro

otoguro-misa@nite.go.jp

2

Research Center for Biotechnology, Indonesian Institute of Sciences, JI. Raya Bogor Km. 46,
Cibinong 16911, Indonesia

3

Department of Biology, Faculty of Mathematics and Natural Sciences, Bogor Agricultural
University, JI Raya pajajaran, Bogor 16144, Indonesia

4

Soil Research Institute, JI. Ir. H. Juanda 98, Bogor 16002, Indonesia

5

Research Center for Biology, Indonesian Institute of Sciences, JI. Raya Bogor Km. 46, Cibinong
16911, Indonesia

The taxonomic positions of actinomycete strains 1003-0915r and 1003-0825, isolated from soil
on the Indonesian island of Bali, were examined using a polyphasic taxonomic approach. The
morphological and chemotaxonomic characteristics of these organisms are typical of the genus
Streptomyces. Phylogenetic analyses performed using almost-complete 16$ rRNA gene
sequences demonstrated that the strains were closely related to Streptomyces glauciniger and
Streptomyces fi/acinus. However, DNA-DNA hybridization and phenotypic characteristics
revealed that the strains differed from known Streptomyces species. Therefore, we conclude that
strains ID03-0915r and ID03-0825 (=BTCC B-563) represent a novel species of the genus
Streptomyces, for which we propose the name Streptomyces ba/iensis sp. nov. The type strain is
strain ID03-0915r (= BTCC B-608r = NBRC 104276r).

The genus Streptomyces was proposed by Waksman &
Henrici (1943) and includes aerobic, spore-forming soil
bacteria with high DNA G+C contents (69-78 molo/o);
rod-shaped spores originate from the substrate mycelium,
11-diaminopimelic acid (LL-A2pm) is found in the cell wall
and galactose and mannose are found in whole-cell
hydrolysates. Although the genus Streptomyces contains
more than 500 species (Hain et al., 1997) with validly

published names, the genus remains a target for screening
for novel secondary metabolites.
In the course of an investiftion of actinomycetes from
Indonesia, strains 1D03-0915 and 1003-0825 were isolated
from soil collected from the island of Bali. These isolates
formed colonies typical of the genus Streptomyces. The aim
of this study was to determine the taxonomic positions of
strains ID03-0915T and JD03-0825 by a polyphasic
Abbreviation: A 2 pm, diaminopimelic acid.
The GenBank/EMBUDDBJ accession numbers for the 16S rRNA gene
sequences of strains 1003-0915T (=NBRC 104276T) and 1003-08'25
BTCC 8-563) are AB441718 and AB44 1719.

(=

Detailed cultural properties of the novel strains are available as
supplementary material with the online version of this paper.

2158

taxonomic approach that included phylogenetic analyses,
chemotaxonomic characteristics, DNA-DNA hybridization
and physiological properties.
The strains were isolated using the SOS/yeast extract
method (Hayakawa & Nonomura, 1989) and humic acid/
vitamin (HV) agar (Hayakawa & Nonomura, 1987)
supplemented with cydohe:ximide (SO mg 1-1) and nali1
dixic acid (20 mg r ). Morphological and chemotaxonomic studies were performed with the two isolates to
confirm whether they exhibited properties similar to those
of the genus Streptomyces. Morphology was observed under
a light microscope and a scanning electron microscope
(SEM model JSM-6060; JEOL) on yeast extract-starch (YS)
medium or HV agar incubated for 14 days at 28 °C.
Cultural and physiological characteristics were examined as
described previously (Shirling & Gottlieb, 1966)
A2pm isomers and whole-cell sugar patterns were analysed
according to the procedures developed by Hasegawa et aC·.
(1983) and Lechevalier & Lechevalier (1980). Fatty acid
compositions were analysed by GC using the MIDI system
(Sasser, 1990; Kampfer & Kroppenstedt, 1996). Isoprenoid

quinones and polar lipids were examined as described
previously (Schaal, 1985; Minnilcin et al., 1984; Tamura et
007179 © 2009 IUMS Printed in Great Britain

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M. Otoguro and others

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100

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thermotineatus NBRC 14750T (AB184618)
S. thioluteus NBRC 13341 1 (AY999848)
S. blastmyceticus NBRC 127471 (AB249910)
S. lilacinus NBRC 12884T (AB249906)
S. abikoensis NBRC 13860T (AB184537)
'----S. maJaysiensis NBRC 164461 (AB249918)
S. baliensis NBRC 1042761 (AB441718)

S. glauciniger NBRC 1009 t 3T (AB249964)
S. rubidus CGMCC 4.20261 (AY876941)
S. yangfinensis 13071 (AY876940)
S. yeochonensis NBRC 1007821 (AB249943)
S. glaucosporvs NBRC 1541 ST (AB184664)
..----S. megasporus NBRC 147491 (AB184617)
S. macrosporus NBRC 147481 (AB184616)

Botanic Garden on Bali, Indonesia. Strain 1003-0825
( = BTCC B-563) is a second strain of the species.

Acknowledgements
This study was conducted under the Joint Research Project between
Department of Biotechnology, National Institute of Technology and
Evaluation, Japan, and the Indonesian Institute of Sciences (UPI)
representing Indonesian Government Research Institutes. The
authors would Like to thank Ms Yayoi Salciyama for her assistance
with the chemotaxonomic analyses, Mr Nobuyu.ki Goto for providing
the 16S rRNA gene sequences and Dr Tomohiko Tamura for
providing valuable suggestions.

References
Fig. 1. Phylogenetic tree constructed by the neighbour-joining
method (Saitou & Nei, 1987) using almost-complete 16S rRNA
gene sequences, showing the relationships of strain NBRC
104276T (=ID03-0915T) with type strains of closely related
Streptomyces species. Numbers on branches indicate percentage
bootstrap values determined for 1000 replicates (only values
above 60% are indicated). Bar, 0.01 Kr.uc· Asterisks. indicate
branches of the tree that were also recovered using the maximumparsimony (Fitch, 1971) and maximum-likelihood (Felsenstein,
1981) tree-making algorithms.

Streptomyces species be recognized as belonging to distinct
species of the genus (Labeda, 1993, 1996, 1998).
It is clear from the phenotypic and genotypic data that the
two isolates should be classified within a novel species of
the genus Streptomyces, for which we propose the name
Streptomyces baliensis sp. nov.

Description of Streptomyces baliensls sp. nov.

Streptomyces baliensis (ba.li.en' sis. N.L. masc. adj. baliensis
pertaining to the island of Bali, Indonesia, where the first
strains were isolated).
Aerobic and strains Gram-positive. Forms well-branched
vegetative hyphae and white to grey aerial mycelium. The
substrate mycelium is pale yellow to yellow. The aerial
mycelium is moderate white to grey on yeast extract/malt
extract agar or oatmeal agar. Spore surface is smooth. Soluble
pigments are not produced. Melanin pigments are produced
on tyrosine agar. Glucose, galactose, mannose, melibiose and
lactose are used as sole carbon sources. Grows at 10-30 °C
with an optimum around at 28 °C; no growth at 37 °C.
Optimum growth around pH 7.0. No growth in the presence
of 2 % NaCl. Additional phenotypic properties are listed in
Table 1. Type II phospholipids and menaquinones MK9(1It;), MK-9(H8 ) and MK-9(H4 ) are detected. The major
cellular fatty acids are iso-C 16 :o and iso-C14 , 0 • The G+C
content of DNA of the type strain is 71.l mol%.

ｅｺ｡ｫｾ＠
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Hashimoto, Y. & Yabuuchi, E. (1989). Fluorometric
deoxyribonucleic acid-deoxyribonucleic acid hybridization in miaodilution wells as an alternative to membrane filter hybrid.i7.ation in
which radioisotopes are used to determine genetic relatedness among
bacterial strains. Intl Syrt Bacterial 39, 224-229.

Felsenstein, J. (1981). Evolutionary trees from DNA sequences: a
maximum likelihood approach. J Mol Evol 17, 368-376.
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach
using the bootstrap. Evolution 39, 783-791.
Fitch, W. M. (1971). Toward defining the course of evolution:
minimum change for a specific tree topology. Syst Zool 20, 406-416.
Hain, T., Ward-Rainey, N., Kroppenstedt, R. M., Stackebrandt, E. &
Rainey, F. A. .(1997). Discrimination of StreptQmyces albidojlavus
strains based on the size and number of 16S-23S ribosomal DNA
intergenic spacers. Intl Syrt Bacterial 47, 202-206.
Hasegawa, T., Taklzawa, M. & Tanlda, S. (1983). A rapid analysis for
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H. (2003). Taxonomic re-evaluation of
Hatano, K., Nishii, T. & ｋ｡ｳｾ＠
whorl-forming Streptomyces (formerly Streptoverticillium) species by
using phenotypes, DNA-DNA hybridization and sequence of gyrB,
and proposal of Streptomyces luteireticuli (ex Katoh and Arai 1957)
corrig., sp. nov., nom. rev. Intl Syst Evol Microbiol 53, 1519-1529.

Hayakawa, M. & Nonomura, H. (1987). Humic acid-vitamin agar, a
new medium for selective isolation of soil actinomycetes. J Ferment
Technol 65, 501-509.
Hayakawa, M. & Nonomura, H. (1989). A new method for the

intensive isolation of actinomycetes from soil Actinomycetologica 3,
95-104.
Kimpfer, P. & Kroppenstedt, R. M. (1996). Numerical analysis of fatty
acid patterns of corynefonn bacteria and related taxa. Can J Microbiol
42, 989-1005.
Kumar, ｓｾ＠ Tamura, K. & Nel, M. (2004). MEGA3: integrated software
for molecular evolutionary genetics analyses and sequence alignment.

Brief Bioinform S,

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Labeda, D. P. (1993). DNA relatedness among strains of the
Streptomyces lavendulae pbenotypic cluster group. Int J Syrt
Bacterial 43, 822-825.
\
Labeda, D. P. (1996). DNA relatedness among verticil-forming
Streptomyces species (formerly Streptovertidllium species). Int J Syrt
Bacteriol 46, 699-703.

Type strain is strain ID03-0915T (=BTCC B-608T =NBRC
104276T), isolated from a soil sample collected in Eka karya

Labeda, D. P. (1998). DNA relatedness among the Streptomyces
fulvissimus and Strepwmyces griswviridis phenotypic cluster groups.
Int J Syst Bacterial 48, 829-832.

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