ORIGINAL PAPER

Streptomyces jiujiangensis sp. nov., isolated from soilin South China

Bing-Huo Zhang • Juan Cheng • Li Li •

Yong-Guang Zhang • Hong-Fei Wang •

Han-Quan Li • Jian-Yuan Yang • Wen-Jun Li

Received: 27 November 2013 / Accepted: 29 January 2014 / Published online: 11 February 2014

� Springer International Publishing Switzerland 2014

Abstract An actinomycete capable of lysing cya-

nobacteria, strain JXJ 0074T, was isolated from a soil

sample collected from Jiangxi province, south China,

and characterized by using polyphasic taxonomy. The

new isolate showed morphological and chemotaxo-

nomic properties typical of members of the genus

Streptomyces. Phylogenetic analysis of the near-com-

plete 16S rRNA gene sequence indicated that strain

JXJ 0074T should be affiliated to the genus Strepto-

myces and exhibited highest similarities to Strepto-

myces shenzhenensis DSM 42034T (98.99 %) and

Streptomyces lucensis NBRC 13056T (98.60 %),

while the similarities to other members of the genus

are lower than 98.22 % similarity. However, the

DNA–DNA hybridization values between strain JXJ

0074T and S. shenzhenensis DSM 42034T or S.

lucensis NBRC 13056T were 46.2 ± 2.6 and

32.6 ± 3.1 %, respectively. Thus, on the basis of the

polyphasic data, strain JXJ 0074T represents a novel

species of the genus Streptomyces, for which the name

Streptomyces jiujiangensis sp. nov. is proposed. The

type strain is JXJ 0074T (= BCRC 16953T = KCTC

29262T).

Keywords Streptomyces jiujiangensis sp. nov. �Cyano-lytic actinomycete � Polyphasic

taxonomy

Introduction

Cyanobacterial blooms have become one of the most

prominent environmental concerns worldwide (Chen

et al. 2011; Dagnino et al. 2006; de Figueiredo et al.

2004; Wang et al. 2007; Guo 2007; Wu et al. 2011) and

pose a serious threat to the environment and human

health (Azevedo et al. 2002; Han et al. 2011; Oehrle

et al. 2010). It is difficult to regulate the occurrence of

cyanobacteria by conventional methods such as

biomanipulation and algicides (Ozaki et al. 2008).

Extensive research has indicated that actinomycetes

and their metabolites have great potential for control-

ling cyanobacterial blooms (Choi et al. 2005; Feng

Bing-Huo Zhang and Juan Cheng have contributed equally to

this work.

Electronic supplementary material The online version ofthis article (doi:10.1007/s10482-014-0132-5) contains supple-mentary material, which is available to authorized users.

B.-H. Zhang � J. Cheng � W.-J. Li (&)

Key Laboratory of Microbial Diversity in Southwest

China, Ministry of Education, Yunnan Institute of

Microbiology, Yunnan University, Kunming 650091, PR,

China

e-mail: liact@hotmail.com; wjli@ynu.edu.cn

B.-H. Zhang � H.-Q. Li � J.-Y. Yang

Jiujiang University, Jiujiang 332000, PR, China

L. Li � Y.-G. Zhang � H.-F. Wang � W.-J. Li

Key Laboratory of Biogeography and Bioresource in Arid

Land, Xinjiang Institute of Ecology and Geography,

Chinese Academy of Sciences, Urumqi 830011, China

123

Antonie van Leeuwenhoek (2014) 105:763–770

DOI 10.1007/s10482-014-0132-5

et al. 2013; Safferman and Morris 1962; Whyte et al.

1985; Yamamoto et al. 1998; Sigee et al. 1999; Yu

et al. 2011).

Actinomycetes are still the main known producers

of bioactive compounds and 45 % of 22,500 bioactive

compounds from microbes are produced by actino-

mycetes (Berdy 2005). Streptomyces, as the largest

antibiotic-producing genus (Watve et al. 2001), is the

dominant group of actinomycetes, and 75 % of

bioactive compounds from actinomycetes are pro-

duced by members of the genus Streptomyces (Berdy

2005). During a search for bacteria capable of lysing

cyanobacteria (cyano-lytic), one strain JXJ 0074T with

strong cyano-lytic activity was isolated from a soil

sample. The objective of this study was to determine

the taxonomic position of cyano-lytic strain JXJ

0074T.

Materials and methods

Isolation and maintenance of strain

Strain JXJ 0074T was isolated from a soil sample

(29o45‘N, 115o59‘E) collected from the rhizosphere of

a pine tree in a forest park of Jiujiang city, south China,

by using a serial dilution technique. After four days of

incubation on ISP2 medium (yeast extract-malt extract

agar; Shirling and Gottlieb 1966) at 28 �C, colonies

were picked and re-streaked repeatedly onto ISP2

medium to obtain pure cultures. The purified strain

was maintained on YIM 38 medium (Li et al. 2007) at

28 �C and stored as glycerol suspensions (20 %, v/v)

at-80 �C.

Morphological, cultural, physiological,

biochemical characteristics

Cultural characteristics were determined after 2 weeks

incubation at 28 �C on ISP2, ISP4 (inorganic salts-

starch agar), ISP5 (glycerol-asparagine agar), ISP6

(peptone yeast iron medium) (Shirling and Gottlieb

1966), Nutrient agar, tryptic soy agar (TSA) and

Czapek’s agar which were prepared according to Dong

and Cai (2001). Colour determination was carried out

by using colour chips from the ISCC–NBS colour

charts (standard samples, no. 2106) (Kelly 1964). The

specimen was prepared as described by Dong and Cai

(2001) and morphological properties were observed

by using a light microscope (Olympus BX43) and

scanning electron microscope (VEGA\\TESCNA)

after incubation on YIM 38 medium at 28 �C for

7 days.

Carbon source utilization was determined accord-

ing to Shirling and Gottlieb (1966) and Locci (1989).

Growth at various temperatures (4, 10, 15, 20, 28, 33,

37, 45, 50 and 55 �C), pH (3.0–11.0) and NaCl

contents (0–10 %, w/v, with interval of 1 %) were

examined according to Xu et al. (2005), using YIM 38

medium as the basal medium. Catalase activity was

tested with 3 % H2O2 according to standard method.

Other phenotypic characteristics were determined

using standard procedures (Goodfellow 1971; Wil-

liams et al. 1983).

Chemotaxonomy

The analysis of the isomer of diaminopimelic acid and

whole-cell sugars were performed by using the

procedures developed by Hasegawa et al. (1983) and

Tang et al. (2009). Polar lipids were extracted and

analysed according to published procedures (Minnikin

et al. 1979; Collins and Jones, 1980). Analysis of fatty

acids was performed by using the microbial identifi-

cation system (Sherlock Version 6.1; MIDI database:

TSSA6). Menaquinones were extracted according to

Collins et al. (1977) and separated by HPLC (Krop-

penstedt 1982).

Molecular analysis

Extraction of genomic DNA and PCR amplification of

the 16S rRNA gene were done according to Li et al.

(2007). The resultant 16S rRNA gene sequence was

aligned with sequences of the most closely related taxa

by using CLUSTAL_X1.83 (Thompson et al. 1997). A

phylogenetic tree was constructed by using the

neighbour-joining tree-making algorithms (Saitou

and Nei 1987) with MEGA version 5.0 (Tamura

et al. 2011). The Maximum-likelihood tree was

constructed by using MEGA version 5.0 (Tamura

et al. 2011). The topology of the phylogenetic tree was

evaluated by using bootstrap analysis with 1,000

replicates (Felsenstein 1985).

The G?C content of genomic DNA was deter-

mined using the HPLC method (Mesbah et al. 1989).

The quantitative microplate DNA–DNA hybridiza-

tions were carried out under optimal conditions as

764 Antonie van Leeuwenhoek (2014) 105:763–770

123

described by Ezaki et al. (1989). One of the two DNAs

for hybridization was labelled while the other was

immobilized, and the reciprocal experiments were

performed. The concentration of the two DNAs was

strictly controlled. Five replications for hybridization

were performed for each sample and the highest and

lowest values in each sample were excluded. The

relatedness values are expressed as the means of the

remaining three values and the results of DNA–DNA

hybridizations were taken from the means of related-

ness values.

Cyano-lytic activity tests

After being incubated in liquid medium (glucose 15 g,

soybean powder 15 g, soluble starch 10 g, yeast

extract 2 g, malt extract 2 g, peptone 2 g, NaCl 4 g,

K2HPO4 0.4 g, MgSO4.7H2O 0.5 g, CaCO3 2 g, H2O

1,000 ml, pH 7.8. CaCO3 was added into the medium

after adjustment of pH) for 5 days at 28 �C, the culture

broth of strain JXJ 0074T was centrifuged at

4,000 rpm and 2 % (v/v) of the resultant supernatant

was added into the cyanobacterial cultures. The tested

cyanobacteria included Microcystis aeruginosa

FACHB-905, M. aeruginosa FACHB-1203, Micro-

cystis wesenbergii FACHB -1112, Microcystis viridis

FACHB-1284, Microcystis flosaquae FACHB-1285,

Oscillatoria planctonica FACHB-708, Anabaena flos-

aquae FACHB-1092, Nostoc punctiforme FACHB-

252 and Oscillatoria tennuis FACHB-247, which were

all obtained from Institute of Hydrobiology, Chinese

Academy of Sciences. The cyanobacteria were

Table 1 Growth and cultural characteristics of strain JXJ-0074T on different growth media after incubation for 2 weeks at 28 �C

Medium Growth Aerial mycelium Substrate mycelium Diffusible pigment

Yeast extract-malt extract agar (IPS 2) Good White Gray yellow Gray yellow

Inorganic salts-starch agar (ISP 4) Good White Pink yellow None

Glycerol-asparagine agar (ISP 5) Moderate White Yellow white None

Peptone yeast iron medium (ISP6) Good White Vilid yellow None

Czapek solution agar (Difco) Poor – Vilid yellow None

Nutrient agar (Difco) Moderate White Violet None

Tryptic soy agar (TSA, Difco) Moderate – Vilid yellow None

Fig. 1 Scanning electron

micrograph of spore chains

of strain JXJ 0074T after

growth on YIM 38 medium

at 28 �C for 7 days. Bar,

2 lm

Antonie van Leeuwenhoek (2014) 105:763–770 765

123

cultured in HGZ medium (Yu et al. 2011) under an

illumination of 30–50 lmol photon/m2/s on a 12 h

light–dark cycle at 25 �C. The contents of chlorophyll

a of the cyanobacterial cultures were measured

according to Chen et al. (2006). The cyano-lytic

activities of the supernatant were evaluated by the

removal rates of the chlorophyll a. The metabolites of

strain JXJ 0074T were analyzed on thin layer

chromatography (TLC) by ninhydrin and anisalde-

hyde staining.

Results and discussion

Strain JXJ 0074T was observed to develop well-

branched substrate and aerial mycelia on ISP2, ISP4

Table 2 Phenotypic

characteristics

differentiating strain JXJ

0074T from its closest

phylogenetic neighbours, S.

shenzhenensis DSM 42034T

and S. lucensis NBRC

13056T

Taxa: 1, strain JXJ 0074T;

2, S. shenzhenensis DSM

42034T (Hu et al., 2011); 3,

S. lucensis NBRC 13056T

(Hu et al., 2011)

?, Positive reaction; -,

Negative reaction; ND, No

data

Characteristic JXJ 0074T 1 2

Spore chains Straight or spiral type Spiral or looped Spiral

Spore surface Smooth Smooth Spiny

Diffusible Pigment Yellow – –

Temperatures for growth (�C) 10–045 15–45 10–45

NaCl (w/v %) tolerance 0–3 0–3 0–3

pH value for growth 6–8 5–7 6–8

Degradation tests

Gelatin ? – –

Milk coagulation ? – ND

Milk peptonization ? ? ND

Nitrate reduction ? – –

Starch – ? –

Tween 40 ? ? –

Tween 80 ? ? –

Tyrosine ? ND –

Urea – ? –

Carbon utilization

D-arabinose ? – –

D-cellobiose – ? –

D-fructose ? ? –

D-glucose – ? ND

Inositol – ? –

Lactose ? ND –

D-mannitol – ? –

D-raffinose – ? –

L-rhamnose – ? ?

Succinic acid – ND ?

Sucrose – ? ND

D-trehalose ? ? –

D-xylose – ? –

Nitrogen utilization

D-arginine – ? –

L-glutamine – ? –

L-methionine ? – –

L-ornithine ? – ?

Amino acids Glycine, LL-DAP LL- and meso-DAP Glycine, LL-DAP

DNA G ? C content (mol %) 70.4 75 69.2

766 Antonie van Leeuwenhoek (2014) 105:763–770

123

and ISP6 media, with moderate growth on ISP5,

nutrient agar and TSA and poor growth on Czapek’s

agar. Soluble gray yellow pigments were found to be

produced on ISP2 medium (Table 1). Spore chains

were observed to be of the straight or rectiflexibile

type, with elliptical spores (about 0.4–0.6 lm in

diameter and 0.6–1.0 lm in length) and smooth spore

surfaces (Fig. 1). Detailed physiological characteris-

tics are given in Table 2 and the species description.

The results of cyano-lytic testing indicated that

strain JXJ 0074T secreted metabolites which exhibited

strong cyano-lytic activities to M. aeruginosa

FACHB-905, M. aeruginosa FACHB-1203, M. wes-

enbergii FACHB -1112, M. viridis FACHB-1284 and

M. flosaquae FACHB-1285, but weak or no cyano-

lytic activity to the rest cyanobacteria used in this

study. The active compounds were suggested to

contain amino-groups by ninhydrin staining (data not

shown).

Strain JXJ 0074T was found to contain LL-diami-

nopimelic acid in its cell wall, with whole-cell

sugars of rhamnose, ribose, galactose and glucose.

Polar lipids were determined to include

diphosphatidylglycerol, phosphatidylethanolamine,

phosphatidylinositol, phosphatidylinositolmanno-

sides, an unidentified aminophospholipid, phosphati-

dylinositol dimannoside and an unknown

phospholipid (see supplementary Fig. S1). The men-

aquinones were identified as MK-9(H8) (67.1 %),

MK-9(H6) (18.5 %), MK-7 (9.4 %), MK-7(H2)

(1.8 %), MK-10(H4) (1.8 %), MK-10(H6) (0.7 %),

MK-9(H10) (0.5 %) and MK-10(H2) (0.2 %). The

major components of the fatty acids were determined

to be anteiso-C15:0 (43.6 %), iso-C16:0 (17.7 %),

anteiso-C17:0 (15.8 %), anteiso -C17:1 w9c (6.7 %),

iso-C15:0 (4.3 %), iso-H C16:1 (3.8 %) and iso-C14:0

(2.6 %). The G?C content of the genomic DNA of the

type strain was determined to be 70.4 mol%.

Analysis of the almost-complete 16S rRNA gene

sequence (1,516 bp; GenBank accession number

KF938657) indicated that strain JXJ 0074T belongs

to the genus Streptomyces, and it formed a distinct

clade with Streptomyces shenzhenensis DSM 42034T

by using both tree-making methods (Fig. 2). The

phylogenetic analysis suggested an affiliation between

strain JXJ 0074T, S. shenzhenensis DSM 42034T and

Fig. 2 Neighbour-joining

phylogenetic tree based on

16S rRNA gene sequences

of strain JXJ 0074T and its

closest relative species of

the genus Streptomyces.

Bootstrap values (expressed

as percentages of 1,000

replications) [ 50 % are

shown at the nodes.

Asterisks indicate clades that

were conserved when the

maximum-likeli Table 1.

Growth and cultural

characteristics of strain JXJ-

0074T on different growth

media after incubation for

2 weeks at 28 �C

Antonie van Leeuwenhoek (2014) 105:763–770 767

123

species affiliated with clades 11 and 12 as defined by

Labeda et al. (2012). The 16S rRNA gene sequence of

strain JXJ 0074T showed the highest similarities to

those of S. shenzhenensis DSM 42034T (98.99 %) and

S. lucensis NBRC 13056T (98.60 %) and had lower

than 98.22 % similarities with all the other type strains

of the genus Streptomyces. Stackebrandt and Ebers

(2006) recommended an increase of about 2 % (from

97 % to 98.7–99 %) in the threshold for 16S rRNA

gene sequence similarity used to determine the

uniqueness of a novel isolate, provided that this level

of difference in the sequences was supported by clear

phenotypic differences. In this study, therefore, DNA–

DNA relatedness experiments were only carried out

between strain JXJ 0074T and the type strains of the

validly named species to which it appeared most

closely related: S. shenzhenensis DSM 42034T

(98.99 %) and S. lucensis NBRC 13056T (98.60 %).

DNA–DNA relatedness with S. shenzhenensis DSM

42034T and S. lucensis NBRC 13056T were

46.2 ± 2.6 % and 32.6 ± 3.1 % respectively (see

supplementary Table S1), which supported the

hypothesis that these three strains belong to different

genomic species. Many other phenotypic characteris-

tics also distinguished strain JXJ 0074T from its

closest relatives, such as production of diffusible

pigment, nitrate reduction, carbon- and nitrogen-

source utilization (Table 2). Thus, based on the data

in this study, we propose that strain JXJ 0074T

represents a novel species of the genus Streptomyces,

for which the name Streptomyces jiujiangensis sp.

nov. is proposed.

Description of Streptomyces jiujiangensis sp. nov

Streptomyces jiujiangensis (jiu.jiang’en.sis. N.L.

masc. adj. jiujiangensis. pertaining to Jiujiang, China,

from where the strain was isolated).

Aerobic, Gram-positive actinomycete that forms

well-branched substrate and aerial mycelia; aerial

mycelia differentiate into straight or rectiflexibile

spore chains. Spores are elliptical with a smooth

surface. Aerial mycelia are white; vegetative mycelia

are yellow-white. Gray yellow soluble pigments are

produced. The pH, NaCl concentrations and temper-

ature range for growth are pH 6.0–10.0 (optimum pH

7.0), 0–3 % NaCl and 10–45 �C (optimum 28 �C).

Positive in tests for catalase, milk coagulation, milk

peptonization, nitrate reduction, but negative for urea

and H2S production. Hydrolyses Tweens 20, 40, 60

and 80, gelatin and tyrosine, but not cellulose or

starch. D-arabinose, D-galactose, D-fructose, lactose, D-

mannose, starch and D-trehalose can be used as sole

carbon sources, but not D-cellobiose, inositol, D-

glucose, maltose, D-mannitol, D-raffinose, L-rhamnose,

sodium malate, succinic acid, sucrose, xylitol or D-

xylose. L-alanine, L-asparagine, L-hydroxyproline,

glycine, L-methionine, L-ornithine, L-phenylalanine,

L-proline, L-serine, L-tyrosine and L-valine can be used

as sole nitrogen sources, but not D-arginine, L-gluta-

mine, L-histidine, L-lysine or L-tryptophan.

The type strain, JXJ 0074T (= BCRC

16953T = KCTC 29262T), was isolated from a soil

sample collected in Jiangxi province, south China. The

16S rRNA gene sequence of strain JXJ 0074T was

submitted in the GenBank database under the acces-

sion number KF938657.

Acknowledgments The authors are grateful to Prof. Hans-

Peter Klenk from DSMZ and Dr. Tomohiko Tamura from

NBRC for their kind providing reference type strains. This

research was supported by the Natural Science Foundation of

China (No. 31060010) and Programs of the Education

Department (No. GJJ10619) and Science and Technology

Department (No. 20111BBG70012-4) of Jiangxi Province of

China. Y-G Zhang and L Li were both supported by West Light

Foundation of The Chinese Academy of Sciences. W-J Li was

also supported by the ‘Hundred Talents Program’ of the Chinese

Academy of Sciences.

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