ORIGINAL PAPER

Streptomyces fukangensis sp. nov., a novel alkaliphilicactinomycete isolated from a saline-alkaline soil

Yong-Guang Zhang • Hong-Fei Wang • Qing Liu • Wael N. Hozzein •

Mohammed A. M. Wadaan • Juan Cheng • Yue-Ji Chen •

Yuan-Ming Zhang • Wen-Jun Li

Received: 26 July 2013 / Accepted: 25 September 2013 / Published online: 5 October 2013

� Springer Science+Business Media Dordrecht 2013

Abstract An alkaliphilic actinobacterium, designated

EGI 80050T, was isolated from a desert soil sample of

Xinjiang, north-west China, and characterized by a

polyphasic approach. The isolate was observed to

produce purple orange-yellow aerial mycelium and dark

orange-yellow substrate mycelium on yeast extract-malt

extract agar medium. Whole-cell hydrolysates of strain

EGI 80050T were found to contain LL-diaminopimelic

acid as the diagnostic diamino acid, and galactose,

glucose, rhamnose and mannose as the main sugars. The

major fatty acids identified were C16:0-iso (36.8 %),

C15:0-anteiso (17.3 %), 15:0-iso (13.2 %) and 14:0-iso

(10.5 %). The predominant menaquinones detected

were MK-9(H6) and MK-9(H8), while the characteristic

polar lipids were identified as diphosphatidylglycerol,

phosphatidylglycerol, phosphatidylinositol, phosphati-

dylinositol mannosides, phosphatidylmethylethanola-

mine and three unknown phospholipids. The G?C

content of the genomic DNA was determined to be

67.9 mol%. Phylogenetic analysis based on 16S rRNA

gene sequences affiliated the strain EGI 80050T to the

genus Streptomyces. Levels of 16 rRNA gene sequence

similarities between strain EGI 80050T and Streptomy-

ces candidus NRRL ISP-5141T, Streptomyces cremeus

NBRC 12760T, Streptomyces spiroverticillatus NBRC

12821T, Streptomyces violaceorectus NBRC 13102T,

Streptomyces cinereoruber subsp. cinereoruber NBRC

12756T were 96.7, 96.6, 96.6, 96.6 and 96.6 %, respec-

tively. Based on the phenotypic, chemotaxonomic and

phylogenetic data, strain EGI 80050T is considered to

represent a novel species of the genus Streptomyces, for

which the name Streptomyces fukangensis sp. nov. (type

strain EGI 80050T = BCRC 16945T = JCM 19127T) is

proposed.

Yong-Guang Zhang and Hong-Fei Wang contributed equally to

this work.

Electronic supplementary material The online version ofthis article (doi:10.1007/s10482-013-0045-8) contains supple-mentary material, which is available to authorized users.

Y.-G. Zhang � H.-F. Wang � Y.-J. Chen �Y.-M. Zhang � W.-J. Li (&)

Key Laboratory of Biogeography and Bioresource in Arid

Land, Xinjiang Institute of Ecology and Geography,

Chinese Academy of Sciences, Ur}umqi 830011,

People’s Republic of China

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

H.-F. Wang

University of Chinese Academy of Sciences,

Beijing 100049, China

Q. Liu � J. Cheng � W.-J. Li

Yunnan Institute of Microbiology, Yunnan University,

Kunming 650091, Yunnan, People’s Republic of China

W. N. Hozzein � M. A. M. Wadaan � W.-J. Li

Bioproducts Research Chair (BRC), College of Science,

King Saud University, P.O. Box 2455, Riyadh 11451,

Kingdom of Saudi Arabia

123

Antonie van Leeuwenhoek (2013) 104:1227–1233

DOI 10.1007/s10482-013-0045-8

Keywords Alkaliphilic actinomycete �Polyphasic taxonomy � Streptomyces

fukangensis sp. nov.

Introduction

The genus Streptomyces was proposed by Waksman

and Henrici (1943). At the time of writing, the genus

contains nearly 630 validly named species (Euzeby

2012). Streptomyces species are well known as a rich

source of antibiotics and bioactive molecules (Berdy

2005, 2012; Goodfellow and Fiedler 2010). In recent

years, the search for novel pharmaceutical agents

against drug resistant microbes from common Strep-

tomyces species has become a more difficult and costly

task, therefore, more attention has focused on strep-

tomycetes from unusual and unexplored environ-

ments, such as marine environments (Kin 2006) and

desert soil (Li et al. 2005; Rateb et al. 2011a, b;

Nachtigall et al. 2011; Santhanam et al. 2013). During

our investigations on the diversity and bioactivity of

actinomycetes from a desert soil of Xinjiang, north-

west China, a novel alkaliphilic actinomycete strain,

designated EGI 80050T, was isolated. Polyphasic

analyses established the affiliation of the new isolate

to the genus Streptomyces. The isolate represents a

novel species of the genus Streptomyces, for which the

name Streptomyces fukangensis sp. nov. is proposed.

Materials and methods

Isolation and culture of the organism

Strain EGI 80050T was isolated from a desert sample,

collected from Fukang, Xinjiang, north-west China,

after 4 weeks incubation at 30 �C on a modified

Cellulose-Casein-Multi-Salts medium (CCMS) (Tang

et al. 2008). The isolation medium consisted of 10 g

microcrystalline cellulose, 0.3 g casein, 0.2 g KNO3,

0.5 g K2HPO4, 0.02 g CaCO3, 0.01 g FeSO4, 10 g

NaCl, 15 g agar and 1 l distilled water. After steriliza-

tion, the medium was adjusted to pH 10.0 with

autoclaved 10 N NaOH to select for alkaliphilic

bacteria. Horikoshi-I medium (Horikoshi 1999)

adjusted to pH 10.0 with 10 N NaOH instead of

Na2CO3 addition was used for cultivating and main-

taining the purified isolate. Strain EGI 80050T was

preserved as glycerol suspensions (20 %, w/v) at

-80 �C. The strain has been deposited in the Biore-

sources Collection and Research Center, Taiwan

(BCRC) as strain BCRC 16945T and in the Japan

Collection of Microorganisms (JCM) as strain JCM

19127T. Streptomyces cinereoruber subsp. cinereoru-

ber DSM 40279T and Streptomyces violaceorectus

DSM 41512T were obtained from German Collection of

Microorganisms and Cell Cultures (DSMZ) and grown

on DSMZ medium 65 at 30 �C for physiological tests.

Morphological, physiological and biochemical

characteristics

Strain EGI 80050T was cultured on Horikoshi-I medium

(Horikoshi 1999) adjusted to pH 10.0 with 10 N NaOH,

for 14–28 days at 30 �C, and morphological properties

were observed by light microscopy (Olympus micro-

scope BH-2) and scanning electron microscopy (Quanta

200; FEI). Culture features were determined after 2 and

4 weeks incubation at 30 �C according to the methods

of Shirling and Gottlieb (1966). All media were adjusted

to pH 10.0 with NaOH. Colours of the aerial and

substrate mycelia were determined with the ISCC–NBS

colour charts (standard sample no. 2,106; Kelly 1964).

Carbon sources utilization tests were performed accord-

ing to the methods described by Shirling and Gottlieb

(1966). Nitrogen sources utilization tests were carried

out as described by Williams et al. (1983). NaCl

tolerance tests were performed on Tryptone Soy Agar

(TSA) adjusted to pH 10.0 and supplemented with

various NaCl concentrations (0, 1, 2.5, 5, 7.5, 10, 12.5,

15, 17.5, 20, 25 and 30 %, w/v). Temperature range for

growth was examined at 5, 10, 15, 20, 25, 30, 35, 40, 45,

55 and 60 �C on TSA adjusted to pH 10.0. Growth at

different pH values (4.0–12.0, at intervals of 1.0 pH unit)

was examined on Tryptone Soy Broth (TSB) using the

buffer system described by Xu et al. (2005). Other

physiological and biochemical characteristics were

examined as described previously (Goodfellow 1971;

Williams et al. 1983).

Chemotaxonomy

Biomass for chemical and molecular studies was

obtained by cultivation in shake flasks (at 150 r.p.m.)

using Horikoshi-I broth adjusted to pH 10.0 with

NaOH after incubation at 30 �C for 3 weeks. Amino

acids of whole-cell hydrolysates were analyzed by

1228 Antonie van Leeuwenhoek (2013) 104:1227–1233

123

TLC as described previously (Staneck and Roberts

1974). Cell-wall sugars were detected after precolumn

derivatization with 1-phenyl-3-methyl-5-pyrazolone

(PMP) by HPLC (Tang et al. 2009). Polar lipids were

extracted and identified by two-dimensional TLC

following the method of Minnikin et al. (1984).

Menaquinones were extracted and analysed by HPLC

as described previously (Collins et al. 1977). For fatty

acid analysis, strain EGI 80050T was cultured on TSB

medium adjusted to pH 10.0 with NaOH at 30 �C for

7 days. Reference strains were cultured on TSB

medium with pH 7.0. Cellular fatty acids analysis

was performed as described by Sasser (1990) accord-

ing to the standard protocol of the MIDI/Hewlett

Packard Microbial Identification System. For deter-

mination of G?C content, the genomic DNA of EGI

80050T was prepared according to Marmur (1961).

The G?C content of the DNA was determined by the

HPLC method (Mesbah et al.1989).

Phylogenetic analysis

Genomic DNA preparation, PCR amplification and

sequencing of the 16S rRNA gene were carried out

using procedures described by Li et al. (2007).

Multiple alignments with sequences of the Strepto-

myces type strains, and calculations of levels of

sequence similarities were carried out using the

EzTaxon-eserver (http://eztaxon-e.ezbiocloud.net/;

Kim et al. 2012). Phylogenetic analysis was performed

using three tree-making algorithms: the neighbour-

joining (Saitou and Nei 1987), maximum-likelihood

(Felsenstein 1981) and maximum-parsimony (Fitch

1971) by using the software MEGA 5.0 (Tamura et al.

2011). The topologies of the resultant trees were

evaluated by using the bootstrap resampling method of

Felsenstein (1985) with 1,000 replicates.

Results and discussion

Phenotypic characteristics

Morphological observation of 14–28 day old cultures

of strain EGI 80050T revealed that substrate mycelia

were abundant, well developed and not fragmented,

while long spore chains, sparsely borne on the aerial

mycelia, were straight to flexuous and non-motile

(Fig. 1). Strain EGI 80050T was observed to grow well

on ISP2, ISP5 and Cazpek’s agar, weakly on ISP3,

PDA and nutrient agar, while no growth was observed

on ISP4. Soluble pigments (moderate yellow) were

produced only on ISP2 among the tested media. The

colours of the aerial and substrate mycelia of the strain

were variable on the media used in the study (Table 1).

The strain EGI 80050T was found to be able to grow

at pH 7.0–11.0, 0–7.5 % NaCl and 10–40 �C. Optimal

growth was observed at pH 9.0–10.0, 2.5–5.0 % NaCl

and 30 �C. The strain was determined to be positive for

oxidase, urease, gel liquefaction and nitrate reduction,

while negative for catalase and production of H2S. The

strain was found to degrade Tween 20, Tween 40,

Tween 60 and Tween 80, but not starch and tryptophan.

The differential characteristics of the strain EGI 80050T

Fig. 1 Scanning electron micrographs (a, b) of the aerial mycelia of strain EGI 80050T grown on Horikoshi-I medium adjusted pH to

10.0 for 4 weeks at 30 �C. Bar, 10 lm

Antonie van Leeuwenhoek (2013) 104:1227–1233 1229

123

and its closely related reference type strains are shown

in Table 2, while the detailed characteristics of the

strain are given in the species description.

Chemotaxonomic characteristics

Strain EGI 80050T was found to contain LL-diamino-

pimelic acid (DAP). Whole-cell hydrolysates contained

galactose, glucose, rhamnose and mannose as the major

sugars. The polar lipid profile contained diphosphatidyl-

glycerol, phosphatidylglycerol, phosphatidylinositol,

phosphatidylinositol mannosides, phosphatidylmethyl-

ethanolamine and three unknown phospholipids (Fig.

S1). The predominant menaquinones were identified as

MK-9(H6) (74.7 %) and MK-9(H8) (23.0 %). The major

fatty acids identified ([10 %) were iso-C16:0 (36.8 %),

anteiso-C15:0 (17.3 %), iso-15:0 (13.2 %), iso-14:0 and

(10.5 %). A detailed comparison of fatty acid profiles of

the strains EGI 80050T, Streptomyces cinereoruber

subsp. cinereoruber DSM 40279T and Streptomyces

violaceorectus DSM 41512T is given in Table 3. The

DNA G?C content of strain EGI 80050T was deter-

mined to be 67.9 mol%.

Phylogenetic analysis

The almost complete 16S rRNA gene sequence

(1,528 bp) was determined for strain EGI 80050T

(GenBank accession number KF040416). Phylogenetic

analysis based on the 16S rRNA gene sequences

showed that the strain is related to members of the

genus Streptomyces. Strain EGI 80050T showed the

highest 16S rRNA gene sequence similarities to

Streptomyces candidus NRRL ISP-5141T (96.7 %),

Streptomyces cremeus NBRC 12760T (96.6 %), Strep-

tomyces spiroverticillatus NBRC 12821T (96.6 %), S.

violaceorectus NBRC 13102T (96.6 %) and S. cinere-

oruber subsp. cinereoruber NBRC 12756T (96.6 %).

The sequence similarities between strain EGI 80050T

and other members of the genus Streptomyces were

below 96.6 %. The phylogenetic analysis showed that

strain EGI 80050T forms a distinct clade that was

different from other closely related species of the genus

Streptomyces (Fig. 2). This distinction was supported

by all tree-making methods used in this study (Figs. S2

and S3). The closest related species were identified as S.

cinereoruber subsp. cinereoruber DSM 40279T and S.

violaceorectus DSM 41512T, the latter of which was

placed in clade 46 by Labeda et al. (2012). The results

of the 16S rRNA gene sequence comparison demon-

strated that strain EGI 80050T is a new species forming

a distinct clade within the genus Streptomyces.

On the basis of phenotypic, chemotaxonomic and

phylogenetic analysis, strain EGI 80050T was found to

exhibit the typical characteristics of the genus Strep-

tomyces: abundant and not-fragmented substrate

mycelium, well developed aerial hyphae; the cell wall

amino acid (LL-diaminopimelic acid); whole-cell sug-

ars (galactose, glucose, rhamose and mannose) and the

predominant menquinones [MK-9(H6) and MK-

9(H8)]. However, strain EGI 80050T possesses some

different characteristics from its closest phylogenetic

neighbours S. violaceorectus DSM 40279T and

S. cinereoruber subsp. cinereoruber DSM 41512T,

the details of which are given in Table 3.

Based on the characteristics from the phenotypic,

chemotaxonomic and phylogenetic analysis described

above, it is concluded that strain EGI 80050T is a

Table 1 Cultural characteristics of strain EGI 80050T

Mediaa Growth Aerial mycelium color Substrate mycelium color Diffusible pigment

Yeast extract-malt extract agar (ISP2) Good Purple orange-yellow Dark orange-yellow Moderate yellow

Oatmeal agar (ISP3) Weak –b Moderate yellow brown None

Inorganic starch agar (ISP4) – – – –

Glycerol-asparagine agar (ISP5) Good Strong olive-green Purple orange-yellow None

Czapek’s agar Good Purple orange-yellow Light orange-yellow None

Nutrient agar Weak Greenish yellow-gray Purple orange-yellow None

Potato-dextrose-agar Weak Yellow white Moderate yellow brown None

Gauze No. 1 Weak – Moderate yellow brown None

a All media were adjusted to pH 10.0b – not observed or no growth

1230 Antonie van Leeuwenhoek (2013) 104:1227–1233

123

representative of a novel species in the genus Strep-

tomyces. The name Streptomyces fukangensis sp. nov.

is proposed for the new species.

Description of Streptomyces fukangensis sp. nov.

Streptomyces fukangensis [fu.kang.ensis. N.L. masic.

adj. fukangensis pertaining to Fukang (Xinjiang,

China), where the type strain was isolated].

Gram-positive, aerobic actinomycete. Substrate

mycelia are abundant, well-developed and not frag-

mented. While the aerial mycelia are sparse and not

fragmented, long spore chains, borne on the aerial

mycelia, are straight to flexuous and non-motile.

Orange-yellow to olive-green aerial mycelia and

orange-yellow to yellow-brown substrate mycelia.

Diffusible moderate yellow pigment is produced only

on ISP2. Grows well on ISP2, ISP5 and Cazpek’s agar,

weakly on ISP3, PDA and nutrient agar, but not on ISP4.

Growth occurs at pH 6.0–11.0, 0–7.5 % NaCl, and

10–40 �C, with optimal growth at pH 9.0-10.0, 30 �C in

the presence of 2.5 % (w/v) NaCl. Utilizes trisodium

Table 2 Characteristics that distinguish strain EGI 80050T

from its closest phylogenetic neighbours Streptomyces cine-

reoruber subsp. cinereoruber DSM 40279T and Streptomyces

violaceorectus DSM 41512T

Characteristics 1 2 3

Morphology

Aerial

mycelium

Sparse Abundanta Abundanta

Diffusible

pigments

Moderate

yellow

Melanoid, yellow to

pinkish brown

pigmenta

Only

melanoida

Growth at

pH range 7.0–11.0 6.0–9.0 6.0–9.0

Optimal pH 9.0–10.0 7.0–8.0 7.0–8.0

NaCl

tolerance

(w/v, %)

7.5 5.0 5.0

Optimal

NaCl

(w/v, %)

2.5 0 0

Temperature

range (�C)

10–40 10–50 10–45

Physiology

Production of

H2S

- ? ?

Catalase ? - ?

Urease ? - -

Growth on sole carbon source

L-Arabinose - ? ?

D-Galactose - ? ?

Glycerol - ? ?

D-Xyluose - ? ?

Growth on sole nitrogen source

D-Arginine ? - ?

L-Tryptophan ? - ?

Glutamic

acid

- - ?

Predominant menaquinone

MK-9(H6) 74.6 30.9 49.7

MK-9(H8) 23.0 66.9 48.5

All the test strains showed positive resultsforgel liquefaction,

nitrate reduction, Tweens 20, 40, 60 and 80 degradation, while

negative results for oxidase test and tyrosine hydrolysis were

recorded. All of them could utilize sodium acetate, D-(?)-

cellobiose, D-fructose, inosiol, D-mannose, D-raffinose, trehalose,

D-mannitol, D-ribose, sodium oxalate, soluble starch, L-alanine, L-

asparagine, L-glycine, L-histidine, hypoxanthine, L-lysine, L-

methionine, L-phenylalanine, L-serine and L-tyrosine as either sole

C or N sourcesa Data from Kampfer (2012)

Strains: 1 EGI 80050T, 2 DSM 40279T, 3 DSM 41512T

? positive, utilized; - negative, not utilized

Table 3 Detailed comparison of cellular fatty acids of strain

EGI 80050T, Streptomyces cinereoruber subsp. cinereoruber

DSM 40279T and Streptomyces violaceorectus DSM 41512T

Fatty acids 1 2 3

14:0 iso 10.5 7.5 7.0

15:0 iso 13.2 11.4 10.9

15:0 anteiso 17.3 25.5 25.2

16:1 iso H 1.9 1.2 1.6

16:0 iso 36.6 26.4 24.4

16:00 5.6 6.8 6.3

17:1 anteiso x9c ND ND 1.2

17:0 iso 3.1 7.2 6.3

17:0 anteiso 4.6 10.2 10.9

C17:0 cyclo 1.0 0.2 0.4

Sum in feature 3a 1.0 0.6 1.6

Sum in feature 9a 1.2 0.7 1.4

All data are from the present study in which all strains were

cultured in Trypticase Soy Broth, except pH adjusted to 10.0

with 10 N NaOH for cultivation of EGI 80050T. Strains: 1 EGI

80050T, 2 DSM 40279T, 3 DSM 41512T. Values were

percentages of total fatty acids, ND, not detecteda Summed features represent two or three fatty acids that can

not be separated by the Microbial Identification System.

Summed Feature 3, 16:1 x7c/16:1 x6c, 16:1 x6c/16:1 x7c.

Summed Feature 9, 17:1 iso x9c, 16:0 10-methyl

Antonie van Leeuwenhoek (2013) 104:1227–1233 1231

123

citrate, D-glucose, L-rhamnose, sucrose and xylitol;

weakly utilizes sodium acetate, D(?)-cellobiose, D-

fructose, inosiol, D-mannitol, D-mannose, sodium oxa-

late, D-raffinose, D-ribose, soluble starch and trehalose;

while L-arabinose, dulcitol, D-galactose, glycerol and D-

xylose are not utilised. Utilizes L-alanine, D-arginine, L-

asparagine, L-glycine, L-histidine, hypoxanthine, L-

lysine, L-methionine, L-phenylalanine, L-serine, L-tyro-

sine and L-tryptophan as the sole nitrogen sources, but

not D-glutamic acid. Positive for oxidase, urease, gelatin

liquefaction and nitrate reduction, but negative for

catalase activity and production of H2S. Hydrolyzes

Tweens 20, 40, 60 and 80. Contains LL-diaminopimelic

acid (LL-DAP), galactose, glucose, mannose and rham-

nose in the whole-cell hydrolysates. The polar lipids

consist of diphosphatidylglycerol, phosphatidylglyc-

erol, phosphatidylinositol, phosphatidylinositol manno-

sides, phosphatidylmethylethanolamine and three

unknown phospholipids. The menaquinone system

comprises MK-9(H6) and MK-9(H8). The major fatty

acids include iso-C16:0, anteiso-C15:0, iso-15:0 and iso-

14:0. The G?C content of the genomic DNA of the type

strain is 67.9 mol%.

The type strain is EGI 80050T (=BCRC

16945T = JCM 19127T) isolated from a saline-alkaline

soil collected from Fukang, Xinjiang, north-west China.

The 16S rRNA gene sequence of strain EGI 80050T has

been deposited in GenBank under the accession number

KF040416.

Acknowledgments The authors are grateful to Dr. Hans-Peter

Klenk (DSMZ) for providing the reference type strains. This

research was supported by the Hundred Talents Program of

Chinese Academy of Sciences and the West Light Foundation of

Chinese Academy of Sciences (RCPY201203).

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