Antonie van Leeuwenhoek DOI 10.1007/s10482-014-0301-6

ORIGINAL PAPER

Streptomyces ferrugineus sp. nov., isolated from mangrove soil in Thailand Chang-ying Ruan • Li Zhang • Wan-wan Ye • Xiu-chao Xie • Rattanaporn Srivibool Kannika Duangmal • Wasu Pathom-aree • Zi-xin Deng • Kui Hong

•

Received: 14 July 2014 / Accepted: 6 October 2014 Ó Springer International Publishing Switzerland 2014

Abstract Bacterial strain HV38T was isolated from mangrove soil, which was collected from Thailand. Chemotaxonomic and morphological characteristics were found to be typical of members of the genus Streptomyces. The strain was found to form a distinct phyletic line in the Streptomyces 16S rRNA gene tree and to be closely associated with the type strains of Streptomyces coeruleofuscus CGMCC 4.1667T (98.84 % sequence similarity), Streptomyces chromofuscus CGMCC 4.1451T (98.63 %) and Streptomyces albidoflavus CGMCC 4.1291T (98.56 %). The major menaquinones were identified as MK-9(H8) and MK-

9(H10). Its major cellular fatty acids were found to be iso-C14:0, iso-C15:0, anteiso-C15:0, iso-C16:1x8c, C16:0, anteiso-C16:1x8c, iso-C16:0 and anteiso-C16:0. The DNA–DNA hybridization values between strain HV38T with S. coeruleofuscus CGMCC 4.1667T, S. chromofuscus CGMCC 4.1451T and S. albidoflavus CGMCC 4.1291T were 32.7 ± 0.9, 21.8 ± 0.3 and 19.9 ± 0.9 %, respectively, which clearly supported the conclusion that they belong to separate genomic species. Cumulatively, the data indicated that strain HV38T represents a novel species of the genus Streptomyces, for which the name Streptomyces ferrugineus sp. nov. is proposed. The type strain is HV38T (=CCTCC AA2014009T = DSM 42152T).

The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequence of strain HV38T is KF767859.

Keywords Streptomyces ferrugineus sp. nov.  Polyphasic taxonomy  Mangrove soil

Electronic supplementary material The online version of this article (doi:10.1007/s10482-014-0301-6) contains supplementary material, which is available to authorized users. C. Ruan  X. Xie (&) Shaanxi Engineering Research Center of Edible and Medicated Fungi, School of Bioscience and Engineering, Shaanxi University of Technology, Hanzhong 723000, People’s Republic of China e-mail: [email protected] C. Ruan  L. Zhang  W. Ye  Z. Deng  K. Hong (&) Key Laboratory of Combinatorial Biosynthesis and Drug Discovery (Wuhan University), Ministry of Education, Wuhan University School of Pharmaceutical Sciences, Wuhan 430071, People’s Republic of China e-mail: [email protected]

R. Srivibool Institute of Marine Science, Burapha University, Chonburi 20131, Thailand K. Duangmal Department of Microbiology, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand W. Pathom-aree (&) Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand e-mail: [email protected]

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Introduction The genus Streptomyces was first described by Waksman and Henrici 1943 and is the type genus of the family Streptomycetaceae. It is one of the largest genera within the phylum Actinobacteria (Ka¨mpfer and Labeda 2006; Lodders and Ka¨mpfer 2007). Members of the family Streptomycetaceae include the genera Streptomyces, Kitasatospora (Zhang et al. 1997) and Streptacidiphilus (Kim et al. 2003). At the time of writing, more than 600 validly named species (List of Prokaryotic Names with Standing in Nomenclature; http://www.bacterio.cict.fr/) have been described in the genus Streptomyces. Mangroves are woody plants located in tropical and subtropical intertidal coastal regions, which are considered to be productive environments for the isolation of actinomycetes (Hong et al. 2009). Mangroves have been a rich source of actinomycetes and the discovery of members of at least 25 genera, 11 families and 8 suborders have been reported in the last decade (Hong 2013), including several novel species of Streptomyces, such as Streptomyces sanyensis (Sui et al. 2011), Streptomyces shenzhenensis (Hu et al. 2011) and Streptomyces qinglanensis (Hu et al. 2012). Additionally, many natural products have been isolated from mangrove actinomycetes, including alkaloids, benzene derivatives, cyclopentenone derivatives, dilactones, macrolides, 2-pyranones and sesquiterpenes (Xu et al. 2014). Therefore, collecting and exploring the actinobacteria from mangrove is both of high interest and important for both biotechnology and for understanding microbial diversity. In this study, we report the isolation of an actinomycete strain, HV38T, from mangrove soil collected in Thailand and its polyphasic taxonomic characterization as a novel member of the genus Streptomyces, for which the name Streptomyces ferrugineus sp. nov. is proposed.

cycloheximide (50 mg/L) and nystatin (30 mg/L). After 5–7 days of aerobic incubation at 28 °C, it formed a yellowish colony and produced a fuchsia pigment. Aerial mycelia were white and undeveloped. The single colony was transferred, purified and maintained on yeast extract-malt extract (ISP 2) agar medium (Shirling and Gottlieb 1966). Abundant biomass of a pure culture on ISP 2 agar was collected for long-term preservation as mycelia and spore suspensions in glycerol (20 %, v/v) at -80 °C. The reference strains Streptomyces coeruleofuscus CGMCC 4.1667T (=NBRC 12757T), Streptomyces chromofuscus CGMCC 4.1451T (=NBRC 12851T) and Streptomyces albidoflavus CGMCC 4.1291T (=DSM 40455T) were obtained from the China General Microbiological Culture Collection Centre (CGMCC). Phenotypic characterization The isolate HV38T and the reference strains were analyzed for cultural and morphological features after growth on several established media at 28 °C for 2–3 weeks using the method previously described by Shirling and Gottlieb (1966). Strain HV38T was cultured on oatmeal agar (ISP 3) medium at 28 °C for 15 days, then the morphological characteristics were observed by scanning electron microscopy (Hitachi, TM3000). The utilization of amino acids (0.5 % w/v final concentration) as nitrogen source was tested as described by Williams et al. (1983). Carbon source utilization was tested on ISP 9 medium supplemented with 1 % (w/v) carbon source (final concentration) (Shirling and Gottlieb 1966). The procedures of Williams et al. (1983) and Ka¨mpfer et al. (1991) were used to detect other biochemical and physiological characteristics, including hydrolysis of aesculin, production of catalase and H2S. Chemotaxonomy

Materials and methods Isolation and maintenance of organisms During a study on diversity of actinobacterial resources in mangrove soils in Thailand (13°300 2300 N; 101°00 1100 E), strain HV38T was isolated on Humic acid-vitamin agar (HV) medium (Hayakawa et al. 2004) supplemented with K2Cr2O7 (50 mg/L),

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Biomass for chemical systematic studies was harvested and washed after incubation at 28 °C for 3–5 days in shaken flasks (220 rpm) with yeast extract-malt extract broth (ISP 2). Whole-cell sugars and amino acids were analyzed by thin layer chromatography (TLC) as described previously (Lechevalier and Lechevalier 1980). Phospholipids were analyzed by two-dimensional TLC using the well-established

Antonie van Leeuwenhoek

method described by Minnikin et al. (1984). Menaquinones were determined following the procedure of Minnikin et al. (1984) and carried out by high performance liquid chromatography (HPLC) (Wang et al. 2011). Cellular fatty acids were extracted by the method of Sasser (1990) and the composition was determined by GC–MS performed on a GC instrument (7890A; Agilent) coupled with a mass selective detector (MS5975C; Agilent) and an auto-sampler injector (7693A; Agilent). A capillary column HP-5MS (5 % Phenyl Methyl Siloxane) with dimensions of 30 m 9 250 lm 9 0.25 lm (Agilent 19091N-133) was used for the separation of fatty acid methyl esters. The initial temperature of 100 °C was maintained for 5 min, raised to 240 °C at the rate of 10 °C min-1. Injected volume of sample was 1 lL and helium was used as a carrier gas at a flow rate of 0.8 ml min-1 without split. The temperatures of the injector and detector were 230 and 250 °C, respectively. The MS was operated in the electron multiplier voltage (EMV) mode at 988 V in the scan range of 50–400 m/z. NIST 08 MS library was used as the database for comparison. Menaquinones were extracted from freeze-dried biomass, purified according to Minnikin et al. (1984) and analyzed by HPLC with an ODS-BP C18 column (4.66250 mm). The elution solvent was methanol and 2-propanol (3:2, v/v) based on the method of Li et al. (2013).

followed by 30 cycles of denaturation (94 °C for 1 min), primer annealing (55 °C for 1.5 min) and primer extension (72 °C for 1.5 min). At the end of the cycle, the reaction mixture was kept at 72 °C for 10 min and then cooled to 4 °C. The almost-complete 16S rRNA gene sequence of strain HV38T was analyzed using public databases and the EzTaxon Cloud server (http://www.Eztaxon.org; Kim et al. 2012) to calculate the similarities. First, we constructed a large phylogenetic tree using the 16S rRNA gene sequence of strain HV38T and those of all of the type strains of validly named Streptomyces (n = 609). In this way, we obtained the ten most closely related strains to strain HV38T from the tree. Then we constructed another phylogenetic tree using the 16S rRNA gene sequences of those ten strains and ten other 16S rRNA gene sequences which have the highest similarity to strain HV38T, which were chosen from GenBank. The initial alignment was performed using CLUSTAL_X software (Thompson et al. 1997). Phylogenetic trees were obtained using the neighbourjoining (Saitou and Nei 1987), maximum-likelihood (Felsenstein 1985) (Supplementary Fig. S4) and maximum-parsimony (Fitch 1971) algorithms via MEGA 5.0 software (Tamura et al. 2011). Streptacidiphilus anmyonensis AM-11T (DQ904546) was used as the out group (Cho et al. 2008).

Phylogenetic analyses

Strain HV38T was isolated from a mangrove soil sample. The strain was observed to grow well on ATCC 172 agar, Czapek’s agar (CA), potato-glucose agar (PDA), ISP 2–ISP 4 and M8 agar media. However, it was found to grow poorly on ISP 5, ISP 6 and nutrient agar media. Strain HV38T was observed to produce a fushcia pigment on all media tested. Spore chains appeared as rectiflexibiles in nature and the spore (0.5 9 1.5 lm) surfaces are smooth and non-motile (Supplementary Fig. S1). The whole-cell sugars were found to contain glucose and ribose. The whole-cell wall amino acids were found to include alanine, glycine, LL-diaminopimelic acid (LLDAP) and a small amount of meso-diaminopimelic acid (meso-DAP) (Supplementary Fig. S2). The characteristic polar lipids were identified as diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol, phosphatidylinositol mannosides and unknown phospholipids

Genomic DNA was obtained by the method of Pospiech and Neumann (1995). The level of DNA– DNA relatedness between strain HV38T and its closest phylogenetic neighbours was measured on nylon membranes at 65 °C using the method described by Wang et al. (2011). The DNA G?C content of strain HV38T was determined by HPLC (Qu and Hong 2009) using standard bases as control. DNA for PCR was obtained using a Fast Pre-24 instrument (MP Biomedicals). The 16S rRNA gene was amplified using the PCR method with Taq DNA polymerase (Takara) and primers 27F (50 -AGAGTTTGATCCTGGCTCAG-30 ) and 1492R (50 -GGTTACCTTGTTACG ACTT-30 ). Amplification was carried out using a DNA thermal cycler (C1000TM; Applied Bio-RAD) according to the following program: 94 °C for 5 min

Results and discussion

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Antonie van Leeuwenhoek Table 1 Cellular fatty acid profile of strain HV38T compared with reference strains Fatty acid profiles

1

2

3

4

iso-C14:0

7.5

7.5

–

3.8

anteiso-C14:0

–

–

–

3.1

C15:0

–

43.6

39.4

–

iso-C15:0

6.8

12.3

36.7

24.1

anteiso-C15:0

26.1

–

–

27.5

iso-C16:1x8c

18.1

4.2

–

4.3

C16:0

24.8

1.4

12.7

3.2

anteiso-C16:1x8c

6.5

–

–

–

iso-C16:0

2.3

17.2

–

9.6

anteiso-C16:0

7.7

13.7

–

20.3

iso-C16:1

–

–

9.8

–

iso-C17:0

–

–

1.3

–

iso-C17:1

–

–

–

4.1

Taxa 1 HV38T (S. ferrugineus sp. nov.), 2 S. coeruleofuscus CGMCC 4.1667T, 3 S. chromofuscus CGMCC 4.1451T, 4 S. albidoflavus CGMCC 4.1291T. All data are from this study

(Supplementary Fig. S3). The major menaquinones were identified as MK-9(H8) (40.5 %) and MK-9(H10) (56.4 %), with small amounts of MK-9(H4) (0.2 %), MK-9(H6) (1.0 %), MK-10 (1.3 %) and MK-10(H6) (0.6 %). The major cellular fatty acids were determined to be iso-C14:0 (7.6 %), iso-C15:0 (6.8 %), anteiso-C15:0 (26.1 %), iso-C16:1x8c (18.1 %), C16:0 (24.8 %), anteisoC16:1x8c (6.5 %), iso-C16:0 (2.3 %) and anteiso-C16:0 (7.7 %) (Table 1). The DNA G?C content was determined to be 67.0 mol%. The almost-complete 16S rRNA gene sequence of strain HV38T (1,488 nt, GenBank/EMBL/DDBJ accession number KF767859) was compared with the 16S rRNA gene sequences of all members of the genus Streptomyces. The highest level of sequence similarity was found to be with S. coeruleofuscus NBRC 12757T (98.84 % similarity, =CGMCC 4.1667T), followed by S. chromofuscus NBRC 12851T (98.63 %, =CGMCC 4.1451T), Streptomyces somaliensis NRBC 12916T (98.57 %), Streptomyces

Table 2 Differential characteristics of strain HV38T and its closest relative strains. All data are from this study except where indicated Characteristic

1

2

3

4

Soluble pigment on ISP 2

Fuchsia

None

None

None

Menaquinones

MK-9(H4), MK-9(H6), MK-9(H8), MK-8(H4), MK-8(H8) and MK-10(H4)

ND

MK-9(H6), MK-9(H8) and MK-9(H10)*

ND

Polar lipids profile

DPG, PE, PI, PIM, PLS

ND

DPG, PE, PI, PIMs*

ND

Aesculin degradation

-

?

?

-

Cellulose decomposition

-

?

-

-

Catalase production

-

-

-

?

Nitrate reduction

-

?

-

-

Maximum NaCl tolerance

9%

4%

4%

5%

Growth at pH 12

?

-

?

-

Maximum temperature tolerance

40 °C

40 °C

45 °C

37 °C

Nitrogen utilization L-isoleucine

-

W

-

-

L-leucine

W

-

-

-

L-serine

?

W

W

-

Adonitol

?

?

W

W

D-raffinose

W

-

-

W

Uracil

?

-

?

Carbon utilization

T

T

W T

Taxa 1 HV38 (S. ferrugineus sp. nov.), 2 S. coeruleofuscus CGMCC 4.1667 , 3 S. chromofuscus CGMCC 4.1451 , 4 S. albidoflavus CGMCC 4.1291T DPG diphosphatidylglycerol, PE phosphatidylethanolamine, PI phosphatidylinositol, PIM phosphatidylinositol mannosides, PLS unknown phospholipids ? positive, - negative, W weakly positive, ND no data, * data from Promnuan et al. (2013)

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Antonie van Leeuwenhoek Streptomyces hydrogenans NBRC 13475T (AB184868) Streptomyces daghestanicus NRRL B-5418T (DQ442497) Streptomyces somaliensis NBRC 12916T (AB184243) 57* Streptomyces albidoflavus CGMCC 4.1291T (Z76676) 58* Streptomyces ferruginens HV38T (KF767859) Streptomyces coeruleofuscus CGMCC 4.1667T (AB184840) * 66* Streptomyces chromofuscus CGMCC 4.1451T (AB184194) Streptomyces malachitospinus NBRC 101004T (AB249954) 98* Streptomyces glaucescens NBRC 12774T (AB184843) 100* * Streptomyces pharetrae CZA14T (AY699792) Streptomyces nogalater JCM 4799T (AB045886) * Streptomyces cinerochromogenes NBRC 13822T (AB184507) Streptomyces achromogenes subsp. rubradiris NBRC 14000T (AB184561) Streptomyces rameus LMG 20326T (AJ781379) 70* T 100* Streptomyces tricolor LMG 20328 (AJ781380) Streptomyces bangladeshensis AAB-4T (AY750056) Streptomyces aurantiogriseus NBRC 12842T (AB184188) Streptacidiphilus anmyonensis AM-11T (DQ904546) * 75 100*

0.005

Fig. 1 Neighbour-joining phylogenetic tree based on nearly complete 16S rRNA gene sequences. The relationships between strain HV38T and the type strains of phylogenetically close species of the genus Streptomyces were analyzed. Streptacidiphilus anmyonensis AM-11T (DQ904546) was used as the out group (Cho et al. 2008). Asterisks indicate branches which were

also found using the maximum-likelihood (Felsenstein 1985) and maximum-parsimony (Fitch 1971) methods. Numbers at nodes are percentage bootstrap values based on 1,000 replicates; only values [50 % are shown. Bar 0.005 substitutions per nucleotide position

spinoverrucosus NRBC 14228T (98.56 %) and S. albidoflavus DSM 40455T (98.56 %, =CGMCC 4.1291T). Based on a large phylogenetic tree of the type strains of Streptomyces species (n = 609), the sequences of ten closely related type strains were chosen, together with the next ten type strains with the highest 16S rRNA gene sequence similarity obtained from EzTaxon. The sequences were used to construct a neighbour-joining phylogenetic tree (Fig. 1) which demonstrated the relationship of strain HV38T to closely related Streptomyces species. Furthermore, DNA–DNA hybridization was tested between strain HV38T and S. coeruleofuscus CGMCC 4.1667T, S. chromofuscus CGMCC 4.1451T and S. albidoflavus CGMCC 4.1291T giving values of 32.7 ± 0.9, 21.8 ± 0.3, and 19.9 ± 0.9 %, respectively, which are well below the 70 % cut-off value for delineating novel prokaryotic species (Wayne et al. 1987). Other phenotypic and chemotaxonomic profiles are shown in Table 2. It is evident that strain HV38T can be distinguished from previously described species of the genus Streptomyces. On the basis of the combination of cultural characteristics, chemotaxonomic properties, phenotypic and genotypic data, it can be concluded that strain HV38T represents a novel species of the genus

Streptomyces, for which the name Streptomyces ferrugineus sp. nov. is proposed. Description of Streptomyces ferrugineus sp. nov. Streptomyces ferrugineus (fer.ru.gi’ne.us. L. masc. adj. n. ferrugineus, pertaining to the colour of the soluble pigment). Produces extensively branch substrate hyphae after cultivation for 2–3 weeks at 28 °C on ISP 3 agar medium. The aerial mycelia are white but undeveloped. A fuchsia coloured diffusible pigment is produced on all agar media tested in the present study. The pH and NaCl tolerance ranges for growth are 5.0–13.0 (optimum, pH 7.0) and 0–9 % (optimum, 2 %), respectively. The temperature range for growth is from 10 to 40 °C, with optimum growth temperature of 32 °C. L-arginine, L-glutamine, L-histidine, L-lysine, Lproline, L-serine and L-threonine are utilised as sole nitrogen source; glycine, L-isoleucine, L-leucine, Lmethionine and L-valine are weakly utilized; N-acetylL-cysteine, L-aspartic acid, L-glutamic, L-phenylalanine and L-tyrosine are not utilised. Can utilise adonitol, L-arabinose, D-cellobiose, D-fructose, inositol, D-galactose, D-lactose, maltose, D-mannitol, Dmannose, D-melezitose, melibiose, D-salicin, L-rhamnose, D-ribose, D-trehalose, uracil, D-xylose, and can

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weakly utilise D-raffinose but cannot utilise succinic acid as sole carbon source. The whole-cell wall amino acids contain alanine, glycine, LL-diaminopimelic acid (LL-DAP) and a small amount of meso-diaminopimelic acid (meso-DAP). The whole-cell sugars are glucose and ribose. The major cellular fatty acids include iso-C14:0, iso-C15:0, anteiso-C15:0, iso-C16:1x8c, C16:0, anteiso-C16:1x8c, iso-C16:0 and anteiso-C16:0. The polar lipids include diphosphatidylglycerol, phosphatidylethanolamine, phosphatidylinositol, phosphatidylinositol mannosides and unknown phospholipids. The major menaquinones are MK-9(H8), MK9(H10), with small amounts of MK-9(H4), MK-9(H6), MK-10 and MK-10(H6). The DNA G?C content of the type strain is 67.0 mol%. The type strain HV38T (=CCTCC AA2014009T = DSM 42152T) was isolated from mangrove soil collected from Thailand. The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain HV38T is KF767859. Acknowledgments Kui Hong, Wasu Pathom-aree, Kannika Duangmal and Rattanaporn Srivibool are grateful for the financial support from the NSFC (31111140297)-NRCT Grant for the Thai–Chinese Cooperative Project, ‘‘Actinomycetes from coastal marine and mangrove sediments of Eastern Thailand and their ability to produce bioactive compounds’’ and for the Chinese MOST-TICA Sino–Thai Joint Research and Development Project, ‘‘Selective isolation and prepharmaceutical research on novel and rare actinomycetes from tropical marine and terrestrial habitats’’ (19-505J).

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