Streptomyces Manipurensis Sp. Nov., a Novel Actinomycete Isolated from a Limestone Deposit Site in Manipur, India

Antonie van Leeuwenhoek (2012) 102:133–139 DOI 10.1007/s10482-012-9720-4

ORIGINAL PAPER

Streptomyces manipurensis sp. nov., a novel actinomycete isolated from a limestone deposit site in Manipur, India

Salam Nimaichand • Wen-Yong Zhu • Ling-Ling Yang • Hong Ming • Guo-Xing Nie • Shu-Kun Tang • Debananda S. Ningthoujam • Wen-Jun Li

Received: 1 February 2012 / Accepted: 3 March 2012 / Published online: 16 March 2012 Ó Springer Science+Business Media B.V. 2012

Abstract A novel actinobacterium, designated % and strain MBRL 201T showed closest similarities to MBRL 201T, was isolated from a sample collected Streptomyces virginiae NBRC 12827T (99.6 %) and from a limestone quarry at Hundung, Manipur, India. Streptomyces cinnamonensis NBRC 15873T (99.6 %). The strain was characterized using polyphasic taxon- The DNA relatedness between MBRL 201T and the omy. Comparison of the 16S rRNA gene sequence of type strains of S. virginiae NBRC 12827T and strain MBRL 201T and other Streptomyces species S. cinnamonensis NBRC 15873T were 44.5 and 35.6 % T showed sequence similarities ranging from 93.0 to 99.6 respectively. Strain MBRL 201 contained LL-diamino-

pimelic acid (A2pm) as the diagnostic diamino acid, with glucose as the main sugar, while small amounts of galactose, glucose, mannose, rhamnose, ribose and Electronic supplementary material The online version of xylose were also present in cell-wall hydrolysates. The this article (doi:10.1007/s10482-012-9720-4) contains major fatty acids identiﬁed were anteiso-C15:0 (38.9 %), supplementary material, which is available to authorized users. iso-C15:0 (19.9 %) and anteiso-C17:1 (14.7 %). The S. Nimaichand Á W.-Y. Zhu Á L.-L. Yang Á predominant menaquinones detected were MK-9(H6) H. Ming Á S.-K. Tang Á W.-J. Li (&) and MK-9(H8), while the polar lipids were diphosphat- Key Laboratory of Microbial Diversity in Southwest idylglycerol, phosphatidylmethylethanolamine, phos- China, Ministry of Education, and Laboratory for phatidylglycerol, phosphatidylethanolamine, Conservation and Utilization of Bio-Resources, Yunnan Institute of Microbiology, Yunnan University, Kunming phosphatidylinositol and phosphatidylinositolmanno- 650091, People’s Republic of China sides, with other unknown phospholipids and lipids. e-mail: [email protected] The G?C content of the genomic DNA was 72.9 %. The phenotypic and genotypic data showed that strain MBRL S. Nimaichand Á D. S. Ningthoujam T Microbial Biotechnology Research Laboratory, 201 merits recognition as a representative of a novel Department of Biochemistry, Manipur University, species of the genus Streptomyces. It is proposed that the Canchipur, Imphal 795003, Manipur, India isolate should be classiﬁed in the genus Streptomyces as a novel species, Streptomyces manipurensis sp.nov.The H. Ming T T Department of Life Sciences and Technology, type strain is MBRL 201 (=DSM 42029 = JCM T Xinxiang Medical University, 17351 ). Xinxiang 453003, People’s Republic of China

G.-X. Nie College of Life Sciences, Henan Normal University, Keywords Streptomyces manipurensis sp. nov. Á Xinxiang 453007, People’s Republic of China Hundung Á Limestone quarry 123 134 Antonie van Leeuwenhoek (2012) 102:133–139

Introduction Strain MRBL 201T was preserved as lyophilized spore suspensions in skim milk at room temperature and as The genus Streptomyces was proposed by Waksman glycerol suspensions (20 %, v/v) at -80 °C. and Henrici (1943) and emended subsequently by Rainey et al. (1997) and Kim et al. (2003). The genus is Phenotypic characteristics placed in the family Streptomycetaceae of the suborder Streptomycineae (Stackebrandt et al. 1997; Zhi et al. To observe its morphological characteristics, strain 2009). The genus is characterized by presence of high MBRL 201T was cultivated aerobically on SCNA DNA G?C content, formation of extensively branched (28 °C) for 2 weeks. Morphology of spores and substrate and aerial mycelia, the presence of mycelia was observed by using light microscopy LL-diaminopimelic acid (LL-DAP) and absence of (Olympus BH2) and scanning electron microscopy characteristic sugars in the cell wall (cell wall type I, (SEM) (Quanta 200, FEI). Growth on various Inter- Lechevalier and Lechevalier 1970) (Anderson and national Streptomyces Project (ISP, Shirling and Wellington 2001). The genus continues to be the major Gottlieb 1966) media, tryptic soy agar (TSA, Difco), source of antimicrobial metabolites including antibi- SCNA, Czapek’s agar and Nutrient agar (NA) were otics to date (Ningthoujam et al. 2009). At the time of observed. The colony color was determined using the writing, there are 597 validly published Streptomyces ISCC-NBS color chart (Kelly 1964). Utilization of species, containing 38 subspecies (Euzeby 2012; http:// sole carbon and nitrogen sources was determined as www.bacterio.cict.fr/s/streptomycesa.html). Labeda described by Shirling and Gottlieb (1966). Tests for et al. (2012) presented an overview on the phylogeny of decomposition of casein and tyrosine, and acid different species included in the family Streptomycet- production from carbohydrates were performed fol- acea, and showed, through analysis of the 16S rRNA lowing the methods of Gordon et al. (1974). Hydro- gene sequences, the presence of 615 taxa within the lysis of starch, gelatin and Tweens 20, 40, 60 and 80 family. The study presents the polyphasic character- was determined as described by Collins et al. (2004). ization of a novel strain, MBRL 201T, which we pro- Nitrate reduction was monitored as described by Lanyi pose as representative of a novel species of the genus (1987). Growth at different temperatures (5, 15, 28, Streptomyces. 37, 42, 50 and 60 °C), pH (4–10) and NaCl concen- trations (0, 2, 5, 7 and 10 % w/v) was determined on TSA as described by Goodfellow (1986). Catalase Materials and methods activity was observed by assessing bubble production

in 3 % (v/v) H2O2. Other biochemical tests including Strains and culture conditions Voges–Proskauer, methyl red and the production of indole were performed as described by Goodfellow Strain MBRL 201T was isolated from a soil sample (1986). collected from a limestone quarry at Hundung, Man- ipur, India (25.05°N, 94.33°E) on Starch Casein Chemotaxonomy Nitrate Agar (SCNA, Kuster and Williams 1964) adjusted to pH 8.5 as the selective isolation medium. The amino acid content of the cell wall were Soil samples were air-dried for a week, crushed and determined according to Staneck and Roberts (1974) sieved. One gram of the sieved soil was treated with and the sugars of the whole cell hydrolysates were 0.1 g CaCO3 for 1 day to prevent the growth of fast analyzed as described by Tang et al. (2009). For other growing bacteria. It was then suspended in 99 mL chemotaxonomic analyses, strain MBRL 201T was sterile distilled water and kept in an orbital shaker at grown on tryptic soy broth (TSB, Difco) for 1 week 150 rpm for 30 min. The suspension was centrifuged (250 rpm, 28 °C). Cell biomass was harvested by (1,6009g; 10 min) and 0.1 mL of the supernatant was centrifugation, washed with distilled water and lyoph- decimally diluted. 0.1 mL each of the diluted samples ilized. Polar lipids were extracted and analyzed by was spread on SCNA plates (pH 8.5) and incubated at two-dimensional TLC as described by Minnikin et al. 28 °C for 1 week. The isolates obtained were subcul- (1984). The extraction of menaquinones was per- tured in the same medium to obtain pure cultures. formed as described by Collins et al. (1977) and 123 Antonie van Leeuwenhoek (2012) 102:133–139 135 analyzed by HPLC (Tamaoka et al. 1983). Cellular triplicate by the thermal renaturation method (DeLey fatty acids were extracted, methylated and analyzed by et al. 1970) using Lambda 35 UV/Vis Spectropho- using the Sherlock Microbial Identification System tometer (Perkin Elmer) equipped with PTP 6?6 (MIDI) according to the method of Sasser (1990) and Peltier Temperature Programmer (Perkin Elmer) and the manufacturer’s instructions. The fatty acid methyl BG-chiller E15 (Baygene Biotech Company Limited). esters were then analysed by GC (Agilent Technolo- gies 7890A GC System) by using the Microbial Identification software package (Sherlock Version Results and discussion 6.1; MIDI database: TSBA6). Strain MBRL 201T formed extensive substrate and Molecular analysis aerial mycelia with long conidia (approximately 70 spores). At maturity, the strain formed rectiflexibile Genomic DNA isolation and PCR amplification of the spore chains. A scanning electron micrograph dem- 16S rRNA gene was done as described by Li et al. onstrating the aerial mycelia for strain MBRL 201T is (2007). The almost complete 16S rRNA gene shown in Fig. 1. The strain grew well in all the media sequence (1523 bp) of the strain was submitted to tested with no pigmentation (Table 1). The strain was EzTaxon server (Chun et al. 2007) and aligned with found to be able to hydrolyze tyrosine, starch (weakly) the 16S rRNA gene sequences of other Streptomyces and Tweens 20, 40, 60 and 80 but not casein and species using CLUSTAL X version 2.1 (Larkin et al. gelatin. The strain was positive for catalase and indole 2007). Phylogenetic analyses were performed using production tests but negative for methyl red, Voges– the software package MEGA version 5.0 (Tamura Proskauer, citrate utilization and nitrate reduction et al. 2011). Distances (using distance options accord- tests. The differentiating properties of strain MBRL ing to Kimura’s two-parameter model; Kimura 1983) 201T from the related type strains Streptomyces were calculated and clustering was performed with the virginiae NBRC 12827T and Streptomyces cinnamon- neighbor-joining (NJ) method (Saitou and Nei 1987). ensis NBRC 15873T are listed in Table 2 and other To determine the support of each clade, bootstrap phenotypic characteristics are mentioned in the spe- analysis was performed with 1,000 resamplings (Fel- cies description. T senstein 1985). The validity of the NJ tree was Strain MBRL 201 had LL-diaminopimelic acid evaluated with the maximum parsimony (MP) tree (A2pm) as the diagnostic cell wall diamino acid, (Kluge and Farris 1969) drawn using MEGA 5.0. The Glucose was the main sugar detected in the whole cell G?C content of the genomic DNA was determined hydrolysates along with small amounts of galactose, according to the method described by Mesbah et al. mannose, rhamnose, ribose and xylose. The major (1989). DNA–DNA relatedness was studied in polar lipids detected were diphosphatidylglycerol,

Fig. 1 Scanning electron micrographs for strain MBRL 201T grown on SCNA medium for 2 weeks at 28 °C, a bar 5 lm and b bar 30 lm 123 136 Antonie van Leeuwenhoek (2012) 102:133–139

T Table 1 Culture characteristics of MBRL 201T on different 15873 , were selected for DNA–DNA hybridization ISP and other selective media as observed using ISCC-NBS studies. The experiments showed that strain MBRL Color Chart (Kelly 1964) 201T displayed low DNA–DNA reassociation values Medium Colour of mycelium Soluble with S. virginiae NBRC 12827T (44.5 ± 3.1 %) and pigment T Aerial (spore Substrate S. cinnamonensis NBRC 15873 (35.6 ± 2.2 %), mass) thereby indicating that the whole genomic DNA relatedness values are well below the delineating 70 ISP2 Grey brown Brown – % cut-off point for species identiﬁcation (Wayne et al. ISP3 Grey brown Grey – 1987). Based on its morphological characteristics and ISP4 White Yellow white – 16S rRNA gene sequence analysis results, the new ISP5 Yellow brown Yellow brown – species should be put in the cluster 39 which was a ISP6 Grey N.D. – identiﬁed by Labeda et al. (2012). ISP7 Yellow pink Brown – The genotypic and phenotypic features described NA Grey Orange yellow – above suggest that strain MBRL 201T could be clearly Czapek’s Yellow pink Orange yellow – distinguished from its closest phylogenetic relatives. SCNA Reddish brown Yellow brown – Besides low DNA–DNA relatedness with the closest TSA Yellow brown Yellow brown – phylogenetic neighbors, the strain is also distinguished a The result was not determined due to deep colour from media from them by several phenotypic properties as listed in Table 2. Therefore, the Hundung strain MBRL 201T is considered to represent a new species of the genus Streptomyces, for which the name Streptomyces phosphatidylmethylethanolamine, phosphatidylglyc- manipurensis sp. nov., is proposed. erol, phosphatidylethanolamine, phosphatidylinositol and phosphatidylinositolmannoside, with other unknown phospholipids and lipids (see Supplementary Fig. S1). Description of Streptomyces manipurensis sp. nov.

MK-9(H6) and MK-9(H8) were the predominant menaquinones detected. The fatty acid methyl ester proﬁle Streptomyces manipurensis (ma.ni.pur.en’sis. N.L.

([1 %) contained anteiso-C15:0 (38.9 %), iso-C15:0 (19.9 masc. adj. manipurensis pertaining to Manipur, a state %), anteiso-C17:1 (14.7 %), C16:0 (7.7 %), iso-C17:0 (6.6 in North East India, the source of the soil from which %), iso-C16:0 (6.5 %), iso-C14:0 (1.1 %), and Sum in the type strain was isolated). Feature 9 containing C16:1x7c/C16:1x6c (1.0 %). Gram-stain positive, aerobic and spore forming with The G?C content of the genomic DNA was 72.9 %. conidia containing up to approximately 70 spores. EzTaxon sequence similarity results showed that the Rectiﬂexibile spore chains, and each spore on maturity strain MBRL 201T has close 16S rRNA gene sequence measures 0.6–1 lm in diameter. Growth occurs at homologies ([97 %) with 209 Streptomyces type 15–37 °C and pH 6–10, with optimum growth at strains. Combining EzTaxon analysis and phyloge- 28 °C and pH 8. Growth occurs in presence of up to 2 netic neighbour-joining tree (Fig. 2) results indicated % NaCl. Utilizes L-arabinose, D-cellobiose, fructose, T that strain MBRL 201 is closely related to S. virginiae D-galactose, maltose, D-mannose, rafﬁnose, ribose, NBRC 12827T and S. cinnamonensis NBRC 15873T sodium malate and succinic acid as sole carbon sources; (16S rRNA gene sequence similarities of 99.66 and and L-alanine, L-arginine, L-asparagine, glycine, L-histidine, 99.66 %, respectively) and this phylogenetic relation- L-hydroxyproline, L-leucine, potassium nitrate, proline, ship was also supported in the tree generated with the L-serine, L-tryptophan and L-tyrosine as sole nitrogen MP algorithm with higher bootstrap values (see sources. Does not utilize dulcitol, meso-inositol, lactose, Supplementary Fig. S2). Streptomyces strains sharing mannitol, rhamnose, L-sorbose, trehalose, xylitol, [99.5 % 16S rRNA gene sequence similarities have D-xylose, L-aspartic acid, glutamic acid, DL-methionine, been reported among novel species (Bouchek-Mechi- L-ornithine, L-phenylalanine or L-valine as either sole che et al. 2000; Dastager et al. 2007; Goodfellow et al. carbon or nitrogen sources. No acid production from 2007). Hence only the two closest relatives, S. virgin- fructose, glucose, lactose, maltose, mannitol or sucrose. iae NBRC 12827T and S. cinnamonensis NBRC Hydrolyzes starch, Tweens 20, 40, 60 and 80, and

123 Antonie van Leeuwenhoek (2012) 102:133–139 137

Table 2 Differential characteristics between strain MBRL 201T and S. virginiae NBRC 12827T and S. cinnamonensis NBRC 15873T Characteristics S. manipurensis S. virginiae S. cinnamonensis MBRL 201T NBRC 12827T NBRC 15873T pH range 6–10 6–8 6–9 Optimum pH for growth 8 7 7 Hydrolysis of Casein – ?? Starch w – ? Tyrosine ? –– Nitrate reduction – ?? Utilization of sole C-sources L-arabinose ?-- D-cellobiose ??- Fructose ?-? D-galactose ??- D-mannose ??- Rafﬁnose ?-? Sodium malate ?-- Succinic acid ?-- Trehalose --? Utilization of sole N-sources L-arginine ?-? DL-methionine --? L-ornithine -?- L-phenylalanine -?? L-valine -?? Major fatty acids ([5%)

Iso-C15:0 19.9 13.0 15.9

Anteiso-C15:0 38.9 27.7 22.1

Iso-H C16:1 --5.1

Iso-C16:0 6.5 24.5 17.1

C16:0 7.7 6.2 5.6 Sum in feature 9 --6.3

Anteiso-C17:1x9c --5.4

Iso-C17:0 6.6 --

Anteiso-C17:1 14.7 10.1 7.8 G?C (mol%) 72.9 72.0 72.4 ? Positive; - negative; w weakly positive; all the data were from this study All the test strains are positive for hydrolysis of Tweens 20, 40, 60, 80; catalase and indole production tests. All of them utilize maltose, L-alanine, glycine, L-histidine, L-hydroxyproline, potassium nitrate, proline, and L-serine as sole C and N sources. They showed negative results for gelatin hydrolysis, MR, VP and citrate utilization tests, and acid production from fructose, glucose, lactose, maltose, mannitol and sucrose. All the above strains could not utilize dulcitol, meso-inositol, lactose, mannitol, rhamnose, L-sorbose, xylitol and D-xylose as sole C or N sources. They grew in the temperature range 15–37 °C with optimum growth at 28 °C; all the strains could tolerate up to 2 % NaCl concentration

123 138 Antonie van Leeuwenhoek (2012) 102:133–139

S. xanthophaeus NBRC 12829T (AB184177) S. spororaveus LMG 20313T (AJ781370) S. nojiriensis LMG 20094T (AJ781355) S. cirratus NRRL B-3250T (AY999794) 88* S. vinaceus NBRC 13425T (AB184394) S. subrutilus DSM 40445T (X80825) 53 68* S. avidinii NBRC 13429T (AB184395) S. lavendulae subsp. lavendulae NBRC 12789T (AB184146) S. colombiensis NRRL B-1990T (DQ026646) T 57 S. goshikiensis NBRC 12868 (AB184204) 56 S. sporoverrucosus NBRC 15458T (AB184684) 91 S. virginiae NBRC 12827T (AB184175) 95* S. cinnamonensis NBRC 15873T (AB184707) Streptomyces manipurensis MBRL 201T (JN560156) S. yokosukanensis NRRL B-3353T (DQ026652) S. katrae NBRC 13447T (AB184409) 99 S. polychromogenes NBRC 13072T (AB184292) S. racemochromogenes NRRL B-5430T (DQ026656) 100 S. flavotricini NBRC 12770T (AB184132) T 94 S. globosus LMG 19896 (AJ781330) 99* S. toxytricini NBRC 12823T (AB184173)

0.001

Fig. 2 Neighbour-joining tree, based on 16S rRNA gene branches that were also recovered using the MP tree. Numbers at sequences, showing the relationship between strain MBRL nodes are levels of bootstrap support (%) for branch points (1,000 201T and type strains of Streptomyces species. Asterisks indicate resamplings). Bar 0.001 substitutions per nucleotide position tyrosine but not casein and gelatin. Positive in catalase S. N. wishes to thank the University Grants Commission (UGC), and indole production tests but negative in methyl Government of India, for offering him the Rajiv Gandhi National Fellowship. red, Voges–Proskauer, citrate utilization, and nitrate reduction tests. Contains LL-diaminopimelic acid and glucose with small amounts of galactose, mannose, rhamnose, ribose and xylose in the cell wall hydrolysates. References MK-9(H6) (58.7 %) and MK-9(H8) (41.3 %) are the menaquinones present, while the polar lipids consist of Anderson AS, Wellington EMH (2001) The taxonomy of diphosphatidylglycerol, phosphatidylmethylethanola- Streptomyces and related genera. Int J Syst Evol Microbiol mine, phosphatidylglycerol, phosphatidylethanolamine, 51:797–814 Bouchek-Mechiche K, Gardan L, Normand P, Jouan B (2000) phosphatidylinositol and phosphatidylinositolmannoside, DNA relatedness among strains of Streptomyces patho- with other unknown phospholipids and lipids. The fatty genic to potato in France: description of three new species, acid proﬁle ([1%)isasfollows:anteiso-C15:0,iso-C15:0, S. europaeiscabiei sp. nov. and S. stelliscabiei sp. nov. associated with common scab, and S. reticuliscabiei sp. anteiso-C17:1,C16:0,iso-C17:0,iso-C16:0,iso-C14:0 and Sum nov. associated with netted scab. Int J Syst Evol Microbiol in Feature 9 containing C16:1x7c/C16:1x6c. T T 50:91–99 The type strain, MBRL 201 (=DSM 42029 = Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW JCM 17351T), was isolated from a limestone quarry at (2007) EzTaxon: a web-based tool for the identiﬁcation of Hundung, Manipur, India. The GenBank accession prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261 number for the 16S rRNA gene sequence of strain T Collins MD, Pirouz T, Goodfellow M, Minnikin DE (1977) MBRL 201 is JN560156. Distribution of menaquinones in actinomycetes and cory- nebacteria. J Gen Microbiol 100:221–230 Acknowledgments The authors are grateful to Prof. Tomohiko Collins CH, Lyne PM, Grange JM, Falkinham JO (2004) In Tamura (NBRC) for kindly providing the reference type strains. Microbiological Methods, 8th edn. Arnold, London 123 Antonie van Leeuwenhoek (2012) 102:133–139 139

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