IJSEM Papers in Press. Published July 16, 2014 as doi:10.1099/ijs.0.064527-0
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Streptomyces zagrosensis sp. nov., isolated from soil
2 3
Fatemeh Mohammadipanah1,2, Javad Hamedi1,2*, Cathrin Spröer3, Manfred Rohde4, María del
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Carmen Montero-Calasanz3* and Hans-Peter Klenk3
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1
6
Living Organisms, College of Science, University of Tehran, 14155-6455, Tehran, Iran
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2
8
Center, University of Tehran, Tehran, Iran
9
3
Department of Microbial Biotechnology, School of Biology and Center of Excellence in Phylogeny of
University of Tehran Microorganisms Collection (UTMC), Microbial Technology and Products Research
Leibniz-Institut DSMZ - German Collection of Microorganisms and Cell Cultures, Inhoffenstrasse 7b, 38124
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Braunschweig, Germany
11
4
HZI – Helmholtz Centre for Infection Research Inhoffenstraße 7, 38124 Braunschweig, Germany
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Running title: Streptomyces zagrosensis sp. nov.
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Subject Category: New Taxa-Actinobacteria
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*Corresponding author:
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Javad Hamedi, Tel.: +98-21-61113556; Fax: +98-21-66415081, e-mail:
[email protected] 18
María del Carmen Montero-Calasanz, Tel.: +49(0)531 26 16-210; Fax: +49 (0)531 26 16-
19
237, e-mail:
[email protected] 20 21
The INSDC accession number for the 16S rRNA gene sequence of strain HM 1154T is
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JF917242.
23 24 25
Abstract 1
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The taxonomic position of a novel actinomycete isolated from soil in Fars Province (Iran)
27
was determined using a polyphasic approach. Phenotypic and 16S rRNA gene sequence
28
analysis of the isolate matched those described for members of the genus Streptomyces. On
29
ISP2 medium, strain HM 1154T produced a dark cream branched substrate mycelium and
30
Retinaculiaperti aerial hyphae that in some images also appear spiral and that developed
31
into greyish white spore chains with smooth surface. The isolate showed optimal growth at
32
28 °C and pH 6-9 with 0-4 % (w/v) NaCl. Whole cell hydrolyzates contained LL-
33
diaminopimelic acid as diagnostic diamino acid, ribose and glucose. The main
34
phospholipids
35
phosphatidylinositol, three unknown phospholipids and an unknown aminophospholipids;
36
MK-9(H4) and MK-9(H2) were the predominant menaquinones. The major cellular fatty
37
acids were the branched saturated iso-C16:0 and anteiso-C15:0. Strain HM 1154T exhibited
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the highest 16S rRNA sequence similarities to Streptomyces coerulescens DSM 40146T
39
(99.4 %), Streptomyces varsoviensis DSM 40346T (99.3 %), Streptomyces youssoufiensis
40
DSM 41920T (99.2 %), Streptomyces abikoensis DSM 40831T (99.2 %), Streptomyces
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rimosus subsp. primosus DSM 40260T (99.1 %), Streptomyces luteireticuli DSM 40509T
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(99.1 %), Streptomyces thioluteus DSM 40027T (99.1 %), Streptomyces blastmyceticus
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DSM 40029T (99.0 %) and Streptomyces hiroshimensis DSM 40037T (99.0 %). DNA-
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DNA studies showed relatedness values between 11.0-35.8 % with its closest related
45
species. Based on these results, strain HM 1154T (DSM 42018T = UTMC 1154T = CECT
were
phosphatidylethanolamine,
2
diphosphatidylglycerol,
46
8305T) is considered to represent a novel species within the genus Streptomyces, for which
47
the name Streptomyces zagrosensis is proposed.
48 49 50 51
The genus Streptomyces was proposed by Waksman & Henrici (1943) (emend. Witt &
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Stackebrandt 1990; emend. Wellington et al., 1992) to accommodate aerobic, spore-
53
forming actinomycetes. Members of the genus Streptomyces are Gram-positive bacteria
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with a DNA rich in G+C (69–73 mol %) (Williams et al., 1983), containing LL-
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diaminopimelic acid in the peptidoglycan and lacking diagnostic sugars in whole cell
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hydrolyzates (Lechevalier & Lechevalier, 1970). Streptomyces species are common in soil
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(Zheng et al., 2013; Hamedi et al., 2010; Bouizgarne et al., 2009) and known by their
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ability to produce biotechnological useful enzymes (Liu et al., 2013) and, mostly active
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biologically secondary metabolites, such as antibiotics (Kim et al., 2012), antitumor agents
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(Schleissner et al., 2011) and antifungal compounds (Zhao et al., 2010), among others.
61
Peptides, and especially cyclopeptides, have currently received considerable attention
62
because of exhibiting unique structures and interesting pharmacological activities (Laatsch
63
et al., 2011).
64
During studies of the taxonomy and antibiotic production of actinomycetes from Iranian
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soils, the isolate HM 1154T was selected by its ability to produce two new cyclopeptides,
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persipeptide A and B (Mohammadipanah et al., 2012), and recognized as a potentially new
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species in the genus Streptomyces. Herein we describe the taxonomic position of this
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genomically distinct novel lineage based on a polyphasic approach. 3
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Rhizospheric soil samples were collected at 4-6 cm depth in Fars Province (Iran), and then
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first air dried (Nolan & Cross, 1988), followed by a heat-drying step at 120 °C for 10 min
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(Nonomura & Ohara, 1971). Strain HM 1154T was isolated by using the dilution plating
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method on Glucose-Asparagine agar (Nonomura & Ohara, 1969) supplemented with
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cycloheximide (100
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(International Streptomyces Project) 2 agar slants at 4 oC and 20 % (v/v) glycerol
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suspensions at -70 oC.
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Cultural properties of strain HM 1154T were evaluated according to the guidelines of the
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ISP as described by Shirling & Gottlieb (1966). Aerial and substrate mycelia colours were
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determined by comparing with chips from the ISCC-CNBS color charts (Kelly, 1964).
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The intact arrangement of the aerial hyphae and spore chains was observed on ISP 2 agar
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after 14 days at 28oC using the cover-slip technique (Kawato & Shinobu, 1959). Spore
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chain morphology and spore surface ornamentation were examined with a field-emission
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scanning electron microscope (FE-SEM Merlin, Zeiss, Germany). Growth rates were
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determined for temperatures from 10-50 °C at 5 °C increments and for pH values 4-11 (in
84
increments of 1.0 pH units) on modified Bennett medium as described by Williams et al.
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(1989) using Na-sesquicarbonate buffer system for preparation of alkaline media. The
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utilization of carbon sources and acid production were determined using GEN III
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Microplates in an Omnilog device (BIOLOG Inc., Hayward, CA, USA). The GEN III
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Microplates were inoculated with a cell suspension made in a “gelling” inoculating fluid
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(IF) C at a cell density of 98% transmittance, yielding a running time of 3 days in
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Phenotype Microarray mode at 28°C. The exported data were further analyzed with the
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opm package for R (Vaas et al., 2012; 2013) v.1.0.6., using its functionality for merging
μg/ml)
after 14 days incubation at 28 oC and maintained on ISP
4
92
subsequent measurements of the same plate, statistically estimating parameters from the
93
respiration curves such as the maximum height, and automatically “discretizing” these
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values into negative and positive reactions. Strain HM 1154T in comparison with the
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reference strains S. coerulescens DSM 40146T, S. varsoviensis DSM 40346T, and S.
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youssoufiensis DSM 41920T were studied in the GEN III Microplates in two independent
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determinations. Reactions that gave contradictory results between the two repetitions were
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regarded as ambiguous.
99
Strain HM 1154T showed an optimal growth on yeast extract-malt extract agar (ISP2
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medium), glycerol-asparagine agar (ISP5 medium) and tyrosine agar (ISP7 medium), a
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poor growth on oatmeal agar (ISP3 medium) and peptone yeast extract iron agar (ISP6
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medium), and no growth on inorganic salts-starch agar (ISP4 medium). It produced well-
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developed substrate mycelium and aerial mycelium formed by long spore chains (20-50
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spores; spore size 0.4-0.6 µm) (Fig. 1), which is consistent with typical characteristics of
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members of the genus Streptomyces (Kämpfer, 2012). According to the spore chain
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morphology classification by Pridham et al. (1958), isolate HM 1154T showed type
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Retinaculiaperti with smooth surface on ISP2 medium, that in some images also appear
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spiral. This morphology is common in the genus Streptomyces and was already observed in
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the related species S. coelescens and S. varsoviensis on ISP2, ISP3, ISP4 and ISP5 and
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ISP3 and ISP5 media, respectively (Kämpfer, 2012). The mycelia pigmentations varied
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depending on the tested medium. On ISP2 and ISP3 media, both mycelia showed colours
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between white and dark cream, turning to greyish white in sporulation phase. Nevertheless,
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light brownish and even dark orange coloured mycelia were observed on ISP5 and ISP6
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and ISP7 media, respectively. No diffusible pigments were released into tested media. In
5
115
addition, a different spore production was displayed, finding the best spore mass on ISP2
116
medium. Similar observations regarding to the different sporulation capacity on various
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media were already described by Kontro et al. (2005).
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The isolate HM 1154T grew from 10 to 40 oC, the optimal temperature was at 28 °C; no
119
growth was observed below 10 °C or above 40oC. Growth occurred at 0-4 % NaCl (w/v)
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(optimal range), but not at 5% NaCl, and from pH 6 to pH 11 (optimal range was pH 6-9).
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Results from phenotype microarray analysis shown as a heatmap in Fig. S1 in comparison
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to other type strains of Streptomyces, revealed not only significant phenotype differences
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between strain HM 1154T and related species, but also confirmed the wide range of organic
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compounds that Streptomyces species can use as sole sources of carbon for energy and
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growth (Kämpfer, 2012). A summary of select differential phenotypic characteristics is
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presented in Table 1.
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To carry out cell wall amino acids and sugars, polar lipids and respiratory lipoquinones and
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composition of peptidoglycan studies, strain HM 1154T was cultivated in trypticase soy
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broth (TSB) for 6 days in shaking cultures at 200 rpm, pH 7.2 at 28 oC. Cell biomass was
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harvested by centrifugation and washed twice with distilled water. The composition of
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peptidoglycan hydrolysates was examined by TLC as described by Schleifer & Kandler
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(1972). Whole-cell sugars were prepared according to Lechevalier & Lechevalier (1970),
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followed by thin layer chromatography (TLC) analysis (Staneck & Roberts, 1974). Polar
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lipids were extracted, separated by two-dimensional TLC and identified according to
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procedures outlined by Minnikin et al. (1984) with modifications proposed by
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Kroppenstedt & Goodfellow (2006). Respiratory lipoquinones were extracted from freeze-
137
dried cell material using methanol as described by Collins et al. (1977) and analyzed by
6
138
high-performance liquid chromatography (HPLC) (Kroppenstedt, 1982). The extraction of
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cellular fatty acids was carried out from biomass grown on TSB tubes held at 28 °C for 4
140
days. Analysis was conducted using the Microbial Identification System (MIDI) Sherlock
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Version 6.1 (results evaluated against the TSBA40 peak naming table database) as
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described by Sasser (1990).
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Analysis of whole cell wall revealed the presence of the diamino acid LL-diaminopimelic
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and ribose and glucose, indicating its belonging to wall chemotype I (Lechevalier &
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Lechevalier, 1970), which is consistent with other species of the genus Streptomyces
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(William et al., 1989). The predominant menaquinones were MK-9(H4) (59.1 %) and MK-
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9(H2) (25.4 %), but also minor amounts of MK-9(H6) (6.7 %), MK-8(H4) (2.6 %), and MK-
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10(H4) (2.2 %) were displayed. The polar lipids pattern was, as usual in the genus
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Streptomyces,
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diphosphatidylglycerol (DPG), phosphatidylinositol (PI), three unknown phospholipids
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(PL4, PL5 and PL6), an unknown aminophospholipid (APL) and small amounts of other
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three unknown phospholipids (PL1, PL2 and PL3) (Fig. S2). The main fatty acids were the
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saturated branched iso-C16:0 (27.9 %) and anteiso-C15:0 (22.0 %), but also C16:0 (9.9 %),
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anteiso-C17:0 (8.5 %), C16:1 ω7 (8.5 %), iso-C15:0 (4.9 %), iso-C14:0 (4.4 %), iso-C16:1 H (3.5
155
%) and anteiso-C17:1 C (2.6 %) were found. The qualitative and quantitative combination of
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straight-chain and iso- and anteiso-branched fatty acids of strain HM 1154T matched with
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other Streptomyces species and the fatty acid pattern 2c sensu according to the
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classification established by Kroppenstedt (1985).
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Genomic DNA extraction, PCR-mediated amplification of the 16S rRNA gene and
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purification of the PCR product was carried out as described by Rainey et al. (1996).
complex
and
consisted
7
of
phosphatidylethanolamine
(PE),
161
Phylogenetic analyses based on maximum-likelihood (ML) and maximum parsimony (MP)
162
and the rooting of the resulting trees were conducted as previously described (Montero-
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Calasanz et al., 2013). Pairwise similarities were calculated as recommended by Meier-
164
Kolthoff et al. (2013). For DNA-DNA hybridization tests cells were disrupted by using a
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Constant Systems TS 0.75 KW (IUL Instruments, Germany). DNA in the crude lysate was
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purified by chromatography on hydroxyapatite as described by Cashion et al. (1977). DNA-
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DNA hybridization was carried out as described by De Ley et al. (1970) under
168
consideration of the modifications described by Huss et al. (1983) using a model Cary 100
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Bio UV/VIS-spectrophotometer equipped with a Peltier-thermostatted 6x6 multicell
170
changer and a temperature controller with in-situ temperature probe (Varian).
171
The almost complete (1508 bp) 16S rRNA gene sequence of strain HM 1154T showed the
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highest similarity with members of the genus Streptomyces, especially with the type strains
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of Streptomyces coerulescens DSM 40146T (99.4 %), Streptomyces varsoviensis DSM
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40346T (99.3 %), Streptomyces youssoufiensis DSM 41920T (99.2 %), Streptomyces
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abikoensis DSM 40831T (99.2 %), Streptomyces rimosus subsp. primosus DSM 40260T
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(99.1 %), Streptomyces luteireticuli DSM 40509T (99.1 %), Streptomyces thioluteus DSM
177
40027T (99.1 %), Streptomyces blastmyceticus DSM 40029T (99.0 %) and Streptomyces
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hiroshimensis DSM 40037T (99.0 %). Similarity values of 98.9-97.0 % were determined for
179
another 69 type strains belong to the genus Streptomyces. Phylogenetic tree topology
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inferred from ML and MP based on 16S rRNA gene sequences of the strain HM 1154T and
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the closest related Streptomyces species is shown in Fig. 2. The 16S rRNA gene sequence
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similarity between HM 1154T and closely related type strains indicated the need to prove
183
the genomic distinctness of the type strain representing the novel species by DNA-DNA
8
184
hybridization (Table 2). DNA-DNA hybridizations between strain HM 1154T and type
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strains showing similarities of 98.9-97.0 % were not conducted based on the observations
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reported by Meier-Kolthoff et al. (2013) that statistically confirmed that the threshold value
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previously established at 97 % 16S rRNA gene sequence similarity was too conservative in
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microbial species discrimination and determined a Actinobacteria-specific 16S rRNA
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threshold at 99.0 % with a maximun probability of error of 1.00 % to get DNA-DNA
190
hybridization values above the 70% threshold recommended by Wayne et al. (1987) to
191
confirm the species status of novel strains.Genotypic and phenotypic evidences support the
192
distinctiveness of strain HM 1154T from all Streptomyces species. Therefore, we consider
193
strain HM 1154T to represent a novel species of the genus Streptomyces, for which the
194
name Streptomyces zagrosensis is proposed.
195 196
Description of Streptomyces zagrosensis sp. nov.
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Streptomyces zagrosensis (za.gros.en'sis N.L. masc. adj. zagrosensis referring to the Zagros
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mountains range nearby, where type strain was isolated).
199
Aerobic, Gram-staining-positive actinomycete which forms extensive, branched substrate
200
mycelium and aerial hyphae with long Retinaculiaperti spore chains with smooth surface.
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On ISP2 medium, colonies were cream, turning to greyish white in sporulation phase.
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Optimal growth occurs at 28 oC and at pH 6-9. Grows well in the presence of 0-4 % NaCl.
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Dextrin, sucrose, D-raffinose, β-methyl-D-glucoside, N-acetyl-D-glucosamine, N-acetyl-β-
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D-mannosamine, N-acetyl-D-galactosamine, D-glucose, sodium lactate, D-sorbitol,
205
glycerol, D-aspartic acid, gelatin, glycin-L-proline, L-alanine, L-aspartic acid, L-glutamic
206
acid, L-histidine, L-pyroglutamic acid, L-serine, gelatin, D-galacturonic acid, D-gluconic
9
207
acid, D-lactic acid methyl ester, citric acid, α-keto-glutaric acid, L-malic acid, potassium
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tellurite, tween 40, γ-amino-n-butyric acid, β-hydroxy-butyric acid, α-keto-butyric acid,
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propionic acid and acetic acid can be used as sole carbon sources for growth but not for D-
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trehalose, D-cellobiose, β-gentiobiose, D-melibiose, N-acetyl-neuraminic acid, D-mannose,
211
D-galactose, 3-O-methyl-D-glucose, D-fucose, L-fucose, L-rhamnose, inosine, D-serine, D-
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mannitol, myo-inositol, L-arginine, pectin, L-galactonic, acid-γ-lactone, glucuronamide,
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mucic acid, quinic acid, D-saccharic acid, p-hydroxy-phenylacetic acid, methyl pyruvate,
214
L-lactic acid, D-malic acid, bromo-succinic acid, α-hydroxy-butyric acid, acetoacetic acid,
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sodium formate and butyric acid. N-acetyl-D-glucosamine, N-acetyl-β-D-mannosamine,
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N-acetyl-D-galactosamine, D-aspartic acid, L-glutamic acid, glycin-L-proline, L-alanine,
217
L-aspartic acid, L-histidine, L-serine, and
218
nitrogen sources but not N-acetyl-neuraminic acid, inosine, D-serine, L-arginine and
219
glucuronamide. Whole cell hydrolyzates contain LL-diaminopimelic acid as diamino acid,
220
but not diagnostic sugars. The major menaquinones are MK-9(H4) and MK-9(H2). The
221
main
222
phosphatidylinositol, three unknown phospholipids and an unknown aminophospholipid.
223
The fatty acid composition consists mainly of iso-C16:0 and anteiso-C15:0 (22.0 %),
224
complemented by C16:0, anteiso-C17:0 and C16:1 ω7.
225
The type strain HM 1154T (= DSM 42018T= UTMC 1154T= CECT 8305T), was isolated
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from rhizospheric soil taken at a depth of 4-6 cm in Fars Province, Iran.
phospholipids
are
γ-amino-n-butyric
phosphatidylethanolamine,
227 228
Acknowledgements
229
10
acid are utilized as sole
diphosphatidylglycerol,
230
The authors would like to thank the Biotechnology Development Council of Iran for its
231
financial support, Gabi Pötter and Marlen Jando for their help in chemotaxonomic analysis
232
and general assistance at DSMZ.
233 234 235
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334
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336
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350
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351
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352
Fig. 1. Scanning electron micrograph of strain HM 1154T after growth on ISP2 medium for
353
14 days at 28 oC
354
Fig. 2. Maximum likelihood phylogenetic tree inferred from 16S rRNA gene sequences,
355
showing the phylogenetic position of strain HM 1154T and the type strains of related taxa.
356
The branches are scaled in terms of the expected number of substitutions per site (see size
357
bar). Support values from maximum-likelihood (left) and maximum-parsimony (right)
358
bootstrapping are shown above the branches if equal to or larger than 50 %.
359
Table 1. Differential characteristics of strain HM 1154T and the type strains of other
360
closely related Streptomyces species.
361
Strains: 1, S. zagrosensis HM 1154T; 2, S. coerulescens DSM 40146T; 3, S. varsoviensis
362
DSM 40346T; 4, S. youssoufiensis DSM 41920T. All biochemical data are from this study,
363
except diffusible and melanoid pigments data of S. coerulescens, S. varsoviensis and S.
364
youssofiensis.
16
Characteristics Spore Chain Morphology Spore Surface
1
2
Retinaculiaperti Spiral£ Smooth
3
4
Spiral¥
Rectiflexibiles
Spiny£ Smooth¥
Smooth
Diffusible Pigment
-
+£
+
-
Melanoid Pigment
-
+£
-
-
+ -
-
+ +
+ +
-
+/-
+
+
+ + + + + +/+ + + + + -
+ +/+ + + +/+/+ + + + +
+ +/+ + + + -
+/+/+/+ + + + + + + +
+ +
+ -
+ + -
+ +
NaCl Range (w/v): 4% 8% Growth at: pH 5 Utilization of: D-Cellobiose β-Gentiobiose Sucrose D-Raffinose D-Melibiose β-Methyl-D-Glucoside N-Acetyl-β-D-Mannosamine N-Acetyl-D-Galactosamine N-Acetyl-Neuraminic Acid D-Mannose D-Fructose D-Galactose Inosine D-Sorbitol D-Mannitol D-Aspartic Acid L-Arginine D-Galacturonic Acid Citric Acid Adonitol Cisteine Degradation of: Aesculin Adenine Allantoin 365
+, positive reaction; –, negative reaction; +/-, ambiguous
366
, Data taken from Hamdali et al. (2011).
17
367
¥
368
£
, Data taken from Williams et al. (1983). , Data taken from Li et al. (2002)
369 370
Table 2. DNA-DNA hybridizations between strain HM 1154T and its most closely related
371
species of the genus Streptomyces.
372 DNA-DNA hybridization (%)*
Type strain
Pairwise Similarity (%)
11.0 ± 0.1
Streptomyces coerulescens DSM 40146T
99.4
26.1 ± 0.1
Streptomyces varsoviensis DSM 40346T
99.3
35.8 ± 1.9
Streptomyces youssoufiensis DSM 41920T
99.2
14.0 ± 1.3
Streptomyces abikoensis DSM 40831T
99.2
20.8 ± 2.5 20.7 ± 1.2 20.2 ± 4.5 13.5 ± 0.9 31.2 ± 3.1
Streptomyces rimosus subsp. primosus DSM 40260T Streptomyces luteireticuli DSM 40509T Streptomyces thioluteus DSM 40027T Streptomyces blastmyceticus DSM 40029T Streptomyces hiroshimensis DSM 40037T
99.1 99.1 99.1 99.0 99.0
373
*Mean ± SD of two determinations.
374
Supplementary Fig. S1. The parameter “Maximum Height” estimated from the respiration
375
curves as measured with the OmniLog phenotyping device and discretized and visualized
376
as heatmap using the opm package. Plates and substrates are rearranged according to their
377
overall similarity (as depicted using the row and column dendrograms). Orange colour
18
378
indicates positive reaction; blue colour indicates negative reaction; green colour indicates
379
ambiguous reaction. Letters (A/B) indicate each replicate of experiment.
380
Supplementary Fig. S2. Total lipids profile of Streptomyces zagrosensis HM 1154T, after
381
separation by two-dimensional TLC. Plate was sprayed with molydatophosphoric acid for
382
detection of total polar lipid. DPG, diphosphadidylglycerol; PE, phosphatidethanolamine;
383
PI,
384
phospholipids; L1-3, unknown lipids.
phosphatidylinositol;
APL,
unknown
385
19
aminophospholipid;
PL1-6,
unknown
T Streptomyces blastmyceticusXDSMX40029 X(AY999802) 69/59 Streptomyces ardusXDSMX40527TX(AB184864) T Streptomyces cinnamoneusXDSMX40005 X(AB184850) 99/97 T 77/73 Streptomyces hiroshimensisXDSMX40037 X(AB184802) T Streptomyces thioluteusXDSMX40027 X(AJ781360) T Streptomyces morookaenseXDSMX40503 X(AJ781349) T Streptomyces abikoensisXDSMX40831 X(AB184537) T 100/100 X(AB184217) Streptomyces lavendofoliaeXDSMX40217 T X(AB184666) Streptomyces gobitriciniXDSMX41701 T X(AB184819) Streptomyces lilacinusXDSMX40254 Streptomyces coerulescensXDSMX40146TX(AB184122) Streptomyces mobaraensisXDSMX40847TX(AORZ01000256) T Streptomyces iranensisXDSMX41954 X(FJ472862) T Streptomyces orinociXDSMX41571 X(AB184866) T X(AB024441) Streptomyces kasugaensisXDSMX40819 T X(X99943) Streptomyces griseocarneusXDSMX40004 T Streptomyces varsoviensisXDSMX40346 X(DQ026653) T Streptomyces luteireticuliXDSMX40509 X(AB249969) T Streptomyces zagrosensis HM 1154 (JF91724) 100/82 Streptomyces nigerXDSMX43049TX(AB184352) 82/70 Streptomyces olivaceiscleroticusXDSMX40595TX(AJ621606) T 50/Streptomyces monomycini DSMX41801 X(AB249936) T Streptomyces sclerotialusXDSMX43032 X(AJ621608) 80/58 T 67/52 Streptomyces rimosusXsubsp.XprimosusXDSMX40260 X(ANSJ01000404) T X(AJ849545) Streptomyces sparsusXDSMX41858 T 73/54 68/- Streptomyces libaniXsubsp.XprufusXDSMX41230 X(AJ781351) 56/- Streptomyces hygroscopicusXsubsp.Xglebosus DSMX40823TX(AB184479) T 81/87 Streptomyces platensisXDSMX41241 X(AB045882) 50/51 T X(AB184640) Streptomyces caniferusXDSMX41453 T X(DQ026662) Streptomyces ramulosusXDSMX40100 T Streptomyces youssoufiensis DSMX41920 X(FN421338)
99/92
0.007