Open Access

Draft genome sequence of marine-derived Streptomyces sp. TP-A0598, a producer of anti-MRSA antibiotic lydicamycins

  • Hisayuki Komaki1Email author,
  • Natsuko Ichikawa2,
  • Akira Hosoyama2,
  • Nobuyuki Fujita2 and
  • Yasuhiro Igarashi3
Standards in Genomic Sciences201510:58

https://doi.org/10.1186/s40793-015-0046-5

Received: 8 January 2015

Accepted: 21 July 2015

Published: 26 August 2015

Abstract

Streptomyces sp. TP-A0598, isolated from seawater, produces lydicamycin, structurally unique type I polyketide bearing two nitrogen-containing five-membered rings, and four congeners TPU-0037-A, −B, −C, and –D. We herein report the 8 Mb draft genome sequence of this strain, together with classification and features of the organism and generation, annotation and analysis of the genome sequence. The genome encodes 7,240 putative ORFs, of which 4,450 ORFs were assigned with COG categories. Also, 66 tRNA genes and one rRNA operon were identified. The genome contains eight gene clusters involved in the production of polyketides and nonribosomal peptides. Among them, a PKS/NRPS gene cluster was assigned to be responsible for lydicamycin biosynthesis and a plausible biosynthetic pathway was proposed on the basis of gene function prediction. This genome sequence data will facilitate to probe the potential of secondary metabolism in marine-derived Streptomyces.

Keywords

LydicamycinTPU-0037Biosynthetic genePolyketide synthase Streptomyces

Introduction

Members of the genus Streptomyces , Gram-positive filamentous actinomycetes, are an attractive source for bioactive secondary metabolites. Terrestrial surface soil is the most common habitat for Streptomyces but a recent survey has disclosed its ubiquitous distribution in marine environments. Marine Streptomyces are currently attracting much attention as an untouched resource of novel bioactive compounds useful for drug development [13]. In our screening for new anti-MRSA antibiotics, Streptomyces sp. TP-A0598 collected from deep sea water was found to produce lydicamycin and its four new congeners of polyketide origin (Fig. 1) [4]. Lydicamyicn is characterized by the unprecedented pyrrolidine ring modified by an aminoiminomethyl group to which a polyketide-derived carbon chain with multiple hydroxyl and olefinic functionalities is linked and to the other end of the chain is linked an octalin modified by a tetramic acid. Despite this unique structural feature, biosynthetic genes of lydicamycin have not been reported to date. In this study, we conducted whole genome shotgun sequencing of the strain TP-A0598 to identify the PKS gene cluster for lydicamycin. We herein present the draft genome sequence of Streptomyces sp. TP-A0598, together with the description of genome properties and annotation for secondary metabolite genes. The putative lydicamycin biosynthetic gene cluster and a plausible biosynthetic pathway are also reported.
Fig. 1

Chemical structures of lydicamycin and its congeners produced by Streptomyces sp. TP-A0598

Organism information

Classification and features

In the course of screening for new bioactive molecules produced by marine microorganisms, Streptomyces sp. TP-A0598 was isolated from a seawater sample collected in 2,600 meters off the shore and 321 meters in depth at Namerikawa, Toyama, Japan by a membrane filter method and found to produce lydicamycin and its novel congeners. This strain grew well on Bennett’s, ISP 3, ISP 4, ISP 5 and Yeast starch agars. On ISP 5, ISP 6 and ISP 7 agars, the growth was poor. The color of aerial mycelia was grayish olive and that of the reverse side was pale yellow on ISP 3 agar. Diffusible pigments were not formed on any agar media that we examined. Strain TP-A0598 formed spiral spore chains and the spores were cylindrical, 0.5 × 0.9 μm in size, having a warty surface [4]. A scanning electron micrograph of this strain is shown in Fig. 2. Growth occurred at 15–37 °C (optimum 30 °C) and pH 5–9 (optimum pH 7). Strain TP-A0598 exhibited growth with 0–7 % (w/v) NaCl (optimum 0 % NaCl). Strain TP-A0598 utilized D-glucose, sucrose, inositol, L-rhamnose, D-mannitol, D-raffinose, D-fructose, L-arabinose, and D-xylose for growth (Table 1) [4]. This strain was deposited in the NBRC culture collection with the registration number of NBRC 110027. The genes encoding 16S rRNA were amplified by PCR using two universal primers, 9 F and 1541R. After purification of the PCR product by AMPure (Beckman Coulter), the sequencing was carried out according to a established methods [5]. Homology search of the sequence by EzTaxon-e [6] indicated the highest similarity (99.93 %, 1465/1466) to Streptomyces angustmyceticus NBRC 3934T (AB184817) [7] as the closest type strain. A phylogenetic tree was reconstructed on the basis of the 16S rRNA gene sequence together with phylogenetic neighbors that showed over 98.5 % similarity (Fig. 3) using ClustalX2 [8] and NJplot [9]. The phylogenetic analysis confirmed that the strain TP-A0598 belongs to the genus Streptomyces .
Fig. 2

Scanning electron micrograph of Streptomyces sp. TP-A0598 grown on ten-fold diluted ISP 2 medium agar for 11 days at 28 °C. Bar, 5 μm

Table 1

Classification and general features of Streptomyces sp. TP-A0598

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [16]

Phylum Actinobacteria

TAS [17]

Class Actinobacteria

TAS [18]

Order Actinomycetales

TAS [1821]

Suborder Streptomycineae

TAS [18, 19]

Family Streptomycetaceae

TAS [1820, 22, 23]

Genus Streptomyces

TAS [20, 2325]

Species Streptomyces sp.

TAS [4]

Strain TP-A0598

TAS [4]

 

Gram stain

Not tested, likely positive

NAS

 

Cell shape

Branched mycelia

TAS [4]

 

Motility

Not reported

 
 

Sporulation

Sporulating

TAS [4]

 

Temperature range

Grows from 15 °C to 37 °C

IDA

 

Optimum temperature

30 °C

IDA

 

pH range; Optimum

5-9; 7

IDA

 

Carbon source

D-glucose, sucrose, inositol, L-rhamnose, D-mannitol, D-raffinose, D-fructose, L-arabinose, D-xylose

TAS [4]

MIGS-6

Habitat

Marine

TAS [4]

MIGS-6.3

Salinity

Grows from 0 % to 7 % NaCl

IDA

MIGS-22

Oxygen requirement

Aerobic

TAS [4]

MIGS-15

Biotic relationship

Free-living

TAS [4]

MIGS-14

Pathogenicity

Not reported

 

MIGS-4

Geographic location

2,600 meters off the shore at Namerikawa, Toyama, Japan

TAS [4]

MIGS-5

Sample collection

Not reported

 

MIGS-4.1

Latitude

Not reported

 

MIGS-4.2

Longitude

Not reported

 

MIGS-4.4

Attitude

−321 m

TAS [4]

aEvidence codes – IDA: Inferred from Direct Assay; TAS: Traceable Author Statement (i.e., a direct report exists in the literature); NAS: Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence). These evidence codes are the Gene Ontology project [26]

Fig. 3

Phylogenetic tree highlighting the position of Streptomyces sp. TP-A0598 relative to phylogenetically close type strains within the genus Streptomyces. The strains and their corresponding GenBank accession numbers for 16S rRNA genes are shown in parentheses. The tree uses sequences aligned by ClustalX2 [8], and constructed by the neighbor-joining method [27]. All positions containing gaps were eliminated. The building of the tree also involves a bootstrapping process repeated 1000 times to generate a majority consensus tree [28], and only bootstrap values above 50 % are shown at branching points. Kitasatospora setae [29] was used as an outgroup

Chemotaxonomic data

The whole-cell hydrolysates of strain TP-A0598 contained L,L-diaminopimelic acid, glycine, ribose and madurose. The cellular fatty acids consisted of 21 % 14-methylpentadecanoic acid (iso C16), 9 % 13-methyltetradecanoic acid (iso C15:0), 8 % 12-methyltetradecanoic acid (anteiso C15:0) and other minor fatty acids [4].

Genome sequencing information

Genome project history

In collaboration between Toyama Prefectural University and NBRC, the organism was selected for genome sequencing to elucidate the lydicamycin biosynthetic gene cluster. We successfully accomplished the genome project of Streptomyces sp. TP-A0598 as reported in this paper. The draft genome sequence data have been deposited in the INSDC database under the accession number BBNO01000001-BBNO01000020. The project information and its association with MIGS version 2.0 compliance are summarized in Table 2 [10].
Table 2

Project information

MIGS ID

Property

Term

MIGS 31

Finishing quality

Improved-high-quality draft

MIGS-28

Libraries used

454 shotgun library, Illumina pair-end library

MIGS 29

Sequencing platforms

454 GS FLX+, Illumina HiSeq1000

MIGS 31.2

Fold coverage

8.4 ×, 93 ×, respectively

MIGS 30

Assemblers

Newbler v2.6

MIGS 32

Gene calling method

Progidal v2.6

 

Locus Tag

TPA0598

 

GenBank ID

BBNO00000000

 

GenBank Date of Release

January 6, 2015

 

GOLD ID

Not registered

 

BIOPROJECT

PRJDB3150

MIGS 13

Source Material Identifier

NBRC 110027

 

Project relevance

Industrial

Growth conditions and genomic DNA preparation

Streptomyces sp. TP-A0598 monoisolate was grown on polycarbonate membrane filter (Advantec) on double diluted ISP 2 agar medium (0.2 % yeast extract, 0.5 % malt extract, 0.2 % glucose, 2 % agar, pH 7.3) at 28 °C. High quality genomic DNA for sequencing was isolated from the mycelia with an EZ1 DNA Tissue Kit and a Bio Robot EZ1 (Qiagen) according to the protocol for extraction of nucleic acid from Gram-positive bacteria. The size, purity, and double-strand DNA concentration of the genomic DNA were measured by pulsed-field gel electrophoresis, ratio of absorbance values at 260 nm and 280 nm, and Quant-iT PicoGreen dsDNA Assay Kit (Life Technologies) to assess the quality.

Genome sequencing and assembly

Shotgun and pair-end libraries were prepared and sequenced using 454 pyrosequencing technology and HiSeq1000 (Illumina) pair-end technology, respectively (Table 2). The 70 Mb shotgun sequences and 702 Mb pair-end sequences were assembled into 20 scaffolds larger than 500 bp using Newbler v2.6, and subsequently finished using GenoFinisher [11].

Genome annotation

Coding sequences were predicted by Prodigal [12] and tRNA-scanSE [13]. The gene functions were annotated using an in-house genome annotation pipeline and domains related to PKS and NRPS were searched for using the SMART and PFAM domain databases. PKS and NRPS gene clusters and their domain organizations were analyzed manually. Similarity search in the NCBI nr databases was also used for functional prediction of genes in the lydicamycin biosynthetic gene cluster.

Genome properties

The total size of the genome is 8,319,549 bp and the GC content is 71.0 % (Table 3), similar to other genome-sequenced Streptomyces members. Of the total 7,344 genes, 7,240 are protein-coding genes and 75 are RNA genes. The classification of genes into COGs functional categories is shown in Table 4. As for the secondary metabolism, Streptomyces sp. TP-A0598 has two type I PKS, two type II PKS, two NRPS, and two hybrid PKS/NRPS gene clusters, suggesting the high capacity of production of polyketides and nonribosomal peptides.
Table 3

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

8,319,549

100.0

DNA coding (bp)

7,149,098

85.9

DNA G + C (bp)

5,915,420

71.0

DNA scaffolds

20

100.0

Total genes

7,344

100.0

Protein-coding genes

7,240

98.6

RNA genes

75

1.0

Pseudo genes

29

0.4

Genes in internal clusters

761

10.4

Genes with functional prediction

3,207

43.7

Genes assigned to COGs

4,450

60.6

Genes with Pfam domains

4,543

61.9

Genes with signal peptides

653

8.9

Genes with transmembrane helices

1,770

24.1

CRISPR repeats

5

-

Table 4

Number of genes associated with general COG functional categories

Code

Value

% age

Description

J

196

2.70

Translation

A

2

0.03

RNA processing and modification

K

519

7.17

Transcription

L

155

2.14

Replication, recombination and repair

B

0

0.00

Chromatin structure and dynamics

D

40

0.55

Cell cycle control, mitosis and meiosis

V

127

1.75

Defense mechanisms

T

210

2.91

Signal transduction mechanisms

M

192

2.65

Cell wall/membrane biogenesis

N

0

0.00

Cell motility

U

34

0.47

Intracellular trafficking and secretion

O

138

1.91

Posttranslational modification, protein turnover, chaperones

C

271

3.74

Energy production and conversion

G

318

4.39

Carbohydrate transport and metabolism

E

424

5.86

Amino acid transport and metabolism

F

105

1.45

Nucleotide transport and metabolism

H

161

2.22

Coenzyme transport and metabolism

I

187

2.58

Lipid transport and metabolism

P

177

2.44

Inorganic ion transport and metabolism

Q

141

1.95

Secondary metabolites biosynthesis, transport and catabolism

R

631

8.72

General function prediction only

S

422

5.83

Function unknown

-

2,790

38.50

Not in COGs

The total is based on the total number of protein coding genes in the genome

Insights from the genome sequence

The chemical structure of lydicamycin (Fig. 1) suggests that its carbon skeleton is assembled from eleven malonyl-CoA and six methylmalonyl-CoA precursors by type I PKS pathway. In addition, this pathway should be combined with NRPS pathway since lydicamycin bears a tetramic acid moiety derived from the condensation of an amino acid to the polyketide chain. We therefore searched for a type I PKS gene cluster consisting of seventeen PKS modules and an NRPS module. A hybrid PKS/NRPS gene cluster in scaffold03 (Table 5, Fig. 4) consists of seventeen PKS modules and one NRPS module (Fig. 5b). According to the assembly line rule [14], the predicted structure of the polyketide arising from this PKS/NRPS hybrid gene cluster was in good accordance with the actual structure of lydicamycin (Fig. 5b). As a starter unit for the polyketide assembly, 4-guanidinobutyryl CoA could be proposed on the basis of annotation of TPA0598_03_00880, TPA0598_03_00650 and TPA0598_03_00700. These genes were predicted to encode amine oxidase, acyl-CoA ligase, and transacylase by comparing the corresponding genes present in the ECO-02301 biosynthetic gene cluster. In the biosynthesis of ECO-02301, 4-aminobutyryl-CoA is supplied from L-arginine by a sequential action of amine oxidase, acyl-CoA ligase, and amidinohydrolase and is transferred to ACP by transacylase (Fig. 5a) [15]. In the lydicamycin cluster, genes for an amine oxidase (TPA0598_03_00880), an acyl-CoA ligase (TPA0598_03_00650), and a transacylase (TPA0598_03_00700) are present in the surrounding region of the PKS cluster but an amidinohydrolase gene responsible for the hydrolysis of the guanidine residue to the primary amine is lacking (Fig. 5a, Table 5). After the 4-guanidinobutyryl starter is loaded onto ACP of TPA0598_03_00840, the polyketide chain is extended by eight PKSs and a glycine is added to the polyketide terminus by an NRPS module (Fig. 5b), followed by the formation of an octalin and a tetramic acid ring (Fig. 5c). It was not possible to assign a gene responsible for the cyclization of the guanidino precursor into a pyrrolidine ring. A cytochrome P450 (TPA0598_03_00850) would be responsible for the hydroxylation of the octalin carbon at C-8 (Fig. 5c). Production of deoxy- and demethylcongeners suggests that substrate recognition by the AT domain in module3 (second module of TPA0598_03_00740) and the ER domain in module11 (first module of TPA0598_03_00780) is likely not strict (Table 6).
Table 5

Open reading frames in the lydicamycin biosynthetic gene cluster

orf (locus tag)

size (aa)

proposed function

BLAST search

protein homolog, origin, accession number

%b

TPA0598_03_00650a

473

acyl-CoA ligase

hypothetical protein, Streptomyces sp. FxanaC1, WP_018093236

94/96

TPA0598_03_00660

929

LuxR family transcriptional regulator

LuxR family transcriptional regulator, Streptomyces sp. FxanaC1, WP_026170289

91/94

TPA0598_03_00670a

274

unknown

hypothetical protein, Saccharomonospora azurea, EHY88948

53/64

TPA0598_03_00680

632

two-component system histidine kinase

hypothetical protein, Streptomyces sp. FxanaC1, WP_018093233

93/95

TPA0598_03_00690

218

two-compornent system response regulator

LuxR family transcriptional regulator, Streptomyces sp. FxanaC1, WP_018093232

99/99

TPA0598_03_00700a

336

transacylase

ACP S-malonyltransferase, Streptomyces sp. FxanaC1, WP_026170288

89/93

TPA0598_03_00710a

123

unknown

hypothetical protein, Streptomyces sp. FxanaC1, WP_018093229

88/95

TPA0598_03_00720

64

unknown

hypothetical protein JCGZ_17256, Jatropha curcas, KDP45649

43/54

TPA0598_03_00730a

80

unknown

putative protein-disulfide isomerase, Xanthomonas gardneri, EGD16922

56/63

TPA0598_03_00740

3,598

PKS

polyketide synthase, Streptomyces rapamycinicus, AGP57755

58/69

TPA0598_03_00750

7,054

PKS

Beta-ketoacyl synthase, Streptomyces violaceusniger, AEM87320

57/68

TPA0598_03_00760

3,548

PKS

Beta-ketoacyl synthase, Streptomyces violaceusniger, AEM87320

56/67

TPA0598_03_00770

1,846

PKS

Beta-ketoacyl synthase, Streptomyces iranensis, CDR09758

62/73

TPA0598_03_00780

5,648

PKS

polyketide synthase type I, Streptomyces aizunensis, AAX98191

58/69

TPA0598_03_00790

3,662

PKS

hypothetical protein, Streptomyces sp. FxanaC1, WP_018091594

94/96

TPA0598_03_00800

3,265

PKS

polyketide synthase, Streptomyces sp. PRh5, EXU66032

54/66

TPA0598_03_00810

270

unknown

hypothetical protein, Streptomyces sp. FxanaC1, WP_018091596

95/96

TPA0598_03_00820

1,031

NRPS

hypothetical protein, Streptomyces sp. FxanaC1, WP_018091598

94/96

TPA0598_03_00830

300

unknown

hypothetical protein, Streptomyces sp. FxanaC1, WP_018091598

96/98

TPA0598_03_00840

1,923

PKS

hypothetical protein, Streptomyces sp. FxanaC1, WP_018091599

91/94

TPA0598_03_00850a

429

cytochrome P450

cytochrome P450, Streptomyces sp. FxanaC1, WP_026169967

92/96

TPA0598_03_00860

260

unknown

membrane protein, Saccharopolyspora rectivirgula, KEI45939

45/69

TPA0598_03_00870

253

type-II thioesterase

hypothetical protein, Streptomyces sp. FxanaC1, WP_018091603

95/97

TPA0598_03_00880a

551

amine oxidase

amine oxidase, Streptomyces sp. FxanaC1, WP_026169968

96/98

TPA0598_03_00890

344

transcriptional regulator

hypothetical protein, Streptomyces sp. FxanaC1, WP_018091605

96/97

TPA0598_03_00900a

496

amidase

hypothetical protein, Streptomyces sp. FxanaC1, WP_018091606

94/95

aencoded in complementary strand, bidentity/similarity

Fig. 4

Genetic map of lydicamycin biosynthetic gene cluster

Fig. 5

Proposed lydicamycin synthetic pathway. a starter synthesis compared with that of ECO-02301; b chain elongation; c cyclization and modification yielding final products

Table 6

Proposed mechanism to produce lydicamycin congeners

congener

substrate of m3 AT m

m11 ER

CYP450

lydicamycin

methylmalonyl-CoA

active

involved

TPU-0037-A

malonyl-CoA

active

involved

TPU-0037-B

methylmalonyl-CoA

inactive

uninvolved

TPU-0037-C

malonyl-CoA

active

uninvolved

TPU-0037-D

methylmalonyl-CoA

active

uninvolved

Conclusions

The 8 Mb draft genome of Streptomyces sp. TP-A0598, a producer of lydicamycins isolated from seawater, has been deposited at GenBank/ENA/DDBJ under accession number BBNO00000000. We successfully identified the PKS/NRPS hybrid cluster for lydicamycin biosynthesis and proposed a plausible biosynthetic pathway. In addition, the genome of strain TP-A0598 contained seven orphan PKS or NRPS gene cluster but secondary metabolites from these orphan clusters have not been isolated yet. The genome sequence information disclosed in this study will be utilized for the investigation of additional new bioactive compounds from this strain and will also serve as a valuable reference for evaluation of the metabolic potential in marine-derived Streptomyces .

Abbreviations

Agly

Adenylation domain whose substrate is glycine

ACP: 

Acyl carrier protein domain

AT: 

Acyltransferase domain whose substrate is malonyl-CoA

ATm

AT whose substrate is methylmalonyl-CoA

C: 

Condensation domain

CoA: 

Coenzyme A

CYP450: 

Cytochrome P450

DH: 

Dehydratase domain

dh: 

Inactive DH

ER: 

Enoylreductase domain

ISP: 

International Streptomyces project

KS: 

Ketosynthase domain

KR: 

Ketoreductase domain

kr: 

Inactive KR

LM: 

Loading module

m: 

Module

MRSA: 

Methicillin-resistant Staphylococcus aureus

NRPS: 

Nonribosomal peptide synthetase

PKS: 

Polyketide synthase

T: 

Thiolation domain

TE: 

Thioesterase domain

Declarations

Acknowledgements

This research was supported by a Grant-in-aid for Scientific Research from the Ministry of Education, Culture, Sports, and Technology of Japan to Y.I. We are grateful to Ms. Machi Sasagawa for finding the lydicamycin biosynthetic gene cluster and to Dr. Moriyuki Hamada and Ms. Chiyo Shibata for taking electron micrographs. We also thank Ms. Yuko Kitahashi for finishing genome sequences and annotating PKS and NRPS genes.

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Biological Resource Center, National Institute of Technology and Evaluation (NBRC)
(2)
NBRC
(3)
Biotechnology Research Center and Department of Biotechnology, Toyama Prefectural University

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© Komaki et al. 2015