Open Access

Complete genome sequence of Thermomonospora curvata type strain (B9T)

  • Olga Chertkov1, 2,
  • Johannes Sikorski3,
  • Matt Nolan1,
  • Alla Lapidus1,
  • Susan Lucas1,
  • Tijana Glavina Del Rio1,
  • Hope Tice1,
  • Jan-Fang Cheng1,
  • Lynne Goodwin1, 2,
  • Sam Pitluck1,
  • Konstantinos Liolios1,
  • Natalia Ivanova1,
  • Konstantinos Mavromatis1,
  • Natalia Mikhailova1,
  • Galina Ovchinnikova1,
  • Amrita Pati1,
  • Amy Chen4,
  • Krishna Palaniappan4,
  • Olivier D. Ngatchou Djao5,
  • Miriam Land1, 6,
  • Loren Hauser1, 6,
  • Yun-Juan Chang1, 6,
  • Cynthia D. Jeffries1, 6,
  • Thomas Brettin1, 6,
  • Cliff Han1, 2,
  • John C. Detter1, 2,
  • Manfred Rohde5,
  • Markus Göker3,
  • Tanja Woyke1,
  • James Bristow1,
  • Jonathan A. Eisen1, 7,
  • Victor Markowitz4,
  • Philip Hugenholtz1, 8,
  • Hans-Peter Klenk3 and
  • Nikos C. Kyrpides1
Standards in Genomic Sciences20154:4010013

DOI: 10.4056/sigs.1453580

Published: 30 October 2015

Abstract

Thermomonospora curvata Henssen 1957 is the type species of the genus Thermomonospora. This genus is of interest because members of this clade are sources of new antibiotics, enzymes, and products with pharmacological activity. In addition, members of this genus participate in the active degradation of cellulose. This is the first complete genome sequence of a member of the family Thermomonosporaceae. Here we describe the features of this organism, together with the complete genome sequence and annotation. The 5,639,016 bp long genome with its 4,985 protein-coding and 76 RNA genes is a part of the Genomic Encyclopedia of Bacteria and Archaea project.

Keywords

chemoorganotroph facultative aerobe eurythermal thermophile mycelium Gram-positive cellulose degradation Thermomonosporaceae GEBA

Introduction

Strain B9T (= DSM 43183 = ATCC 19995 = JCM 3096) is the type strain of Thermomonospora curvata, which in turn is the type species of the genus Thermomonospora [1]. T. curvata was effectively published in 1957 [1]. When the original strains R30 and R71 were no longer cultivable, strain B9 was proposed as the neotype in 1967 [2]. Currently, there are two species in the genus Thermomonospora, which in turn is one of the six genera in the family Thermomonosporaceae [3]. The generic name Thermomonospora was proposed by Henssen [1] for thermophilic actinomycetes isolated from composted stable manure [4]. Strain B9T was isolated from municipal refuse compost samples [1]. Other (rubber degrading) strains of T. curvata have been isolated from food residues used in animal husbandry in Egypt (strain E4), from compost in Germany (strain E5) [5], and also from municipal solid waste compost (probably USA) [69]. Cellulase biosynthesis has been studied in a catabolite repression-resistant mutant of T. curvata [10]. Here we present a summary classification and a set of features for T. curvata strain B9T, together with the description of the complete genomic sequencing and annotation.

Classification and features

The 16S rRNA gene sequence of the strain B9T (AF002262) shows 98.1% identity with the 16S rRNA gene sequence of T. curvata strain E5 (AY525766) [5].The distance of strain B9T to other members of this family ranged between 5% and 7%. Further analysis shows 94% 16S rRNA gene sequence identity with an uncultured bacterium, clone BG079 (HM362496) and 92% similarity to compost metagenome contig00434 (ADGO01000428) [11] from metagenomic libraries (env_nt) (status October 2010). A representative genomic 16S rRNA sequence of T. curvata was compared using NCBI BLAST under default settings (e.g., considering only the high-scoring segment pairs (HSPs) from the best 250 hits) with the most recent release of the Greengenes database [12] and the relative frequencies, weighted by BLAST scores, of taxa and keywords (reduced to their stem [13]) were determined. The five most frequent genera were Actinomadura (54.3%), Nocardiopsis (12.5%), Actinocorallia (8.8%), Jiangella (5.8%) and Actinoallomurus (5.0%) (208 hits in total). Regarding the two hits to sequences from members of the species, the average identity within HSPs was 99.9%, whereas the average coverage by HSPs was 96.2%. Regarding the single hit to sequences from other members of the genus, the average identity within HSPs was 95.2%, whereas the average coverage by HSPs was 58.4%. Among all other species, the one yielding the highest score was Actinomadura cremea, which corresponded to an identity of 96.3% and a HSP coverage of 85.3%. The highest-scoring environmental sequence was HM362496 (‘microbial naturally composting sugarcane piles decomposting bagasse clone BG079’), which showed an identity of 94.5% and a HSP coverage of 96.3%. Within the labels of environmental samples which yielded hits, the five most frequent keywords were ‘soil’ (4.7%), ‘compost’ (3.1%), ‘microbi’ (2.4%), ‘skin’ (2.0%) and ‘acid’ (2.0%) (41 hits in total). These keywords partially fit to the ecology of compost and food residues, from which the known strains have been isolated [1,5,6]. Environmental samples which yielded hits of a higher score than the highest scoring species were not found.

Figure 1 shows the phylogenetic neighborhood of T. curvata B9T in a 16S rRNA based tree. The sequences of the four 16S rRNA gene copies in the genome differ from each other by up to one nucleotide, and differ by up to five nucleotides from the previously published 16S rRNA sequence (D86945), which contains one ambiguous base call.
Figure 1.

Phylogenetic tree highlighting the position of L. byssophila relative to the type strains of the other genera within the family Cytophagaceae. The tree was inferred from 1,340 aligned characters [1516] of the 16S rRNA gene sequence under the maximum likelihood criterion [17] and rooted with the type strain of the closely related family Sphingobacteriaceae. The branches are scaled in terms of the expected number of substitutions per site. Numbers above branches are support values from 900 bootstrap replicates [18] if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [19] are shown in blue, published genomes in bold [4,20,21].

Strain B9T is facultatively aerobic, Gram-positive, non-acid-alcohol-fast, and chemoorganotrophic [1,4 Table 1]. Based on the original literature, the morphology of neotype B9T was the same as of the original strains [12]. Substrate mycelium was branched and bared aerial hyphae that differentiated into single or short chains of arthrospores [24] (Figure 2, arthrospores not visible). Spores were formed by the differentiation of the sporophores when they reached a given width [2]. Polymorphic and single spores in clusters appeared with a folded surface on branched and unbranched sporophores [2]. They had spindle, lemon or pear forms varying between 0.6–1.5 x 0.3–0.9 µm [2]. The optimal growth occurred at 50°C. However, weak growth was observed at 40°C and 65°C, but no growth at 28°C [2]. Colonies were white or yellow depending on culture medium [2]. On meat extract agar, the growth was moderate, aerial white mycelium formed and the colonies were yellow to brown [2]. On asparagine glucose agar, the growth was low and the aerial mycelium white [2]. On casein glucose agar, a few single colonies were observed [2]. The growth was good and the aerial mycelium white on cellulose agar medium [2]. On Czapek agar, a few spotty colonies were observed [2]. On Czapek peptone agar, the growth was good, almost no aerial mycelium formation [2]. When oatmeal agar was used as medium, the growth was good and the aerial mycelium white [2]. The growth on yeast agar was good, with thick aerial mycelium. In this case, colonies were partially yellow [2]. On yeast glucose agar, the growth was good, aerial mycelium developed later and was white while brownish colonies were formed [2]. On yeast starch agar, the growth was good, white aerial mycelium was formed and colonies were yellow to orange [2]. On potato agar I, spotty growth is observed, while no aerial mycelium was formed [2]. Few single colonies formed on potato agar II [2]. On starch agar medium, the growth was moderate and aerial mycelium was white [2]. Strain B9T showed endogluconase activity and attacks cellulose [4]. It was also active in the decomposition of municipal waste compost [69]. When grown on protein-extracted lucerne fiber compound, strain B9T released 16 times more β-glucosidases compared to growth on cellulose or purified cellulose [34]. Strain B9T grew well at pH 7.5 on any nutrient medium that contains some yeast extract. It showed significant growth even at pH 11 [35]. Tests of the nitrate reduction and phosphatase were positive [4]. The sole carbon sources (1%, w/v) were ribose and sucrose. L-arabinose, galactose, lactose and mannitol were not used [4]. Strain B9T was able to degrade agar, cellulose powder (MN300), carboxymethylcellulose, keratin, xylan, starch, Tween 20 and Tween 80 [4]. Growth was also observed in the presence of crystal violet (0.2 µg/ml), but it was inhibited by kanamycin and novobiocin (each 25µg/ml) [4]. The inability to utilize pectin is an important feature that differentiates strain B9T from other members of the genus Thermomonospora. Amylases of the strain B9T were extremely active and stable at 60–70°C and slightly acid to neutral pH [3638]. Also, endoglucanase and exoglucanase were active in the strain [39]. Cellobiose was found to be a good cellulase inducer [40].
Figure 2.

Scanning electron micrograph of L. byssophila 4M15T

Table 1.

Classification and general features of T. curvata B9T according to the MIGS recommendations [22]

MIGS ID

Property

Term

Evidence code

 

Current classification

Domain Bacteria

TAS [23]

 

Phylum Actinobacteria

TAS [24]

 

Class Actinobacteria

TAS [25]

 

Order Actinomycetales

TAS [2528]

 

Family Thermomonosporaceae

TAS [25,28,29]

 

Genus Thermomonospora

TAS [1,27,30,31]

 

Species Thermomonospora curvata

TAS [1,27]

 

Type strain B9

TAS [2]

 

Gram stain

positive

TAS [1]

 

Cell shape

mycelium

TAS [1]

 

Motility

not mobile

NAS

 

Sporulation

yes

TAS [1]

 

Temperature range

40°C–65°C

TAS [1]

 

Optimum temperature

50°C

TAS [1]

 

Salinity

not reported

NAS

MIGS-22

Oxygen requirement

facultative aerobic

TAS

 

Carbon source

ribose and sucrose

TAS [4]

 

Energy source

chemoorganotroph

TAS [1]

MIGS-6

Habitat

compost, overheated vegetable material, straw

TAS [4]

MIGS-15

Biotic relationship

not reported

NAS

MIGS-14

Pathogenicity

no

TAS [4]

 

Biosafety level

1

TAS [32]

 

Isolation

rye straw

TAS [1]

MIGS-4

Geographic location

unknown, but most probably Berlin, Germany

TAS [1]

MIGS-5

Sample collection time

1959

TAS [1]

MIGS-4.1

Latitude

52.5

NAS

MIGS-4.2

Longitude

13.4

 

MIGS-4.3

Depth

not reported

NAS

MIGS-4.4

Altitude

approx. 34–115 m above sea level

NAS

Evidence codes - IDA: Inferred from Direct Assay (first time in publication); 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 from of the Gene Ontology project [33]. If the evidence code is IDA, then the property was directly observed by one of the authors or an expert mentioned in the acknowledgements

Chemotaxonomy

Strain B9T possesses a cell wall type III with A1γ and with meso-diaminopimelic acid as major constituent [4,41,42]. The principal menaquinones are MK-9(H4), MK-9(H6) and MK-9(H8), with MK-9(H6) being the predominant one (the profile type sensu Kroppenstedt is termed 4B2 [43]) [4]. The fatty acid profile was described to be of type 3a [4]. Members of this type can synthesize terminally branched and 10-methyl-branched fatty acids [43]. T. curvata lacks madurose, a type C sugar and has polar lipids of type IV [4], represented by phosphatidylinositol (PI) and unknown phospholipids (PL), which according to Lechevalier [4445] are, phosphatidyglycerol (PE), phosphatidylinositolmannosides(PIM) and diphosphatidylglycerol (DPG) [4].

Genome sequencing and annotation

Genome project history

This organism was selected for sequencing on the basis of its phylogenetic position [46], and is part of the Genomic Encyclopedia of Bacteria and Archaea project [47]. The genome project is deposited in the Genomes OnLine Database [19] and the complete genome sequence is deposited in GenBank. Sequencing, finishing and annotation were performed by the DOE Joint Genome Institute (JGI). A summary of the project information is shown in Table 2.
Table 2.

Genome sequencing project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

Finished

MIGS-28

Libraries used

One Sanger 6 kb pMCL200 library, one 454 pyrosequence standard library and one Illumina standard library

MIGS-29

Sequencing platforms

ABI3730, 454 GS FLX, Illumina GAii

MIGS-31.2

Sequencing coverage

9.7 × Sanger; 26.6 × pyrosequence

MIGS-30

Assemblers

Newbler version 1.1.02.15, phrap

MIGS-32

Gene calling method

Prodigal 1.4, GenePRIMP

 

INSDC ID

CP001738

 

Genbank Date of Release

November 19, 2009

 

GOLD ID

Gc01146

 

NCBI project ID

20825

 

Database: IMG-GEBA

646311963

MIGS-13

Source material identifier

DSM 43183

 

Project relevance

Tree of Life, GEBA

Growth conditions and DNA isolation

T. curvata B9T, DSM 43183, was grown in DSMZ medium 550 (CYC medium, modified following Cross and Attwell, 1973) [48] at 45°C. DNA was isolated from 0.5–1 g of cell paste using MasterPure Gram-positive NDA purification kit (Epicentre MGP04100) following the standard protocol as recommended by the manufacturer, with modification st/LALM for cell lysis as described in Wu et al. [47]. DNA is available through the DNA bank Network [4950].

Genome sequencing and assembly

The genome of was sequenced using a combination of Sanger and 454 sequencing platforms. All general aspects of library construction and sequencing can be found at the JGI website [51]. Pyrosequencing reads were assembled using the Newbler assembler version 1.1.02.15 (Roche). Large Newbler contigs were broken into 6,203 overlapping fragments of 1,000 bp and entered into assembly as pseudo-reads. The sequences were assigned quality scores based on Newbler consensus q-scores with modifications to account for overlap redundancy and adjust inflated q-scores. A hybrid 454/Sanger assembly was made using the parallel phrap (High Performance Software, LLC). Possible mis-assemblies were corrected with Dupfinisher [52] or transposon bombing of bridging clones (Epicentre Biotechnologies, Madison, WI). A total of 2,673 Sanger finishing reads were produced to close gaps, to resolve repetitive regions, and to raise the quality of the finished sequence. Illumina reads that were used to correct potential base errors and increase consensus quality using a software Polisher developed at JGI [53]. The error rate of the completed genome sequence is less than 1 in 100,000. Together, the combination of the Sanger and 454 sequencing platforms provided 36.3 × coverage of the genome. The final assembly contains 73,067 Sanger reads and 602,893 pyrosequencing reads.

Genome annotation

Genes were identified using Prodigal [54] as part of the Oak Ridge National Laboratory genome annotation pipeline, followed by a round of manual curation using the JGI GenePRIMP pipeline [55]. The predicted CDSs were translated and used to search the National Center for Biotechnology Information (NCBI) nonredundant database, UniProt, TIGRFam, Pfam, PRIAM, KEGG, COG, and InterPro databases. Additional gene prediction analysis and functional annotation was performed within the Integrated Microbial Genomes - Expert Review (IMG-ER) platform [56].

Genome properties

The genome consists of a 5,639,016 bp long chromosome with a 71.6% GC content (Table 3 and Figure 3). Of the 5,061 genes predicted, 4,985 were protein-coding genes, and 76 RNAs; ninety five pseudogenes were also identified. The majority of the protein-coding genes (64.7%) were assigned with a putative function while the remaining ones were annotated as hypothetical proteins. The distribution of genes into COGs functional categories is presented in Table 4.
Figure 3.

Graphical circular map of the genome. From outside to the center: Genes on forward strand (color by COG categories), Genes on reverse strand (color by COG categories), RNA genes (tRNAs green, rRNAs red, other RNAs black), GC content, GC skew.

Table 3.

Genome Statistics

Attribute

Value

% of Total

Genome size (bp)

5,639,016

100.00%

DNA coding region (bp)

4,739,306

84.04%

DNA G+C content (bp)

4,039,905

71.64%

Number of replicons

1

 

Extrachromosomal elements

0

 

Total genes

5,061

100.00%

RNA genes

76

1.50%

rRNA operons

4

 

Protein-coding genes

4,985

98.50%

Pseudo genes

95

1.88%

Genes with function prediction

3,275

64.71%

Genes in paralog clusters

895

17.68%

Genes assigned to COGs

3,274

64.69%

Genes assigned Pfam domains

3,647

72.06%

Genes with signal peptides

1,418

28.02%

Genes with transmembrane helices

1,089

21.52%

CRISPR repeats

12

 
Table 4.

Number of genes associated with the general COG functional categories

Code

value

%age

Description

J

169

4.5

Translation, ribosomal structure and biogenesis

A

2

0.1

RNA processing and modification

K

382

10.1

Transcription

L

174

4.6

Replication, recombination and repair

B

1

0.0

Chromatin structure and dynamics

D

41

1.1

Cell cycle control, cell division, chromosome partitioning

Y

0

0.0

Nuclear structure

V

68

1.8

Defense mechanisms

T

270

7.2

Signal transduction mechanisms

M

159

4.2

Cell wall/membrane/envelope biogenesis

N

2

0.1

Cell motility

Z

2

0.1

Cytoskeleton

W

0

0.0

Extracellular structures

U

38

1.0

Intracellular trafficking and secretion, and vesicular transport

O

134

3.6

Posttranslational modification, protein turnover, chaperones

C

256

6.8

Energy production and conversion

G

193

5.1

Carbohydrate transport and metabolism

E

292

7.7

Amino acid transport and metabolism

F

78

2.1

Nucleotide transport and metabolism

H

161

4.3

Coenzyme transport and metabolism

I

265

6.8

Lipid transport and metabolism

P

160

4.2

Inorganic ion transport and metabolism

Q

181

4.8

Secondary metabolites biosynthesis, transport and catabolism

R

511

13.5

General function prediction only

S

243

6.4

Function unknown

-

1,787

35.3

Not in COGs

Declarations

Acknowledgements

We would like to gratefully acknowledge the help of Marlen Jando for growing T. curvata cultures and Susanne Schneider for DNA extraction and quality analysis (both at DSMZ). This work was performed under the auspices of the US Department of Energy Office of Science, Biological and Environmental Research Program, and by the University of California, Lawrence Berkeley National Laboratory under contract No. DE-AC02-05CH11231, Lawrence Livermore National Laboratory under Contract No. DE-AC52-07NA27344, and Los Alamos National Laboratory under contract No. DE-AC02-06NA25396, UT-Battelle and Oak Ridge National Laboratory under contract DE-AC05-00OR22725, as well as German Research Foundation (DFG) INST 599/1-1.

Authors’ Affiliations

(1)
DOE Joint Genome Institute
(2)
Bioscience Division, Los Alamos National Laboratory
(3)
DSMZ - German Collection of Microorganisms and Cell Cultures GmbH
(4)
Biological Data Management and Technology Center, Lawrence Berkeley National Laboratory
(5)
HZI - Helmholtz Centre for Infection Research
(6)
Oak Ridge National Laboratory
(7)
University of California Davis Genome Center
(8)
Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland

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