Open Access

Draft genome sequence of the cellulolytic endophyte Chitinophaga costaii A37T2T

Standards in Genomic Sciences201712:53

https://doi.org/10.1186/s40793-017-0262-2

Received: 6 January 2017

Accepted: 22 August 2017

Published: 6 September 2017

Abstract

Here we report the draft genome sequence of Chitinophaga costai A37T2T (=CIP 110584T, =LMG 27458T), which was isolated from the endophytic community of Pinus pinaster tree. The total genome size of C. costaii A37T2T is 5.07 Mbp, containing 4204 coding sequences. Strain A37T2T encoded multiple genes likely involved in cellulolytic, chitinolytic and lipolytic activities. This genome showed 1145 unique genes assigned into 109 Cluster of Orthologous Groups in comparison with the complete genome of C. pinensis DSM 2588T. The genomic information suggests the potential of the strain A37T2T to interact with the plant metabolism. As there are only a few bacterial genomes related to Pine Wilt Disease, this work provides a contribution to the field.

Keywords

Chitinophaga costaii A37T2CellulaseChitinaseGenome sequence

Introduction

The genus Chitinophaga belongs to the family Chtiniphagaceae (phylum Bacteroidetes ) alongside with the genera Arachidicoccus , Asinibacterium , Balneola , Cnuella , Crenotalea , Ferruginibacter , Filimonas , Flaviaesturariibacter , Flavihumibacter , Flavisolibacter , Flavitalea , Gracilimonas , Heliimonas , Hydrotalea , Lacibacter , Niabella , Niastella , Parasediminibacterium , Parasegetibacter , Sediminibacterium , Segetibacter , Taibaiella , Terrimonas , Thermoflavifilum and Vibriomonas. The genus Chitinophaga is widely distributed in the environment and strains of this genus have been isolated from pine trees, soil, rhizosphere soil, roots, vermicompost and weathered rock [1]. Twenty-four species belonging to the genus Chitinophaga have been described [2], and only the type species of the genus C. pinensis has the complete genome sequenced [3].

Pinus pinaster trees from Central Portugal present a diverse endophytic microbial community. Strain A37T2T was isolated as part of the endophytic microbiome of pine trees affected by Pine Wilt Disease (PWD) which is a world devastating disease, consequence of Bursaphelenchus xylophilus colonization in pine trees [4]. Here, we show the second genome of the genus Chitinophaga , a draft genome of Chitinophaga costaii A37T2T, previously isolated as endophyte of Pinus pinaster affected by PWD [1].

Organism information

Classification and features

The type strain A37T2T (=CIP 110584 T =LMG 27458 T), was isolated from tree trunk of a Pinus pinaster tree affected by PWD and it described as Chitinophaga costaii (family Chitinophagaceae , phylum Bacteroidetes ) [1]. It was Gram-stain-negative, facultative anaerobic, non-motile, formed rod-shaped cells, 0-5-1 μm in diameter and 1-8 μm in length after 48 h on R2A agar media (Fig. 1). Showed capacity to grow on R2A agar medium at 15-45 °C (optimum, 26-30 °C), at pH 5.5-8.0 (optimum, pH 7) and supplemented with up to 1% (w/v) NaCl (optimum without NaCl). The major fatty acids (>25%) showed by the strain A37T2T are saturated iso-C15: 0 and unsaturated C16: 1 ω5c . The major polar lipids were identified as phosphatidylethanolamine, two unidentified aminophospholipids and one unidentified lipid. No glycolipid was detected. The menaquinone 7 (MK-7) was shown as the major respiratory lipoquinone. The determined DNA G + C content of the C. costaii A37T2T was 46.6 mol%. Key features of this microorganism are summarized in Table 1. A phylogenetic tree based on the 16S rRNA gene sequence of this strain and its closest relative members are given in Fig. 2. The sequences were aligned by SINA (v1.2.9) using the SILVA SEED as reference alignment [5]. Sequences were included in 16S rRNA-based Living Tree Project (LTP) release 115 database [6] by parsimony implemented in the ARB software package version 5.5 [7]. Evolutionary distances were calculated [8] and phylogenetic dendrograms were constructed using the neighbor-joining [9] and Randomized Axelerated Maximum Likelihood (RAxML) method with GTRGAMMA model [10] included in the ARB software [7]. Trees topologies were evaluated by performing bootstrap analysis [11] of 1000 data sets by using ARB software package.
Fig. 1

Scanning electron micrograph of C. costaii A37T2T after 48 h of growth on R2A agar plates at 30 °C

Table 1

Classification and general features of Chitinophaga costaii A37T2T according to the MIGS recommendations [26]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [27]

  

Phylum Bacteroidetes

TAS [28, 29]

  

Class Sphingobacteriia

TAS [28, 30]

  

Order Sphingobacteriales

TAS [28, 31]

  

Family Chitinophagaceae

TAS [32]

  

Genus Chitinophaga

TAS [33]

  

Species Chitinophaga costaii

TAS [1]

  

Type strain: A37T2T (=CIP 110584T, =LMG 27458T)

 
 

Gram stain

Negative

TAS [1]

 

Cell shape

Rod

TAS [1]

 

Motility

Non-motile

TAS [1]

 

Sporulation

Not reported

NAS

 

Temperature range

15-45 °C

TAS [1]

 

Optimum temperature

26-30 °C

TAS [1]

 

pH range; Optimum

5.5-8.0; 7

TAS [1]

 

Carbon source

Glucose

TAS [1]

MIGS-6

Habitat

Endophyte of Pinus pinaster tree

TAS [1]

MIGS-6.3

Salinity

1.0% NaCl (w/v)

TAS [1]

MIGS-22

Oxygen requirement

Facultative anaerobic

TAS [1]

MIGS-15

Biotic relationship

Free-living

TAS [1]

MIGS-14

Pathogenicity

Non-pathogen

NAS

MIGS-4

Geographic location

Portugal

TAS [1]

MIGS-5

Sample collection

July, 2009

NAS

MIGS-4.1

Latitude

40.2962266

NAS

MIGS-4.2

Longitude

−7.9207357

NAS

MIGS-4.4

Altitude

217 m

NAS

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 from the Gene Ontology project [34]

Fig. 2

Phylogenetic tree based on a comparison of the 16S rRNA gene sequence of strain A37T2T and the other type strains within the family Chitinophagaceae. The tree was created using the maximum likelihood method (RAxML). The numbers on the tree indicate the percentages of bootstrap sampling, derived from 1000 replications; values below 50% are not shown. Symbol (•) indicates node branches conserved when the tree was reconstructed using the neighbor-joining method. The isolate characterized in this study is indicated in bold. Scale bar, 1 inferred nucleotide substitution per 100 nucleotides

Genome sequencing information

Genome project history

This Whole Genome Shotgun project has been deposited at ENA under the accession numbers FMAR01000001-FMAR01000056 and in the Integrated Microbial Genomes database (IMG) with Biosample ID SAMN05216457 [12]. The genome sequencing of this organism is part of the Genomic Encyclopedia of Bacteria and Archaea [13], 1000 Microbial Genomes project, phase III (KMG-III) [14], at the U.S. Department of Energy, Joint Genome Institute (JGI). The project information and its association with the MIGS is summarized in Table 2.
Table 2

Project information

MIGS ID

Property

Term

MIGS 31

Finishing quality

Draft

MIGS-28

Libraries used

Illumina Regular Fragment, 300 bp, Tubes

MIGS 29

Sequencing platforms

Illumina HiSeq 2500-1 TB

MIGS 31.2

Fold coverage

297.2

MIGS 30

Assemblers

SPAdes

MIGS 32

Gene calling method

NCBI Prokaryotic Genome Annotation Pipeline

 

Locus Tag

GA0116948

 

Genbank ID

FMAR00000000

 

GenBank Date of Release

August 3, 2016

 

GOLD ID

Gp0139259

 

BIOPROJECT

PRJNA322901

MIGS 13

Source Material Identifier

A37T2T

 

Project relevance

GEBA-KMG

Growth conditions and genomic DNA preparation

The strain A37T2T was grown on R2A agar media at 30 °C during 48 h and its genomic DNA was extracted using the E.Z.N.A. Bacterial DNA Kit (Omega Bio-Tek, Norcross, GA, USA) according to the manufacturer’s instructions.

Genome sequencing and assembly

The draft genome of C. costaii A37T2T was generated at the DOE Joint Genome Institute (JGI) using the Illumina technology [15]. An Illumina 300 bp insert standard shotgun library was constructed and sequenced using the Illumina HiSeq–2500 1 TB platform, generating 9,965,394 reads totaling 1494.8 Mbp. All general aspects of library construction and sequencing performed at the JGI can be found at [16]. All raw Illumina sequence data was filtered using BBDuk [17], which removes known Illumina artifacts and PhiX. Reads with more than one “N” or with quality scores (before trimming) averaging less than 8 or reads shorter than 51 bp (after trimming) were discarded. Remaining reads were mapped to masked versions of human, cat and dog references using BBMAP [17] and discarded if identity exceeded 95%. Sequence masking was performed with BBMask [17]. Following steps were then performed for assembly: (1) artifact filtered Illumina reads were assembled using SPAdes (version 3.6.2) [18]; (2) assembled contigs were discarded if length was <1 kbp. Parameters for the SPAdes assembly were ––cov–cutoff auto ––phred–offset 33 –t 8 –m 40 ––careful –k 25,55,95 ––12.

Genome annotation

Protein-coding genes were identified using Prodigal [19], as part of the DOE-JGI genome annotation pipeline [20]. Additional gene prediction analysis and manual functional annotation were performed within the Integrated Microbial Genomes Expert Review system (IMG-ER), which provides tools for analyzing and reviewing the structural and functional annotations of genomes in a comparative context [12, 21]. Genome annotation procedures are detailed in Markowitz et al. [12] and references therein. Briefly, the predicted CDSs were translated and used to search the NCBI nonredundant database, UNIProt, TIGRFam, Pfam, KEGG, COG and InterPro databases. Transfer RNA genes were identified using the tRNAScan-SE tool and other non-coding RNAs were found using INFERNAL. Ribosomal RNA genes were predicted using hmmsearch against the custom models generated for each type of rRNA.

Genome properties

The draft genome sequence of C. costaii strain A37T2T comprised 5,074,440 bp, based on 1494.8 Mbp of Illumina data with a mapped coverage of 297.2-fold of the genome. The final draft assembly contained 56 contigs in 56 scaffolds with more than 1052 bp. The G + C content was 47.6%. The genome encoded 4204 putative coding sequences (CDSs) (Table 3). Fifty four % of the CDSs, corresponding to 2284 proteins, could be assigned to Cluster of Orthologous Groups (COG) families [22] (Table 4). The draft genome sequence contained four ribosomal RNAs and 50 tRNAs loci (Table 3).
Table 3

General genome features of Chitinophaga costaii A37T2T

Attribute

Value

% of Total

Genome size (bp)

5,074,440

100.00

DNA coding (bp)

4,431,743

87.33

DNA G + C (bp)

2,413,598

47.56

DNA scaffolds

56

100.00

Total genes

4274

100.00

Protein coding genes

4204

98.36

RNA genes

70

1.64

Genes in internal clusters

824

19.28

Genes with function prediction

3041

71.15

Genes assigned to COGs

2284

53.44

Genes with Pfam domains

1976

61.75

Genes with signal peptides

651

15.23

Genes with transmembrane helices

972

22.74

CRISPR repeats

3

0.00

Table 4

Number of genes associated with general COG functional categories

Code

Value

%age

Description

J

186

7.42

Translation, ribosomal structure and biogenesis

A

0

0.00

RNA processing and modification

K

215

8.58

Transcription

L

90

3.50

Replication, recombination and repair

D

19

0.76

Cell cycle control, Cell division, chromosome partitioning

V

98

3.91

Defense mechanisms

T

114

4.55

Signal transduction mechanisms

M

211

8.42

Cell wall/membrane biogenesis

N

12

0.48

Cell motility

U

20

0.80

Intracellular trafficking and secretion

O

136

5.42

Posttranslational modification, protein turnover, chaperones

C

126

5.03

Energy production and conversion

G

165

6.58

Carbohydrate transport and metabolism

E

196

7.82

Amino acid transport and metabolism

F

69

2.75

Nucleotide transport and metabolism

H

141

5.62

Coenzyme transport and metabolism

I

125

4.99

Lipid transport and metabolism

P

150

5.98

Inorganic ion transport and metabolism

Q

70

2.79

Secondary metabolites biosynthesis, transport and catabolism

R

248

9.89

General function prediction only

S

104

4.15

Function unknown

-

1990

46.56

Not in COGs

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

The Average Nucleotide Identity between C. costaii A37T2T and C. pinensis DSM 2588 T was 70.9 based on 1593 of total Bidirectional Best Hits, using MiSI [23]. Figure 3 shows the circular graph of the genome of C. costaii A37T2T query to the only available complete genome of the genus Chitinophaga , C. pinensis DSM 2588 T [2].
Fig. 3

The genome of Chitinophaga costaii A37T2T. From outside to the center: genes of genome of C. pinensis DSM 2588T and its similarity with the genome of C. costaii (50-100%), GC content of C. costaii A37T2T, GC skew of C. costaii A37T2T, genome of C. costaii A37T2T

The comparison between the draft genome of C. costaii A37T2T and the complete genome of C. pinensis DSM 2588 T showed 1145 unique genes only present in the genome of C. costaii A37T2T and 3493 unique genes only present in the genome of C. pinensis DSM 2588 T. Focused on the unique genes present on the genome of strain A37T2T it was possible to assigned 109 COG, summarized in Table 5.
Table 5

Unique Cluster Orthologous Groups present in the genome of C. costaii A37T2T

Catergory Code

Catergory

COG ID

C

Energy production and conversion

COG0280, COG0374, COG0680, COG1740

E

Amino acid transport and metabolism

COG1027, COG1586, COG2355, COG3104

F

Nucleotide transport and metabolism

COG0027

G

Carbohydrate transport and metabolism

COG0021, COG0058, COG0588, COG0662, COG0837, COG1080, COG1803, COG1925, COG2079, COG2893, COG3444, COG3716, COG3934

H

Coenzyme transport and metabolism

COG0561, COG1056, COG2091, COG2227, COG2329

I

Lipid transport and metabolism

COG0671, COG0821, COG2246

J

Translation, ribosomal structure and biogenesis

COG0060, COG0255, COG0257, COG0267, COG0268, COG0333, COG4680

K

Transcription

COG1476, COG4933

L

Replication, recombination and repair

COG0863, COG1722

M

Cell wall/membrane/envelope biogenesis

COG1083, COG1922, COG2089, COG2829, COG2982, COG3511, COG3637

O

Posttranslational modification, protein turnover, chaperones

COG0068, COG0298, COG0309, COG0409

P

Inorganic ion transport and metabolism

COG0428, COG1218, COG1230, COG1416, COG4772

Q

Secondary metabolites biosynthesis, transport and catabolism

COG2130, COG2162, COG3733, COG4242

R

General function prediction only

COG0312, COG0375, COG0429, COG0457, COG1062, COG1373, COG2320, COG3153, COG3488, COG4674, COG0561, COG2130, COG4242

S

Function unknown

COG0393, COG1286, COG2442, COG2962, COG3219, COG3247, COG3310, COG3361, COG3461, COG3477, COG3487, COG3489, COG3528, COG3548, COG3918, COG3943, COG4487, COG4700, COG4859, COG4924

T

Signal transduction mechanisms

COG0517, COG2184, COG2203, COG3292, COG1925

U

Intracellular trafficking, secretion, and vesicular transport

COG1272, COG1826, COG3451

V

Defense mechanisms

COG0286, COG0610, COG0732, COG3512, COG3513, COG4823, COG5499

X

Mobilome: prophages, transposons

COG3385, COG3436, COG3600, COG3654

Insights from the genome sequence

The draft genome sequence of C. costaii A37T2T carries multiple genes involved in cellulolytic activity, including one gene encoding the enzyme cellulase (SCC15587) and six genes encoding for β-glucosidase (SCB82491, SCB92249, SCB95191, SCC15475, SCC57293, SCC61957), which might be involved in cellulose degradation in the environment and in biotechnological processes [24]. As expected for this genus, four genes encoding chitinases (SCC19468, SCC19522, SCC23114, SCC34676) were found. Six genes encoded lysophospholipase L1, including representatives of both of size groups, i.e. less than 300aa (SCB77875, SCC28514, SCC37316, SCC54197) and less than 500aa (SCB98645, SCC50813). Moreover, the genome of strain A37T2T encoded 1-aminocyclopropane-1-carboxylate deaminase (SCB80758), a hydrolase that might be involved in lowering ethylene levels in the plant [25]. In summary, the genome sequence suggested multiple potentials for the strain to interact with the plant metabolism.

Conclusions

This work contributed to the knowledge of the genome sequence of the type species of C. costaii A37T2T (=CIP 110584 T, =LMG 27458 T), an endophyte of P. pinaster affected by PWD. The genome encoded multiple genes involved in cellulolytic activity and the sequence provided insights into the role of bacteria in PWD. As there are only a few bacterial genomes related to PWD, this work provides a contribution to this field.

Abbreviations

PWD: 

Pine wilt disease

PWN: 

Pinewood nematode

Declarations

Funding

We thank to Ana Paula Piedade for SEM analysis. This work was supported by CEMMPRE and by Fundação para a Ciência e a Tecnologia (FCT) under the project UID/EMS/00285/2013. D.N.P. was supported by FCT, postdoctoral fellowship SFRH/BPD/100721/2014. The work conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231.

Authors’ contributions

DNP isolated the strain, extracted the DNA, performed laboratory experiments, analyzed all the data, and with PVM wrote the manuscript. WBW, NS, TW and NCK did the genome sequencing, assembly and annotation. WBW, NS, TW and NCK revise the manuscript. All the authors read and approved the final manuscript.

Competing interests

The authors have no competing of interests to declare.

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Authors’ Affiliations

(1)
CEMMPRE, University of Coimbra
(2)
Department of Microbiology, 527 Biological Sciences Building, University of Georgia
(3)
DOE Joint Genome Institute 2800 Mitchell Drive
(4)
Department of Life Sciences, FCTUC, Faculty of Sciences and Technology, University of Coimbra

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Copyright

© The Author(s). 2017