Open Access

The complete genome sequence of the cold adapted crude-oil degrader: Pedobacter steynii DX4

  • Sijing Chang1, 2, 3,
  • Gaosen Zhang3, 4,
  • Ximing Chen3, 4,
  • Haozhi Long4, 5,
  • Yilin Wang5,
  • Tuo Chen2, 3Email author and
  • Guangxiu Liu3, 4
Standards in Genomic Sciences201712:45

https://doi.org/10.1186/s40793-017-0249-z

Received: 19 October 2016

Accepted: 29 June 2017

Published: 27 July 2017

Abstract

Pedobacter steynii DX4 was isolated from the soil of Tibetan Plateau and it can use crude oil as sole carbon and energy source at 15 °C. The genome of Pedobacter steynii DX4 has been sequenced and served as basis for analysis its metabolic mechanism. It is the first genome of crude oil degrading strain in Pedobacter genus. The 6.58 Mb genome has an average G + C content of 41.31% and encodes 5464 genes. In addition, annotation revealed that Pedobacter steynii DX4 has cold shock proteins, abundant response regulators for cell motility, and enzymes involved in energy conversion and fatty acid metabolism. The genomic characteristics could provide information for further study of oil-degrading microbes for recovery of crude oil polluted environment.

Keywords

Pedobacter Crude oil Degradation Genome

Introduction

The crude oil spills occur frequently and they bring serious pollution to the terrestrial and marine environments [1, 2]. In the bioremediation of crude oil contamination, bacteria work as primary degraders [35]. Numerous strains be capable of degrading hydrocarbons have been singled out and identified from marine and terrestrial environments [68]. It was also reported that in oil polluted areas, Pedobacter is one of the major members of alkane degrading bacterial communities [911]. For the first time in Pedobacter genus, a cultured Pedobacter cryoconitis strain was described to have the ability to degrade crude oil [12]. The Pedobacter steynii strain DX4 was isolated from frozen soil of Tibetan Plateau permafrost region. This organism was selected for genome sequencing for it exhibited the capability to utilize and degrade crude oil at a cold temperature (15 °C). In this paper, our aim was to identify genomic signatures for petroleum degradation in this strain, and investigate its application in bioremediation in cold environments.

Organism information

Classification and features

The soil sample was collected from the Dangxiong County (30.5633°N, 91.4221°E, 4488 m ASL) in the Tibetan Plateau, in 2013. The soil sample was preserved at −20 °C immediately after collection and sent to the State Key Laboratory of Cryospheric Sciences, CAS. The soil type belongs to alpine meadow soil. Crude-oil degrading strains were enriched in liquid MM medium added 2% crude oil (v/v) and incubated for 2 weeks at 20 °C [13]. The suspension of culture collection was surface spread onto the 216 L agar plates and cultivated for 5 days at 20 °C [14]. DX4 colonies on 216 L agar plates are light yellow, slightly domed mucoid and circular with smooth margins. DX4 cells are Gram negative rods, motile, non-spore-forming. The scanning electron micrograph is shown in Fig. 1. Additional characteristics of P. steynii DX4 are shown in Table 1. Growth experiment was carried out in 216 L liquid medium at 20 °C and the OD600 of strain DX4 is shown in Fig. 2. In addition, Fig. 3 shows the crude oil degradation rates of the strain DX4. The degradation was carried out in liquid MM medium added 2% crude oil (v/v) at 15 °C for 2 weeks and crude oil was quantified by using gas chromatography and mass spectrometric detector [15].
Fig. 1

Scanning electron micrograph of P. steynii DX4

Table 1

Classification and general features of Pedobacter steynii DX4

MIGS ID

Property

Term

Evidence code

 

Classification

Domain Bacteria

TAS [41]

  

Phylum Bacteroidetes

TAS [42, 43]

  

Class Sphingobacteriia

TAS [4446]

  

Order Sphingobacteriales

TAS [44]

  

Family Sphingobacteriaceae

TAS [47, 48]

  

Genus Pedobacter

TAS [49]

  

Species Pedobacter steynii

TAS [49]

  

Strain DX4

 
 

Gram stain

Negative

TAS [49]

 

Cell shape

Rod

IDA

 

Motility

Motile

TAS [49]

 

Sporulation

Non-sporulating

TAS [49]

 

Temperature range

4-25 °C

IDA

 

Optimum temperature

20 °C

TAS [50]

 

pH range; Optimum

5-10; 7.5;

IDA

 

Carbon source

Yeast extract, pyruvate, crude oil

IDA

MIGS-6

Habitat

Frozen soil

IDA

MIGS-6.3

Salinity

0.5-4.5% NaCl (w/v)

TAS [51]

MIGS-22

Oxygen requirement

Aerobic

NAS

MIGS-15

Biotic relationship

Free-living

IDA

MIGS-14

Pathogenicity

Non-pathogen

NAS

MIGS-4

Geographic location

China: Tibetan Plateau, Dangxiong County

IDA

MIGS-5

Sample collection

2013

IDA

MIGS-4.1

Latitude

30.5633°N

NAS

MIGS-4.2

Longitude

91.4221°E

NAS

MIGS-4.4

Altitude

4488 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

Fig. 2

Growth curve of P. steynii DX4 in 216 L liquid medium at 20 °C. The absortance at 600 nm was measured every 4 h

Fig. 3

Degrading rates of crude oil by P. steynii DX4. H1 - H16: serial n-alkanes, from Undecane to Hexacosane. H17- H32: branched alkanes and cycloalkanes, in accordance with the order: Undecane,2,6-dimethyl; Dodecane,2-methyl; Dodecane,2,6,11-trimethyl; Pentadecane, 7-methyl; Octane, 2,3,7-trimethyl; Dodecane, 3-methyl; Dodecane, 2,6,10-trimethyl; 1H-Indene, octahydro-2,2,4,4,7,7-hexamethyl-, trans; Undecane, 5-cyclohexyl; H26:Undecane, 4,8-dimethyl; Decahydro-4,4,8,9,10-pentamethylnaphthalene; Pentadecane, 2-methyl; Pentadecane, 2,6,10-trimethyl; Pentadecane, 8-hexyl; Hexadecane; 2,6,10,14-tetramethyl; Ethyl iso-allocholate

The molecular identification was performed with the 27F-1492R primer to amplify the 16S rRNA sequence. The 16S rRNA from DX4 was 99.64% similar to the Pedobacter steynii WB2.3-45T (AM491372) thus DX4 was identified as a strain of P. steynii .

Figure 4 shows the phylogenetic tree constructed from the 16S rRNA sequence together with other related Pedobacter species using MEGA 5.0 software suite. The evolutionary history was inferred by using Neighbor-joining method based on the maximum composite likehood substitution model [16, 17].
Fig. 4

Rooted phylogenetic tree of the 16 S rRNA sequences of Pedobacter steynii strain DX4 and relative species. The 16 S rRNA sequences of Pedobacter species were aligned, and the phylogenetic tree was constructed by using Neighbor-joining method based on the maximum composite likehood substitution model

Genome sequencing information

Genome project history

The strain DX4 was selected for sequencing on the basis of its potential biodegradation capability. The initial Illumina sequencing was performed in April 2016 and the genome was closed by PacBio sequencing in August 2016. The genome project is deposited in the online genome database (NCBI-Genome) and the sequence was released for public access on September 9, 2016. A summary of the project information is shown in the Table 2.
Table 2

Project information of the whole genome sequence of P. steynii DX4

MIGS ID

Property

Term

MIGS-31

Finishing quality

Finished

MIGS-28

Libraries used

Paired-end (average 500 bp)

PacBio (2075 and 2775 kbp)

MIGS-29

Sequencing platforms

Illumina Hiseq 2000 and PacBio

MIGS-31.2

Fold coverage

Illumina paired-end:86×

PacBio: 153×

MIGS-30

Assemblers

SOAPdenovo 2.3,

GapCloser v1.12

HGAP

MIGS-32

Gene calling method

Glimmer3.02

 

Locus Tag

BFS30

 

GenBank ID

CP017141

 

GenBank Date of Release

September 9, 2016

 

GOLD ID

Gp0156107

 

BIOPROJECT

PRJNA339039

MIGS-13

Source Material Identifier

DX4

 

Project relevance

Biodegrading

Growth conditions and genomic DNA preparation

Pedobacter steynii DX4 was inoculated into 216 L liquid medium and grown on a shaker (200 rpm) at 20 °C, until the cells OD600nm > 1.0. Genomic DNA was extracted from freshly grown cells using the E.Z.N.A.® Bacterial DNA Kit following the standard protocol prescribed by the manufacturer.

Genome sequencing and assembly

The complete genome sequence of DX4 was sequenced using Illumina HiSeq2000 for the initial sequencing and assembly, followed by PacBio sequencing to fully close the genome sequence [18, 19]. The Illumina platform generated 1,864,026 reads totaling 561,071,826 bp, and the data were assembled into 9 scaffolds by using SOAP denovo V2.3 [20]. The coverage of the paired-end reads was 86×. For gap closure, sequencing was performed using a PacBio SMRT cell, which resulted in 198,008 reads with an average read length of 4973 bp and a coverage of 153×. The alignment of the PacBio reads were assembled with HGAP [21]. Gap closure was managed using the Gap Closer 1.12 and resulting in the final genome of one complete chromosome. This finished genome was deposited in IMG Database with the Project ID: Gp0156107. And this whole-genome project (BioProject ID: PRJNA339039) has also been registered and assembled sequence data submitted at NCBI GenBank under the accession no.CP017141. The Average Nucleotide Identity (ANI) analysis has been carried out by using a online tool [22].

Genome annotation

Glimmer 3.0 was used to predict open reading frames (ORFs) [23]. The rRNA and tRNA gene predictions and the ORFs annotation were conducted by using BLASTp against NCBI-NR database [24], the COG database [25] and the KEGG database [26]. Genes function annotations were assigned when blastp E-values were ≤0.001 [27]. If there was no significant similarity to protein in other organisms, the gene production was described as hypothetical protein.

Genome properties

The genome statistics is shown in Table 3. The genome of Pedobacter steynii DX4 is 6,581,659 base pairs in size, and has a GC content of 41.31%. Out of the total 5464 genes, 23 genes are pseudogenes and 63 are tRNAs, 13 are rRNA genes, 3 are ncRNA genes, 5362 are coding sequences CDSs. Of the total CDSs, 307 are functioning unknown (5.7%), 414 are general function prediction only (7.7%) and the remaining had a defined function. The COG-distribution of genes is shown in Table 4. The genome map (Fig. 5) was visualized by CG view server. The ANI analysis showed Pedobacter steynii DX4 had 83.33% nucleotide identity with Pedobacter steynii DSM 19110. Comparative analysis between Pedobacter strains isolated from polar region was also performed. The P. steynii DX4 presented 79.03% nucleotide identity with P. cryoconitis PAMC 27485 (isolated from Antarctica), 78.42% with P. antarcticus 4BY and 76.39% with P. arcticus A12, revealing the great genetic distance between these strains.
Table 3

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

6,581,659

100

DNA coding (bp)

6,033,402

91.67

DNA G + C (bp)

2,718,883

41.31

DNA scaffolds

1

 

Total genes

5464

100

Protein coding genes

5362

98.13

RNA genes

79

1.44

Pseudo genes

23

0.42

Genes in internal clusters

NA

 

Genes with function prediction

414

7.58

Genes assigned to COGs

3720

68.01

Genes with Pfam domains

4264

78.04

Genes with signal peptides

804

14.71

Genes with transmembrane helices

178

3.26

CRISPR repeats

1

 
Table 4

Number of genes of Pedobacter steynii DX4 with the general COG functional categories

Code

Value

% of totala

Description

J

155

2.9

Translation, ribosomal structure and biogenesis

A

0

0

RNA processing and modification

K

417

7.8

Transcription

L

146

2.7

Replication, recombination and repair

B

1

0

Chromatin structure and dynamics

D

20

0.4

Cell cycle control, Cell division, chromosome partitioning

V

94

1.8

Defense mechanisms

T

261

4.9

Signal transduction mechanisms

M

306

5.7

Cell wall/membrane biogenesis

N

17

0.3

Cell motility

U

29

0.5

Intracellular trafficking and secretion

O

158

2.9

Posttranslational modification, protein turnover, chaperones

C

150

2.8

Energy production and conversion

G

255

4.8

Carbohydrate transport and metabolism

E

257

4.8

Amino acid transport and metabolism

F

74

1.4

Nucleotide transport and metabolism

H

125

2.3

Coenzyme transport and metabolism

I

154

2.9

Lipid transport and metabolism

P

290

5.4

Inorganic ion transport and metabolism

Q

90

1.7

Secondary metabolites biosynthesis, transport and catabolism

R

414

7.7

General function prediction only

S

307

5.7

Function unknown

-

1642

30.6

Not in COGs

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

Fig. 5

The genome map of Pedobacter steynii strain DX4.Circle 1: Base pair numbers; Circle 2 and Circle 3:Forward and reverse coding domain sequences, the color coding of the CDS represent different Clusters of Orthologous Groups categories; Circle 4: rRNA and tRNA; Circle 5: % GC plot; Circle 6:GC skew [(GC)/(G + C)]

Insights from the genome sequence

Genome annotation predicted many traits support the adaptability of DX4 to cold and crude oil-contaminated environment. The Five cold shock proteins were predicted (NCBI Protein database: WP_069377418.1, WP_062548063.1, WP_048905418.1, WP_008241764.1 and AOM75720.1). These proteins are supposed to play important roles in low temperature conditions [28]. The related strians isolated from antarctic regions, Pedobacter antarcticus 4BY and Pedobacter cryoconitis PAMC 27485, respectively encoded four cold shock proteins. Based on the COG analysis, 261 genes in total were assigned to the signal transduction category. Among them, 22 genes were predicted to encode the response regulators and 6 were found to encode chemotaxis protein CheY [29]. These genes could play regulatory role in environment sensing and cell motility towards the crude oil.

As for aerobic alkane degradation, alkB gene has been considered as a functional biomarker for alkane-degrading bacterial populations in environmental [3032]. But in P. steynii DX4 genome, no alkB homolog coding genes were found. A gene coding for haloalkane dehalogenase (WP_069382597.1, EC 3.8.1.5) was annotated. Haloalkane dehalogenase (HLD) has considerable environmental significance because it converts haloalkanes to corresponding alcohol and hydrogen halide (KEGG database: RN: R02337,) [33, 34]. In addition to that, three luciferase proteins were identified (WP_069377707.1, WP_069380456.1 and WP_069377640.1). Research showed that the bacteria luciferase can utilize reduced FMN in the oxidation of alkanes with the emission of blue-green light [35, 36]. Figure 6 shows the genes coding for HLD and luciferase protein and adjacent genes upstream and downstream, which may be relevant genes participating in the metabolism of crude oil. In addition, the presence of 19 alcohol dehydrogenase and 23 aldehyde dehydrogenase necessary for alkane degradation as well as 11 fatty acid transport and metabolism genes suggest a complete alkane degradation pathway [37, 38].
Fig. 6

Organization of Genes coding for HLD and luciferase and their adjacent genes in P. steynii strain DX4 genome

The antibiotics and secondary metabolite analysis was done using the anti-SMASH platform [39]. In total, 12 secondary metabolite clusters were identified and 11 of them were related to antibiotics. A resorcinol metabolite cluster was identified and this cluster may play important role in the degradation of resorcinol and other aromatic compounds [40]. Interestingly, the 12 secondary metabolite clusters had no similarity with the known clusters, suggesting that the P. steynii strain DX4 may possess novel secondary metabolic pathways.

Conclusions

Pedobacter steynii DX4 was isolated from a cold environment and could utilize crude oil as sole carbon source. The genome of DX4 reported here provides the genetic basis of its crude oil biodegrading mechanism. Genes involved in cold shock, energy conversion and response regulators for cell motility point to the unique abilities of DX4 in oil degradation and cold environment adaptation. Genomic research on DX4 would also provide a blueprint for the application of bioremediation and recovery in cold oil-polluted environments.

Abbreviation

ANI: 

Average nucleotide identity

HLD: 

Haloalkane dehalogenase

Declarations

Funding

This study is supported by grants from the International Scientific and Technological Cooperation Projects of the Ministry of Science and Technology (2014DFA30330), the National Science Foundation of China (41271265).

Authors’ contributions

SJC and GSZ initiated the study. GSZ, TC and GXL designed the research and project outline. SJC, GSZ and XMC drafted the manuscript. HZL and YLW isolated the strain. SJC and XMC assembled and annotated the genome. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis 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)
University of Chinese Academy of Sciences
(2)
State Key Laboratory of Cryospheric Sciences, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences
(3)
Key Laboratory of Extreme Environmental Microbial Resources and Engineering
(4)
Key Laboratory of Desert and Desertification, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences
(5)
College of Bioscience and Bioengineering, Jiangxi Agricultural University

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