Open Access

Draft genome sequence of Paenibacillus sp. strain A2

  • Beiwen Zheng1,
  • Fan Zhang2,
  • Hao Dong3,
  • Lujun Chai2,
  • Fuchang Shu3,
  • Shaojin Yi3,
  • Zhengliang Wang3,
  • Qingfeng Cui4,
  • Hanping Dong4,
  • Zhongzhi Zhang5,
  • Dujie Hou2,
  • Jinshui Yang6Email author and
  • Yuehui She3Email author
Contributed equally
Standards in Genomic Sciences201611:9

DOI: 10.1186/s40793-015-0125-7

Received: 21 July 2014

Accepted: 22 December 2015

Published: 26 January 2016

Abstract

Paenibacillus sp. strain A2 is a Gram-negative rod-shaped bacterium isolated from a mixture of formation water and petroleum in Daqing oilfield, China. This facultative aerobic bacterium was found to have a broad capacity for metabolizing hydrocarbon and organosulfur compounds, which are the main reasons for the interest in sequencing its genome. Here we describe the features of Paenibacillus sp. strain A2, together with the genome sequence and its annotation. The 7,650,246 bp long genome (1 chromosome but no plasmid) exhibits a G+C content of 54.2 % and contains 7575 protein-coding and 49 RNA genes, including 3 rRNA genes. One putative alkane monooxygenase, one putative alkanesulfonate monooxygenase, one putative alkanesulfonate transporter and four putative sulfate transporters were found in the draft genome.

Keywords

Paenibacillus sp. strain A2 Genome Hiseq2000 Sulfonate biodegradation

Introduction

Paenibacillus is a genus of aerobic, Gram-positive, rod-shaped, and endospore forming bacteria, formerly included within the genus Bacillus , but was proposed as a separate genus in 1993 on the basis of its unique distrinctive phenotypic and genotypic features [1]. Strains in this genus have been detected in a variety of environments including soil, water, rhizosphere, vegetable matter, forage and insect larvae, as well as clinical samples [26]. One hundred and forty nine species and four subspecies have previously been recorded in the genus Paenibacillus . These bacteria produce various metabolites, which can catalyze a wide variety of synthetic reactions in fields ranging from cosmetics to biofuel production and have gained importance in agriculture, industrial and medical applications [7].

Surfactant flooding is an important form of EOR to reduce the interfacial tension between oil and water to an ultra-low value [8]. Until now, sulfonate surfactants have been widely adopted as flooding agents in EOR in some oilfields under different geological conditions [9]. Surfactant flooding technology has been widely applied in the Daqing oilfield (China), and in our previous work three indigenous bacteria were isolated as crude-oil degrading species that enhance oil recovery [10]. While screening hydrocarbon-degrading bacteria previously, we isolated a Paenibacillus sp. strain A2 from a mixture of formation water and petroleum in Daqing oilfield. Strain A2 grows aerobically with tetradecane and hexadecane as the sole carbon and energy source, and was also found to have a capacity to metabolize organosulfur compounds. To date, data on the genetic basis of metabolizing hydrocarbon and sulfur compounds in genus Paenibacillus are only sparsely available. To gain insight into the nature and genomic plasticity of this strain from a unique niche its genome was sequenced and here we report a summary classification and genome annotations for Paenibacillus sp. strain A2.

Organism information

Classification and features

Paenibacillus sp. strain A2 was isolated from a mixture of formation water and petroleum in Daqing oilfield, China, in March 2012. It is a Gram-positive bacterium that can grow on LB broth agar at 37 °C. Cells of strain A2 are rod-shaped, showed a diameter ranging 0.4–0.7 μm and from 1.5 to 3.6 μm long, occurring predominantly singly (Fig. 1). Growth occurs under aerobic condition. The optimum temperature for growth is 37 °C, with a temperature range of 15–45 °C (Table 1). Cell morphology, motility and sporulation were examined by using scanning electron microscopy (Quanta 200, FEI Co., USA).
Fig. 1

Scanning electron micrograph of cells of strain A2. Bar: 5.0 μm

Table 1

Classification and general features of Paenibacillus sp. strain A2

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain: Bacteria

TAS [31]

  

Phylum: Firmicutes

TAS [3234]

  

Class: Bacilli

TAS [35, 36]

  

Order: Bacillales

TAS [37, 38]

  

Family: Paenibacillaceae

TAS [36]

  

Genus: Paenibacillus

TAS [1, 3942]

  

Species: Paenibacillus sp.

IDA

  

Strain: A2

IDA

 

Gram stain

Positive

IDA

 

Cell shape

Rod-shaped

IDA

 

Motility

Motile

IDA

 

Sporulation

Spore-forming

IDA

 

Temperature range

Mesophile

IDA

 

Optimum temperature

37rb

IDA

 

pH range; Optimum

5.0–9.0; 6.0–8.0

IDA

 

Carbon source

Glucose, xylose, mannitol, arabinose

IDA

 

Energy source

Glucose, xylose, mannitol, arabinose

IDA

 

Terminal electron receptor

Not reported

IDA

MIGS-6

Habitat

Environment

IDA

MIGS-6.3

Salinity

Tolerates 5 % NaCl

IDA

MIGS-22

Oxygen

Not reported

IDA

MIGS-15

Biotic relationship

Free living

IDA

MIGS-14

Pathogenicity

Non pathogenic, BSL1

NAS

MIGS-4

Geographic location

Daqing, China

IDA

MIGS-5

Sample collection time

March 2012

IDA

MIGS-4.1

Latitude

45°92′N

IDA

MIGS-4.2

Longitude

124°68′E

IDA

MIGS-4.4

Altitude

Not reported

IDA

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 [43]

Comparative 16S rRNA gene sequence analysis by BLASTN using the NCBI-NR/NT database revealed 94–99 % sequence similarity to members of genus Paenibacillus . Neighbor-Joining phylogenetic analysis based on Kimura 2-parameter model indicated the Paenibacillus sp. strain A2 is most closely related the strain Paenibacillus ehimensis KCTC 3748T (AY116665) and Paenibacillus koreensis YC300T (AF130254) (Fig. 2).
Fig. 2

Phylogenetic tree depicting the relationship between Paenibacillus sp. strain A2 and other members of the genus Paenibacillus. The strains and their corresponding Genbank accession numbers are shown following the organism name and indicated in parentheses. The phylogenetic tree uses 16S rRNA gene sequences aligned by the CLUSTALW [7], and phylogenetic inferences were made using Neighbor-joining method based on Kimura 2-parameter model within the MEGA5 software [8] and rooted with Bacillus subtilis strain DSM10T (AJ276351). Bootstrap consensus trees were inferred from 100 replicates, only bootstrap values >50 % were indicated. The scale bar represents 0.01 nucleotide change per nucleotide position

Biochemical features were tested by using two automated systems, the Vitek2 Compact (bioMérieux, Marcy l’Etoile, France) and Phoenix 100 ID/AST system (Becton Dickinson Company, Sparks, MD. USA). Positive reactions were obtained for glucose, xylose, mannitol and arabinose. Negative reactions were observed for fructose, trehalose, gluconic acid, sucrose, maltose, urea, cellobiose, glucoside, tagatose and maltotriose. This strain was susceptible to gentamicin, ciprofloxacin, levofloxacin, moxifloxacin, tri-methoprim/sulfamethoxazole, amoxicillin, imipenem, meropenem, ciprofloxacin, tigecycline and rifampicin, but resistant to metronidazole.

Genome sequencing information

Genome project history

Paenibacillus sp. strain A2 was selected for sequencing on the basis of its phylogenetic position and 16S rRNA similarity to other members of the genus Paenibacillus , and is part of a microbial diversity study of the oilfield aiming at isolating all bacterial species degrading crude-oil. This whole genome shotgun project of Paenibacillus sp. strain A2 is deposited in the Genome On Line Database and the draft genome sequence is deposited at DDBJ/EMBL/GenBank under the accession JFHX00000000 and consists of 180 contigs. A summary of the project information and its association with MIGS version 2.0 compliance are shown in Table 2 [11].
Table 2

Project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

High-quality draft

MIGS-28

Libraries used

One pair-end 450 bp library

MIGS-29

Sequencing platforms

Illumina HiSeq 2000

MIGS-31.2

Fold coverage

180.0 × (based on 450 bp library)

MIGS-30

Assemblers

Velvet 1.2.07

MIGS-32

Gene calling method

Glimmer 3.0

 

Locus Tag

AA76

 

Genbank ID

JFHX00000000

 

Genbank Date of Release

April 2, 2014

 

GOLD ID

Gi0070607

 

BIOPROJECT

PRJNA233560

MIGS-13

Source Material Identifier

CGMCC No. 5647

 

Project relevance

Biotechnology

Growth conditions and genomic DNA preparation

Paenibacillus sp. strain A2 was grown aerobically on LB broth, at 37 °C for 16 h. Genomic DNA was extracted using the DNeasy blood and tissue kit (Qiagen, Germany), according to the manufacturer’s recommended protocol. The quantity of DNA was measured by the NanoDrop Spectrophotometer and Cubit. Then 10 μg of DNA was sent to BGI (Shenzhen, China) for sequencing on a Hiseq2000 system.

Genome sequencing and assembly

One DNA library was generated (450 bp insert size, with the Illumina adapter at both ends detected by Agilent DNA analyzer 2100), then sequenced using an Illumina Hieseq 2000 genomic sequencer, with a 2 × 100 pair end sequencing strategy. Finally, we obtained a total of 5,728,134 M bp and performed the following quality control steps: 1) Reads linked to adapters at both end were considered as sequencing artifacts and removed. 2) Bases with quality index lower than Q20 at both ends were trimmed. 3) Reads with ambiguous bases (N) were removed. 4) Single qualified reads were discarded (In this situation, one read is qualified but its mate is not). Filtered 1378 M clean data were assembled into scaffolds using the Velvet version 1.2.07 with parameters “-scaffolds no” [12], then we use a PAGIT flow [13] to prolong the initial contigs and correct sequencing errors to arrive at a set of improved scaffolds.

Genome annotation

Predicted genes were identified using Glimmer version 3.0 [14]. tRNAscan-SE version 1.21 [15] was used to find tRNA genes, whereas ribosomal RNAs were found by using RNAmmer version 1.2 [16]. To annotate predicted genes, we used HMMER version 3.0 [17] to align genes against Pfam version 27.0 [18] (only pfam-A was used) to find genes with conserved domains. KAAS server [19] was used to assign translated amino acids into KEGG Orthology [20] with single-directional best hit method. Translated genes were aligned with the COG database [21, 22] using NCBI blastp (hits should have scores no less than 60, e value is no more than 1e-6). To find genes with hypothetical or putative functions, we aligned genes against the NCBI nucleotide sequence database (nt database was downloaded at Sep 20, 2013) by using NCBI blastn, only if hits have identity no less than 0.95, coverage no less than 0.9, and reference genes were annotated as putative or hypothetical. To define genes with a signal peptide, we use SignalP version 4.1 [23] to identify genes using default parameters. TMHMM 2.0 [24] was used to identify genes with transmembrane helices. Prophages and putative phage like elements in the genome were identified using prophage-predicting PHAST [25]. Blast of the three genomes together with strain 2745-2 were performed using blast+program [26]. BLAST Ring Image Generator (BRIG) was used for genome alignment visualization [27].

Genome properties

The draft genome sequence of Paenibacillus sp. strain A2 revealed a genome size of 7,650,246 bp and a G+C content of 54.2 % (Table 3). The genome contain 7575 coding sequences, 46 tRNAs (excluding 1 pseudo tRNAs) and incomplete rRNA operons (one small subunit rRNA and two large subunit rRNAs). A total of 3112 protein-coding genes were assigned as putative function or hypothetical proteins. Four thousand seven hundred ten genes were categorized into COGs functional groups (including putative or hypothetical genes). The properties and the statistics of the genome are summarized in Tables 3 and 4. Nine prophage regions have been identified in the genome of strain A2 (Fig. 3), including one intact, six incomplete and two questionable regions (Table 5).
Table 3

Genome statistics

Attribute

Value

% of Totala

Genome size (bp)

7,650,246

100.00

DNA coding region (bp)

6,699,198

87.57

DNA G+C (bp)

4,144,410

54.2

DNA scafflods

180

 

Total genes

7578

100.00

Protein coding genes

7575

99.96

RNA genes

49

0.65

Pseudo genes

211

2.78

Genes in internal clusters

203

2.68

Genes with function prediction

5756

76

Genes with Pfam domains

6300

83.16

Genes assigned to COGs

4710

62.15

Genes with signal peptides

405

5.34

Genes with transmembrane helices

1962

25.89

CRISPR repeats

1

aThe total is based on either the size of the genome in base pairs or the total number of protein coding genes in the annotated genome

Table 4

Number of genes associated with general COG functional categories

Code

Value

% age

Description

J

209

2.76

Translation, ribosomal structure and biogenesis

A

0

0

RNA processing and modification

K

746

9.85

Transcription

L

195

2.57

Replication, recombination and repair

B

4

0.053

Chromatin structure and dynamics

D

85

1.12

Cell cycle control, mitosis and meiosis

V

258

3.41

Defense mechanisms

T

474

6.26

Signal transduction mechanisms

M

282

3.72

Cell wall/membrane biogenesis

N

128

1.69

Cell motility

Z

2

0.026

Cytoskeleton

U

57

0.75

Intracellular trafficking and secretion

O

191

2.52

Posttranslational modification, protein turnover, chaperones

C

351

4.63

Energy production and conversion

G

787

10.39

Carbohydrate transport and metabolism

E

796

10.51

Amino acid transport and metabolism

F

179

2.36

Nucleotide transport and metabolism

H

265

3.50

Coenzyme transport and metabolism

I

196

2.59

Lipid transport and metabolism

P

549

7.25

Inorganic ion transport and metabolism

Q

261

3.45

Secondary metabolites biosynthesis, transport and catabolism

R

1046

13.81

General function prediction only

S

407

5.37

Function unknown

-

468

6.18

Not in COGs

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

Fig. 3

Genomic view of prophage regions identified in the genome of Paenibacillus sp. A2

Table 5

Summary of prophage regions in Paenibacillus sp. A2

Region

Region length

Completeness

CDS

Specific keyword

1

13.2 kb

incomplete

17

tail

2

43.5 kb

intact

55

tail, plate, capsid, protease, portal, terminase, integrase, transposase

3

16.9 kb

incomplete

16

tail

4

23.6 kb

questionable

23

tail, capsid, head, portal, terminase

5

20.2 kb

incomplete

21

terminase, portal, head, capsid, tail

6

19.3 kb

incomplete

21

tail

7

37.7 kb

incomplete

24

integrase, tail

8

30.5 kb

incomplete

25

integrase

9

15.9 kb

questionable

22

tail,lysin, plate

Insights from the genome sequence

Paenibacillus sp. strain A2 grows aerobically with tetradecane and hexadecane as the sole carbon and energy source, and has capability of degrading alkanesulfonate suggesting that it has developed a number of evolutionary strategies that allow for habitat adaptation. To identify pathways associated with niche adaptation to a petroleum reservoir, we explored the genome content for genes associated with hydrocarbon and sulfur metabolism (Table 6). Alkane monooxygenases have been proposed as one of the two unrelated classes of enzymes responsible for the aerobic transformation of midchain-length n-alkanes (C5 to C16) and in some cases even longer alkanes [28]. Sulfate transporters and alkanesulfonate transporter have been shown to play an essential role in metabolizing organosulfur compounds [29, 30]. Based on this knowledge, the genome sequence of strain A2 provides the basis to elucidate its genetic basis for crude oil degradation and adaptation to the petroleum reservoir. BLAST search of nucleotide sequence between strain A2 and other seven Paenibacillus species showed that A2 has highest similarity with Paenibacillus elgii B69, which is consistent with the 16 s rRNA sequence alignment (Fig. 4).
Table 6

Summary of proteins involved in hydrocarbon and sulfur metabolisms

Protein

Start

Stop

Protein product

Length

Description

1

3628875

3629657

WP_025849555.1

260

alkanesulfonate transporter permease subunit

2

3629626

3630852

WP_025849556.1

408

alkanesulfonate monooxygenase

3

6287814

6288827

WP_025846226.1

337

alkane 1-monooxygenase

4

1957755

1958930

WP_025851077.1

391

sulfate adenylyltransferase

5

2493097

2493636

WP_025850577.1

179

adenylylsulfate kinase

6

3634266

3635159

WP_025849561.1

297

sulfate/thiosulfate transporter permease subunit

7

3635181

3636017

WP_025849562.1

278

sulfate transporter

8

3636039

3637142

WP_025849563.1

367

sulfate transporter subunit

9

4328289

4330016

WP_025848942.1

575

sulfate transporter

10

5127629

5128231

WP_025847883.1

200

adenylylsulfate kinase

Fig. 4

Circular representation of seven draft Paenibacillus genomes compared against Paenibaciluus sp. A2. The inner rings show GC content (black) and GC skew (purple/green). The remaining rings show BLASTn results of each genome against P. ehimensis A2 (JFHX01000001.1) using the BRIG program. The strains used in the BLASTn were P. elgii B69 (AFHW01000001.1), P. chitinolyticus NBRC15660 (BBJT01000001.1), P. polymyxa ATCC842 (AFOX01000001.1), P. vortex V453 (ADHJ01000001.1), P. curdlanolyticus YK9 (AEDD01000001.1), P. larvae subsp. larvae BRL-230010 (AARF01000001.1) and P. mucilaginosus KNP414 (CP002869.1)

Conclusions

Paenibacillus sp. strain A2, was isolated from a mixture of formation water and petroleum and has a broad capacity for metabolizing hydrocarbon and organosulfur compounds. To date, no metabolc pathways involved in petroleum degradation or sulfur compounds have been characterized in genus Paenibacillus . The genome sequence of the A2 will hopefully provide new insights into the mechanism of degradation and microorganisms adapt to the petroleum reservoir after surfactant flooding. Furthermore, our data takes a step toward a comprehensive genomic catalog of the metabolic diversity of genus Paenibacillus .

Notes

Abbreviations

EOR: 

enhanced oil recovery

PAGIT: 

post assembly genome improvement toolkit

TMHMM: 

transmembrane prediction using hidden markov models

Declarations

Acknowledgements

This study was sponsored by the National Natural Science Foundation of China (Grant No. 81301461, 51574038 and 51474034), 863 Program (Grant No. 2013AA064402) of the Ministry of Science and Technology, Zhejiang Provincial Natural Science Foundation of China (Grant No. LQ13H190002).

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)
State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University
(2)
Key Laboratory of Marine Reservoir Evolution and Hydrocarbon Accumulation Mechanism, School of Energy Resources, China University of Geosciences
(3)
College of Chemistry and Environmental Engineering, Yangtze University
(4)
Institute of Porous Flow & Fluid Mechanics, Chinese Academy of Sciences
(5)
State Key Laboratory of Heavy Oil Processing, China University of Petroleum
(6)
College of Life Sciences, China Agricultural University

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