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High-quality-draft genomic sequence of Paenibacillus ferrarius CY1T with the potential to bioremediate Cd, Cr and Se contamination

Standards in Genomic Sciences201712:60

https://doi.org/10.1186/s40793-017-0273-z

Received: 5 April 2017

Accepted: 21 September 2017

Published: 10 October 2017

Abstract

Paenibacillus ferrarius CY1T (= KCTC 33419T = CCTCC AB2013369T) is a Gram-positive, aerobic, endospore-forming, motile and rod-shaped bacterium isolated from iron mineral soil. This bacterium reduces sulfate (SO4 2−) to S2−, which reacts with Cd(II) to generate precipitated CdS. It also reduces the toxic chromate [Cr(VI)] and selenite [Se(VI)] to the less bioavailable chromite [Cr(III)] and selenium (Se0), respectively. Thus, strain CY1T has the potential to bioremediate Cd, Cr and Se contamination, which is the main reason for the interest in sequencing its genome. Here we describe the features of strain CY1T, together with the draft genome sequence and its annotation. The 9,184,169 bp long genome exhibits a G + C content of 45.6%, 7909 protein-coding genes and 81 RNA genes. Nine putative Se(IV)-reducing genes, five putative Cr(VI) reductase and nine putative sulfate-reducing genes were identified in the genome.

Keywords

Paenibacillus ferrarius Genome sequenceCadmiumChromate-reducing bacteriumSelenite-reducing bacterium

Introduction

The genus Paenibacillus was established in 1993 with Paenibacillus polymyxa as the type species [1, 2]. The common characteristics of the Paenibacillus members are aerobic, Gram-positive, rod-shaped and endospore-forming [3]. Some Paenibacillus strains have the ability for plant growth promotion, biocontrol, manufacturing process and bioremediation, which making them very important in agricultural, industrial and medical applications [4]. A variety of industrial wastes including crude oil, diesel fuel, textile dyes, aliphatic and aromatic organic pollutants could be degraded by Paenibacillus strains [511]. However, the bioremediation of heavy metal(loids) contamination by Paenibacillus strains are rarely reported.

Paenibacillus ferrarius CY1T is a multi-metal(loids) resistant bacterium isolated from iron mineral soil in Hunan Province, China [12]. During cultivation, it could efficiently reduce sulfate (SO4 2−) to S2−, which could precipitate with cadmium [Cd(II)] to generate CdS [13]. In addition, it also reduces the more toxic chromate [Cr(VI)] and selenite [Se(VI)] to the much less toxic chromite [Cr(III)] and selenium (Se0), respectively. Based on these interesting features, we propose that strain CY1T represents a promising candidate for bioremediation of Cd, Cr and Se contamination. To gain insight into the molecular mechanisms involved in sulfate/chromate/selenite reduction and metal(loids) resistance, and to enhance its biotechnological applications, we analyze the high quality draft genome of this bacterium.

Organism information

Classification and features

P. ferrarius CY1T is a Gram-positive, endospore-forming, motile and aerobic bacterium. The rod-shaped cells are 0.5–0.8 mm in width and 4.2–5.7 mm in length with peritrichous flagella (Fig. 1). Colonies are yellowish to creamy-white, smooth and circular on NA agar plate [12]. Growth occurs at temperature and pH range of 4–37 °C and pH 5.0–8.0, respectively [12]. Optimal growth occurs at 28 °C and pH 6.0–7.0 (Table 1). Strain CY1T grows on NA/R2A/LB and TSA media, but cannot grow on MacConkey agar [12]. The phylogenetic relationship of P. ferrarius CY1T with other members within the genus Paenibacillus is shown in a 16S rRNA based neighbor-joining tree, and strain CY1T is closely related to Paenibacillus marchantiophytorum R55 T (KP056549) (Fig. 2).
Fig. 1

Scan electron microscope (SEM) image of P. ferrarius CY1T cells. The bar scale represents 0.5 μm

Table 1

Classification and general features of Paenibacillus ferrarius CY1T

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [39]

  

Phylum Firmicutes

TAS [4042]

  

Class Bacilli

TAS [43, 44]

  

Order Bacillales

TAS [45, 46]

  

Family Paenibacillaceae

TAS [44]

  

Genus Paenibacillus

Species Paenibacillus ferrarius

TAS [1, 4750]

IDA

  

Strain CY1T

IDA

 

Gram stain

Positive

IDA

 

Cell shape

Rod

IDA

 

Motility

Motile

IDA

 

Sporulation

Endospore

IDA

 

Temperature range

4–37 °C

IDA

 

Optimum temperature

28 °C

IDA

 

pH range; Optimum

5–8; 6–7

IDA

 

Carbon source

Rhamnose, glycogen, sucrose N-acetylglucosamine, maltose, mannitol, D-glucose, salicin, melibiose, D-sorbitol, L-arabinose, mannose, D-xylose, ammonium nitrate and L-proline

IDA

MIGS-6

Habitat

Soil

IDA

MIGS-6.3

Salinity

0–1.5% NaCl (w/v)

IDA

MIGS-22

Oxygen requirement

Aerobic

IDA

MIGS-15

Biotic relationship

Free-living

IDA

MIGS-14

Pathogenicity

Non-pathogen

NAS

MIGS-4

Geographic location

Zhangjiajie city, Hunan province, China

IDA

MIGS-5

Sample collection

2013

IDA

MIGS-4.1

Latitude

N29°35’

IDA

MIGS-4.2

Longitude

E110°54’

IDA

MIGS-4.4

Altitude

860 m

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 from the Gene Ontology project [51]

Fig. 2

Phylogenetic tree depicting the relationship between P. ferrarius CY1T and other members of the genus Paenibacillus. The phylogenetic tree was constructed based on the 16S rRNA gene sequences using neighbor-joining method (MEGA 6.0). The scale bar represents 0.01 nucleotide change per nucleotide position

Physiological and biochemical analyses were performed using the API 20NE test (bioMérieux, France), ID 32GN text (bioMérieux, France) and traditional classification methods. Strain CY1T is positive for oxidase and catalase activities, hydrolysis of Tween 80 and aesculin and production of NH3 and H2S, but is negative for nitrate reduction, citrate utilization, egg yolk reaction, production of indole, and hydrolysis of starch, gelatin, casein, urea, L-tyrosine, arginine, Tween 20, DNA and CM-cellulose [12]. The carbon sources, which can be used by strain CY1T, are shown in Table 1.

The resistance levels of P. ferrarius CY1T for multi-metal(loids) were tested with the minimal inhibition concentration on NA agar plates using Na3AsO3, K2Sb2(C4H2O6)2, Na2SeO3, K2CrO4, CdCl2, PbCl2, CuCl2 and MnCl2. The results showed that the MICs for As(III), Sb(III), Se(IV), Cr(VI), Cd(II), Pb(II), Cu(II) and Mn(II) are 2, 1, 8, 4, 0.08, 1, 0.5 and 100 mmol/L, respectively. In addition, the abilities of strain CY1T for Cd(II) removal, and Cr(VI) and Se(IV) reduction were tested. Strain CY1T was incubated in LB medium for Cd(II) removal and in NA medium for Cr(VI) and Se(IV) reduction, since NA medium can absorb some of the Cd(II). When OD600 reach 0.6-0.7, CdCl2 (50 μmol/L), K2CrO4 (200 μmol/L) and Na2SeO3 (200 μmol/L) were each added to the culture. At designated times, culture samples were taken for measuring the residual concentrations of Cd(II), Cr(VI) and Se(IV). The concentration of Cd(II) was measured by the atomic absorption spectrometry [14]. The concentration of Cr(VI) was measured by the UV spectrophotometer (DU800, Beckman, CA, USA) with the colorimetric diphenylcarbazide method [15], and the concentration of Se(IV) was tested by HPLC-HG-AFS (Beijing Titan Instruments Co., Ltd., China) [16]. The results showed that strain CY1T could remove nearly 50 μmol/L Cd(II) in 72 h (Fig. 3a) and reduce 200 μmol/L Cr(VI) and Se(IV) in 5 h and 6 h, respectively (Fig. 3b, c). The removed Cd(II) is presented as pellets that is most probably by the reaction of Cd(II) with H2S to produce precipitated CdS.
Fig. 3

Cd(II) removal (a), and Cr(VI) (b) and Se(IV) (c) reduction by P. ferrarius CY1T. Strain CY1T was incubated in LB [for Cd(II) removal] or NA medium [for Cr(VI) and Se(IV) reduction] until OD600 reach 0.6-0.7, and then amended with CdCl2 (50 μmol/L),K2CrO4 (200 μmol/L) and Na2SeO3 (200 μmol/L), respectively. At designed times, culture samples were taken for measuring the residual concentration of Cd(II), Cr(VI) and Se(IV). Data are shown as the mean of three replicates, with the error bars represents ± SD

Genome sequencing information

Genome project history

Strain CY1T was selected for genome sequencing on the basis of its ability for Cd(II) removal, Cr(VI) and Se(IV) reduction, these characters made strain CY1T with great value for genetic study and for bioremediation of Cd, Cr and Se contamination. The draft genome sequence is deposited at DDBJ/EMBL/GenBank under the accession number MBTG00000000. The final genome consists of 73 scaffolds with 289.77 × coverage. A summary of the project information is shown in Table 2.
Table 2

Project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

High-quality draft

MIGS-28

Libraries used

Illumina Paired-End library (300 bp insert size)

MIGS-29

Sequencing platforms

Illumina Miseq 2000

MIGS-31.2

Fold coverage

289.77 ×

MIGS-30

Assemblers

SOAPdenovo v2.04

MIGS-32

Gene calling method

GeneMarkS+

 

Locus TAG

BC351

 

Genbank ID

MBTG00000000

 

Genbank Date of Release

Mar 16, 2017

 

Bioproject

PRJNA331076

MIGS-13

Source material identifier

Strain KCTC 33419T (CCTCC AB2013369T)

 

Project relevance

Bioremediation

Growth conditions and genomic DNA preparation

Overnight cultures of strain CY1T was inoculated into 50 mL of NA medium at 28 °C with 120 rpm shaking. After incubation for 36 h, the bacterial cells were harvested through centrifugation (13,400×g for 5 min at 4 °C). Genomic DNA was extracted using the QiAamp kit (Qiagen, Germany). The quality and quantity of the DNA were determined by a spectrophotometer (NanoDrop 2000, Thermo). Then, 10 μg of DNA was sent to Bio-broad Technology Co., Ltd., Wuhan, China for sequencing.

Genome sequencing and assembly

Genome sequencing and assembly were performed by Bio-broad Technology Co., Ltd., Wuhan, China, and all original sequence data can be found at the NCBI Sequence Read Archive. An Illumina standard shotgun library was constructed and sequenced using an Illumina Hiseq2000 platform with pair-end sequencing strategy (300 bp insert size) [17]. The following quality control steps were performed for removing low quality reads: 1) removed the adapter sequences of reads; 2) trimmed the ambiguous bases (N) in 5′ end and the reads with a quality score lower than 20; and 3) filtered the reads which contain N more than 10% or have the length less than 50 bp (without adapters and N in 5′ end). The assembly of CY1T genome is based on 20,189,278 quality reads totaling 3,000,798,615 bp, which provides a coverage of 289.77×. Subsequently, the reads were assembled into 75 contigs (> 200 bp) using SOAPdenovo v2.04 [18], and the gaps between the contigs were closed by GapCloser v1.12 [19].

Genome annotation

The draft genome of strain CY1T was annotated through the RAST server version 2.0 and the NCBI Prokaryotic Genome Annotation Pipeline. Genes were identified using the gene caller GeneMarkS+ with the similarity-based gene detection approach [20]. Pseudogenes were also predicted using the NCBI PGAP. Internal gene clustering was performed by OrthoMCL using Match cutoff of 50% and E-value Exponent cutoff of 1-e5 [21, 22]. The COGs functional categories were assigned by WebMGA server [23] with E-value cutoff of 1-e10. The translations of the predicted CDSs were used to search against the Pfam protein family database [24] and the KEGG database [25]. The transmembrane helices and signal peptides were predicted by TMHMM v. 2.0 [26] and SignalP 4.1 [27], respectively.

Genome properties

The whole genome of strain CY1T reveals a genome size of 9,184,169 bp and a G + C content of 45.6% (Table 3). The genome contains 8260 coding sequences, 19 rRNA, 58 tRNA, and 4 ncRNA. Among 7909 protein-coding genes, 4231 were assigned as putative function, while the other 3678 were designated as hypothetical proteins. In addition, 6632 genes were categorized into COGs functional groups. Information about the genome statistics is shown in Table 3 and the classification of genes into COGs functional categories is summarized in Table 4.
Table 3

Genome statistics

Attribute

Value

% of totala

Genome size (bp)

9,184,169

100.00

DNA coding (bp)

7,828,640

85.24

DNA G + C (bp)

4,205,829

45.79

DNA scaffolds

73

100.00

Contigs

75

100.00

Total genesb

8260

 

RNA genes

81

 

Pseudo genes

209

 

Protein-coding genes

7909

100.00

Genes in internal clusters

648

8.19

Genes with function prediction

4231

53.50

Genes assigned to COGs

6632

83.85

Genes with Pfam domains

6363

80.45

Genes with signal peptides

765

9.67

Genes with transmembrane helices

2251

28.46

CRISPR repeats

24

0.30

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

bAlso includes 209 pseudogenes, 58 tRNA genes, 19 rRNAs and 4 ncRNA

Table 4

Number of genes associated with general COG functional categories

Code

Value

% of totala

Description

J

199

2.52

Translation, ribosomal structure and biogenesis

A

0

0.00

RNA processing and modification

K

732

9.26

Transcription

L

213

2.69

Replication, recombination and repair

B

1

0.01

Chromatin structure and dynamics

D

55

0.70

Cell cycle control, cell division, chromosome partitioning

Y

0

0.00

Nuclear structure

V

128

1.62

Defense mechanisms

T

694

8.77

Signal transduction mechanisms

M

328

4.15

Cell wall/membrane/envelope biogenesis

N

107

1.35

Cell motility

Z

11

0.14

Cytoskeleton

U

63

0.80

Intracellular trafficking, secretion, and vesicular transport

O

146

1.85

Posttranslational modification, protein turnover, chaperones

C

268

3.39

Energy production and conversion

G

1023

12.93

Carbohydrate transport and metabolism

E

432

5.46

Amino acid transport and metabolism

F

121

1.53

Nucleotide transport and metabolism

H

194

2.45

Coenzyme transport and metabolism

I

149

1.88

Lipid transport and metabolism

P

361

4.56

Inorganic ion transport and metabolism

Q

134

1.69

Secondary metabolites biosynthesis, transport and catabolism

R

777

9.82

General function prediction only

S

496

6.27

Function unknown

1277

16.15

Not in COGs

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

Insights from the genome sequence

P. ferrarius CY1T is a multi-metal(loids) resistant bacterium with the capability of SO4 2−, Cr(VI) and Se(IV) reduction, suggesting that it has developed a number of evolutionary strategies to adapt to heavy metal (or metalloids) contaminated environments. To identify pathways and enzymes involved in SO4 2−, Cr(VI) and Se(IV) reduction, high quality draft genome sequence of strain CY1T was generated. The map of the P. ferrarius CY1T genome is shown in Fig. 4.
Fig. 4

A graphical circular map of strain P. ferrarius CY1T. From outside to center, rings 1 and 2 denotes the predicted coding sequences on forward/reverse strand with each gene colored by its assigned COG category; ring 3 shows G + C % content plot and ring 4 shows GC skew

KEGG analysis showed that strain CY1T contains a complete SO4 2− reduction pathway, which is consistent with the phenotype of H2S production. The genes responsible for SO4 2− reduction include sulfate ABC transporter CysPWA, sulfate adenylyltransferase CysD, adenylylsulfate kinase CysC, adenylylsulfate reductase CysH and sulfite reductase CysJI (Table 5). The S2− generated from SO4 2− reduction could react with Cd(II) to form the participated CdS [13], which may contribute to the Cd(II) removal. For Cr(VI) reduction, five NADPH-dependent FMN reductase which have the same conserved domain as the Cr(VI) reductases ChrR (from Pseudomonas putida ) and YieF (from Escherichia coli ) [28], were identified in the genome of strain CY1T (Table 5). It has been reported that thioredoxin reductase ThxR and NADH:flavin oxidoreductase could reduce Se(IV) in Pseudomonas seleniipraecipitans and Rhizobium selenitireducens , respectively [2931]. According to the NCBI and RAST annotation, seven thioredoxin reductases and two NADH-dependent flavin oxidoreductases were found in the genome of strain CY1T (Table 5), and some of these proteins may responsible for Se(IV) reduction in strain CY1T.
Table 5

Putative proteins involved in selenite, chromate and sulfate reduction

Metal(loids)

Putative function

Locus_tag of the predicted protein

Selenite

Thioredoxin reductase

BC351_25440

Thioredoxin reductase

BC351_17745

Thioredoxin reductase

BC351_21345

Thioredoxin reductase

BC351_06135

Thioredoxin reductase

BC351_33000

Thioredoxin reductase

BC351_13625

Thioredoxin-disulfide reductase

BC351_19150

NADH-dependent flavin oxidoreductase

BC351_22155

NADH-dependent flavin oxidoreductase

BC351_12795

Chromate

NADPH-dependent FMN reductase

BC351_21415

NADPH-dependent FMN reductase

BC351_05445

NADPH-dependent FMN reductase

BC351_40245

NADPH-dependent FMN reductase

BC351_15505

NADPH-dependent FMN reductase

BC351_15285

Sulfate

Sulfate adenylyltransferase small subunit CysD

BC351_30725

Adenylyl-sulfate kinase CysC

BC351_31925

Adenylyl-sulfate kinase CysC

BC351_32075

Phosphoadenosine phosphosulfate reductase CysH

BC351_36025

Sulfate ABC transporter substrate-binding protein CysP

BC351_12315

Sulfate ABC transporter CysA

BC351_12325

Sulfate ABC transporter permease subunit CysW

BC351_12330

Sulfite reductase alpha component

BC351_31155

Sulfite reductase beta subunit

BC351_31160

Strain CY1T could tolerant multi-metal(loids), such as As(III), Sb(III), Cr(VI), Cd(II), Pb(II), Cu(II) and Mn(II). Expectably, various metal resistant genes were identified in its genome (Table 6). Several transporters were found to responsible for the efflux of these metal(loids). In addition, the transcriptional regulator ArsR and arsenite reductase ArsC were also found to be involved in the As(III)/Sb(III) resistance (Table 6) [3234]. Recently, it has been reported that an oxidoreductase AnoA, which belongs to the short-chain dehydrogenase/reductase family, and catalase KatA, which is responsible for H2O2 degradation, are all involved in bacterial Sb(III) oxidation/resistance in Agrobacterium tumefaciens GW4 [3538]. One AnoA homologue oxidoreductase gene and five catalase genes were identified in the genome of strain CY1T (Table 6), which may associate with Sb(III) oxidation/resistance.
Table 6

Putative proteins involved in metal(loid) resistance

Heavy metal

Putative function

Locus_tag of the predicted protein

Arsenic

Arsenic transporter

BC351_03410

Arsenical efflux pump membrane protein ArsB

BC351_32265

Arsenic ABC transporter ATPase

BC351_35545

ArsR family transcriptional regulator

BC351_32260

ArsR family transcriptional regulator

BC351_02635

Arsenate reductase ArsC

BC351_15540

Antimony

Oxidoreductase (putative AnoA)

BC351_17295

Catalase

BC351_40130

Catalase

BC351_06195

Catalase

BC351_15905

Catalase

BC351_07965

Catalase

BC351_29865

Chromate

ChrA protein

BC351_26450

Chromate transporter

BC351_15935

Chromate transporter

BC351_29720

Chromate transporter

BC351_29725

Cadmium, lead and zinc

Cobalt-zinc-cadmium resistance protein

BC351_15845

Cobalt-zinc-cadmium efflux system protein

BC351_17600

Cation diffusion facilitator family transporter

BC351_20420

Cation diffusion facilitator family transporter

BC351_03295

RND family efflux transporter

BC351_25240

RND family efflix transporter/ MFP transporter

BC351_17480

RND family efflux transporter, MFP subunit

BC351_10185

Efflux transporter periplasmic adaptor subunit

BC351_04820

Efflux transporter periplasmic adaptor subunit

BC351_25355

Cd2+/Zn2+-exporting ATPase \cadmium transporter

BC351_28470

HlyD family secretion protein

BC351_33510

HlyD family secretion protein\ MFP transporter

BC351_35605

Multidrug efflux pump subunit AcrA

BC351_02380

Efflux transporter periplasmic adaptor subunit

BC351_37435

Cation transporter

BC351_08750

Zinc transporter ZitB

BC351_12865

Cadmium transporter

BC351_35590

Cadmium-translocating P-type ATPase

BC351_14640

Copper

Bcr/CflA family drug resistance efflux transporter

BC351_19565

Multidrug resistance transporter, Bcr/CflA family

BC351_07275

Copper transport protein

BC351_15720

Copper-translocating P-type ATPase

BC351_26145

Copper-translocating P-type ATPase

BC351_38485

Copper-transporting P-type ATPase CopZ

BC351_38480

Manganese

Manganese transport protein MntH

BC351_25600

Manganese transport protein MntH

BC351_14100

Conclusions

The genome of P. ferrarius CY1T harbors various genes responsible for sulfate transport and reduction, chromate and selenite reduction and resistance of multi-metal(loids), which is consistent with its phenotypes. To date, the utilization of Paenibacillus species in immobilization of heavy-metals (or metalloids) is still limited and the genes and enzymes involves in Cr(VI) and Se(IV) reduction were poorly understood in Paenibacillus members. The genomic sequence of strain CY1T enriches the genome information of Paenibacillus strains. More importantly, the genome information provides basis for understanding molecular mechanisms of microbial redox transformations of metal(loids).

Declarations

Acknowledgements

We thank Mr. Xian Xia and Dr. Jing Huang for technical assistance. This study was supported by National key research and development program of China (2016YFD0800702).

Authors’ contributions

JL, WG, MS and YC conducted the study. JL performed the data analyses and wrote the manuscript. GW participated in research design and revised the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

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Authors’ Affiliations

(1)
State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University

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