Open Access

Draft genomic sequence of a chromate- and sulfate-reducing Alishewanella strain with the ability to bioremediate Cr and Cd contamination

  • Xian Xia1,
  • Jiahong Li1,
  • Shuijiao Liao1, 2,
  • Gaoting Zhou1, 2,
  • Hui Wang1,
  • Liqiong Li1,
  • Biao Xu1 and
  • Gejiao Wang1Email author
Standards in Genomic Sciences201611:48

https://doi.org/10.1186/s40793-016-0169-3

Received: 19 December 2015

Accepted: 22 July 2016

Published: 5 August 2016

Abstract

Alishewanella sp. WH16-1 (= CCTCC M201507) is a facultative anaerobic, motile, Gram-negative, rod-shaped bacterium isolated from soil of a copper and iron mine. This strain efficiently reduces chromate (Cr6+) to the much less toxic Cr3+. In addition, it reduces sulfate (SO4 2−) to S2−. The S2− could react with Cd2+ to generate precipitated CdS. Thus, strain WH16-1 shows a great potential to bioremediate Cr and Cd contaimination. Here we describe the features of this organism, together with the draft genome and comparative genomic results among strain WH16-1 and other Alishewanella strains. The genome comprises 3,488,867 bp, 50.4 % G + C content, 3,132 protein-coding genes and 80 RNA genes. Both putative chromate- and sulfate-reducing genes are identified.

Keywords

Alishewanella Chromate-reducing bacterium Sulfate-reducing bacterium Cadmium Chromium

Introduction

The genus Alishewanella was established by Vogel et al., in 2000 with Alishewanella fetalis as the type species. It belongs to the family Alteromonadaceae of the class Gammaproteobacteria [1]. So far, Alishewanella contains six species: A. fetalis , Alishewanella aestuarii , Alishewanella jeotgali , Alishewanella agri and Alishewanella tabrizica and Alishewanella solinquinati [16]. The common characteristics of the genus Alishewanella are Gram-negative, rod-shaped and positive for oxidase and catalase [16]. Some Alishewanella strains were able to degrade pectin which is applicable in bioremediation of food industrial wastes [711]. Three Alishewanella strains ( A. aestuarii B11T , A. jeotgali KCTC 22429T and A. agri BL06T) have been sequenced and the pectin degradation pathway was found in their genomes [811]. Some strains of Alishewanella were reported to tolerate arsenic [12, 13], but the ability of Alishewanella strains to resist or transform other heavy metal(loids) have not been reported.

Alishewanella sp. WH16-1 was isolated from mining soil in 2009. This strain could resist to multiple heavy metals. During cultivation, it could efficiently reduce the toxic chromate (Cr6+) to the much less toxic and less bioavaliable Cr3+. It could also reduce sulfate (SO4 2−) to S2−. When Cd2+ was present, the S2− reacted with Cd2+ and precipitated as CdS. These characteristics made strain WH16-1 a great potential for bioremediate Cr and Cd contamination. In pot experiments of rice, tobacco and Chinese cabbage, with the addition of the bacterial culture, the amount of Cr and Cd in the plants decreased significantly [14]. Sequencing the genome of WH16-1 and comparing its attributes with the other Alishewanella genomes would provide a means of establishing the molecular determinants required for chromate/sulfate reduction, heavy metal resistance and pectin degradation, and for better application of these strains. Here we report the high quality draft genomic information of strain WH16-1 and compare it to the three sequenced Alishewanella genomes.

Organism information

Classification and features

Phylogenetic analysis was performed by the neighbor-joining method based on 16S rRNA gene sequences. Strain WH16-1 is closely related to A. agri BL06T (99.7 %) and A. fetalis CCUG 30811T (99.1 %) (Fig. 1). A similar result was obtained based on gyrase B gene (gyrB) sequences (Additional file 1: Figure S1). The gyrB sequences has been successfully used to establish phylogenetic relatedness in Alishewanella [1], Pseudomonas [15], Acinetobacter [16], Vibrio [17], Bacillus [18] and Shewanella [19].
Fig. 1

Phylogenetic tree highlighting the phylogenetic position of Alishewanella sp. WH16-1. The phylogenetic tree was constructed based on the 16S rRNA gene sequences. The analysis was inferred by MEGA 6.0 [45] with NJ algorithm and 1,000 bootstrap repetitions were computed to estimate the reliability of the tree

Strain WH16-1 is Gram-negative, facultatively anaerobic, motile and rod-shaped (0.3–0.5 × 1.2–2.0) (Fig. 2). Colonies are white, circular and raised on LB agar plate. Growth occurs at 4–40 °C, in 0–8 % (w/v) NaCl and at pH 4–11. Optimal growth occurs at 37 °C, 1 % (w/v) NaCl and at pH 6.0–8.0 (Table 1). It can grow in LB, trypticase soy broth and R2A medium. API 20NE test (bioMérieux) in combination of traditional classification methods were used to analyze the physiological and biochemical characteristics. Strain WH16-1 is positive for oxidase and catalase activities and is able to reduce nitrate to nitrite. It is positive for aesculinase, gelatinase, arginine dihydrolase and urease but is negative for indole and β-galactosidase. It can use D-sucrose and maltose as the sole carbon sources. It cannot assimilate D-glucose, L-arabinose, D-mannose, D-mannitol, N-acetylglucosamine, gluconate, capric acid, adipic acid, malic acid, trisodium citrate or phenylacetic acid. Most of these biochemical characteristics are similar to the other Alishewanella strains [16]. However, unlike some Alishewanella strains [811], strain WH16-1 cannot degrade pectin.
Fig. 2

Scan electron microscope (SEM) image of Alishewanella sp. WH16-1 cells. The bar scale represents 1 μm

Table 1

Classification and general features of Alishewanella sp. WH16-1 [47]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [48]

  

Phylum Proteobacteria

TAS [49, 50]

  

Class Gammaproteobacteria

TAS [5153]

  

Order Alteromonadales

TAS [5254]

  

Family Alteromonadaceae

TAS [55]

  

Genus Alishewanella

Species Alishewanella sp.

TAS [1]

  

Strain WH16-1

 
 

Gram stain

negative

IDA

 

Cell shape

rod

IDA

 

Motility

motile

IDA

 

Sporulation

non-sporulating

NAS

 

Temperature range

4–40 °C

IDA

 

Optimum temperature

37 °C

IDA

 

pH range; Optimum

4–11; 6–8

IDA

 

Carbon source

maltose, D-sucrose

IDA

MIGS-6

Habitat

soil

IDA

MIGS-6.3

Salinity

0–8 % NaCl (w/v), optimal at 1 %

IDA

MIGS-22

Oxygen requirement

facultative anaerobic

IDA

MIGS-15

Biotic relationship

free-living

IDA

MIGS-14

Pathogenicity

non-pathogen

NAS

MIGS-4

Geographic location

Huangshi city, Hubei province, China

IDA

MIGS-5

Sample collection

2009

IDA

MIGS-4.1

Latitude

N29°40′–30°15′

IDA

MIGS-4.2

Longitude

E114°31′–115°20′

IDA

MIGS-4.4

Altitude

not reported

 

These evidence codes are from the Gene Ontology project [56]

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)

a Evidence codes

Interestingly, the strain could reduce 1 mmol/L Cr6+ (added as K2CrO4) in 36 h and remove 60 μmol/L Cd2+ (added as CdCl2) in 60 h (by the production of precipitated CdS [20] in LB liquid medium) (Fig. 3). In addition, this strain is tolerant to multi-metal(loids). The minimal inhibition concentration tests for different heavy metals were carried out on LB agar plates and incubated at 37 °C for 2 days. The MICs for K2CrO4, CdCl2, PbCl2, CuCl2 and Na3AsO3 are 45, 0.08, 10, 1 and 1 mmol/L, respectively.
Fig. 3

Cr6+ and Cd2+ removed by Alishewanella sp. WH16-1. Control stands for null LB medium. Strain WH16-1 was incubated until OD600 reach 1.0, and then amended with K2CrO4 (1 mmol/L) and CdCl2 (0.06 mmol/L), respectively. The cultures were removed at 12 h intervals. After centrifuging at 12,000 rpm for 2 min, the supernatant was used to determine the residual concentration of Cr6+ and Cd2+. The concentration of Cr6+ and Cd2+ were measured by the UV spectrophotometer (DU800, Beckman, CA, USA) with the colorimetric diphenylcarbazide (DPC) method [46] and the atomic absorption spectrometry AAS, respectively

Genome sequencing information

Genome project history

Strain WH16-1 was selected for genome sequencing based on its ability to reduce Cr6+ and SO4 2− and preliminary application for soil Cr and Cd bioremediation. Since 2009, this strain has been used in both basic and bioremediation studies and the results are very promising. It was sequenced by Majorbio Bio-pharm Technology Co., Ltd, Shanghai, China. The genome sequencing and assembly information of the project is given in Table 2. The final genome consists of 133 scaffolds with approximately 345.3 × coverage. The draft genome sequence was annotated by NCBI PGAP. The genome sequence is available in DDBJ/EMBL/GenBank under accession number LCWL00000000.
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 Hiseq 2000

MIGS-31.2

Fold coverage

345.3 ×

MIGS-30

Assemblers

SOAPdenovo v1.05

MIGS-32

Gene calling method

GeneMarkS+

 

Locus TAG

AAY72

 

Genbank ID

LCWL00000000

 

Genbank Date of Release

2015.11.12

 

Bioproject

PRJNA283029

MIGS-13

Source material identifier

Strain CCTCC M201507

 

Project relevance

Bioremediation

Growth conditions and genomic DNA preparation

A single colony of strain WH16-1 was incubated into 50 ml LB medium and grown aerobically at 37 °C for 36 h with 150 rpm shaking. The cells were collected by centrifugation. The DNA was extracted, concentrated and purified using the QiAamp kit (Qiagen, Germany). A NanoDrop Spectrophotometer 2000 was used to determine the quality and quantity of the DNA. Six micrograms of DNA was sent to Majorbio Bio-pharm Technology Co., Ltd (Shanghai, China) for sequencing.

Genome sequencing and assembly

The genome sequencing of strain WH16-1 was performed on an Illumina Hiseq2000 [21] and assembled by Majorbio Bio-pharm Technology Co., Ltd, Shanghai, China. An Illumina standard shotgun library was constructed and sequenced, which generated 12,683,662 reads totaling 1,281,049,862 bp. All original sequence data can be found at the NCBI Sequence Read Archive [22]. The following steps were performed for removing low quality reads: (1) removed the adapter o reads; (2) cut the 5′ end bases which were not A, T, G, C; (3) filtered the reads which have a quality score lower than 20; (4) filtered the reads which contained N more than 10 %; and (5) removed the reads which have the length less than 25 bp after processed by the previous four steps. The reads were assembled into 156 contigs using SOAPdenovo v1.05 [23]. A total of 149 contigs were obtained after removing the contigs < 200 bp. The total size of the genome is 3,488,867 bp and the final assembly is based on 1,205 Mbp of Illumina data which provides a coverage of 345.3 × .

Genome annotation

The draft genome of WH16-1 was annotated through the NCBI PGAP, which combines the gene caller GeneMarkS+ [24] with the similarity-based gene detection approach. Protein function classification was performed by WebMGA [25] with E-value cutoff of 1-e10. The transmembrane helices were predicted by TMHMM v. 2.0 [26]. Signal peptides in the genome were predicted by SignalP 4.1 [27]. The translations of the predicted CDSs were also used to search against the Pfam protein family database with E-value cutoff of 1-e5 [28] and the KEGG database [29]. Internal gene clustering was performed by OrthoMCL using Match cutoff of 50 % and E-value Exponent cutoff of 1-e5 [30, 31].

Genome properties

The whole genome of strain WH16-1 is 3,488,867 bp in length, with an average G + C content of 50.4 %, and is distributed in 149 contigs (>200 bp). The genome properties and statistics are summarized in Table 3. There are 80 predicted RNA including 73 tRNA, 5 rRNAs and 2 ncRNA. In addition, a total of 3,132 protein-coding genes are identified. The distribution of genes into COGs functional categories is presented in Table 4.
Table 3

Nucleotide content and gene count levels of the genome

Attribute

Genome (total)

 

Value

% of totala

Genome size (bp)

3,488,867

100.00

DNA coding (bp)

3,117,033

89.34

DNA G + C (bp)

1,759,785

50.44

DNA scaffolds

133

100.00

Contigs

149

100.00

Total genesb

3,282

 

RNA genes

80

 

Pseudo genes

73

 

Protein-coding genes

3,132

100.00

Genes in internal clusters

1,190

37.99

Genes with function prediction

2,388

76.25

Genes assigned to COGs

2,249

71.81

Genes with Pfam domains

2,710

86.53

Genes with signal peptides

367

11.72

Genes with transmembrane helices

1,101

35.15

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

bAlso includes 73 pseudogenes, 73 tRNA genes, 5 rRNAs and 2 ncRNA

Table 4

Number of genes associated with the 25 general COG functional categories

Code

Value

% of totala

Description

J

175

5.59

Translation

A

1

0.03

RNA processing and modification

K

153

4.89

Transcription

L

141

4.50

Replication, recombination and repair

B

2

0.06

Chromatin structure and dynamics

D

34

1.09

Cell cycle control, mitosis and meiosis

Y

0

0.00

Nuclear structure

V

56

1.79

Defense mechanisms

T

216

6.90

Signal transduction mechanisms

M

156

4.98

Cell wall/membrane biogenesis

N

87

2.78

Cell motility

Z

0

0.00

Cytoskeleton

W

0

0.00

Extracellular structures

U

77

2.46

Intracellular trafficking and secretion

O

116

3.70

Posttranslational modification, protein turnover, chaperones

C

157

5.01

Energy production and conversion

G

90

2.87

Carbohydrate transport and metabolism

E

207

6.61

Amino acid transport and metabolism

F

62

1.98

Nucleotide transport and metabolism

H

132

4.21

Coenzyme transport and metabolism

I

85

2.71

Lipid transport and metabolism

P

148

4.73

Inorganic ion transport and metabolism

Q

41

1.31

Secondary metabolites biosynthesis, transport and catabolism

R

244

7.79

General function prediction only

S

202

6.45

Function unknown

-

885

28.26

Not in COGs

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

Insights from the genome sequence

Strain WH16-1 has the genes for a complete SO4 2− reduction pathway according to the KEGG analysis, including CysPUWA, CysN, CysD, CysC, CysH and CysIJ (Additional file 1: Figure S2; Additional file 2: Table S1). This pathway contained several steps: 1) the SO4 2− is uptaken by the putative CysPUWA into the cell [32]; 2) the intracellular SO4 2− is acetylated to adenylylsulphate (APS) by sulfate adenylyltransferases CysN and CysD [33]; 3) the APS is phosphorylated to phosphoadenylylsulphate (PAPS) by APS kinase CysC and, 4) the PAPS is reduced to sulfite (SO3 2−) by PAPS reductase CysH [33] and, 5) the SO3 2− is finally reduced to sulfide (S2−) by sulfite reductase CysIJ [33]. Strain WH16-1 was able to remove Cd2+ most probably due to the reaction between S2− and Cd2+ to form the precipitated CdS [20]. For Cr6+ reduction, a putative chromate reductase YieF was found (Additional file 2: Table S1). YieF was reported to responsible for the reduction of Cr6+ in cytoplasm [34]. An individual chromate transport gene chrA and a chromate resistance cluster including chrBAC, hp1, chrF, lppy/lpqo, hp2 and ABC transport permease gene are found in the genome (Additional file 2: Table S2) [35, 36]. Currently, we have disrupted the chrA (AAY72_02075) and the ABC transport permease genes, respectively. The chromate resistance levels were both decreased significantly in the chrA and ABC transport permease gene mutant strains (data not shown).

In addition, various heavy metal transformation and resistance determinants are identified in the genome of strain WH16-1 Several transporters (MntH, CzcA and ZntA) that might be involved in the efflux of Cd2+, Pb2+ and Zn2+ are found [3739]. Cu2+, As3+ and Hg2+ resistance determinants are also present, such as Cu transporter ATPase [40], Cu2+ resistance system CopABCD [41], Ars [42] and Pst [43] systems for arsenic resistance and MerTPADE system for mercury resistance [44] (Additional file 2: Table S2).

Strain WH16-1 has a genome size (3.49 Mbp), similar to A. jeotgali KCTC 22429T (3.84 Mbp), A. aestuarii B11T (3.59 Mbp) and A. agri BL06T (3.49 Mbp) [810] (Fig. 4). The G + C content of strain WH16-1 (50.4 %) is also consistent with the other Alishewanella strains ( A. jeotgali KCTC 22429T , 50.7 %, A. aestuarii B11T, 51 % and A. agri BL06T, 50.6 %). Strain WH16-1 shares 2,474 proteins with the other three Alishewanella genomes and has 217 strain-specific proteins (Fig. 5). The 2,474 core genes include yieF, chrA, the ten genes in the whole sulfate reduction pathway and most of the heavy metal resistance genes (Additional file 2: Table S1-S2). Strain WH16-1 possesses the higher number of chromatin resistance genes compared to the other three strains.
Fig. 4

A graphical circular map of the comparison between reference strain Alishewanella sp. WH16-1 and three sequenced strains of the Alishewanella species. From outside to center, rings 1, 4 show protein-coding genes colored by COG categories on forward/reverse strand; rings 2, 3 denote genes on forward/reverse strand; rings 5, 6, 7 show the CDS vs CDS BLAST results of strain WH16-1 with those of A. agri BL06T, A. jeotgali KCTC 22429T and A. aestuarii B11T, respectively; ring 8 shows G + C % content plot and the innermost ring shows GC skew

Fig. 5

The Venn diagram depicting the core and unique genes between Alishewanella sp. WH16-1 and other three Alishewanella species (A. agri BL06T, A. jeotgali KCTC 22429T and A. aestuarii B11T)

In addition, A. agri BL06T, A. jeotgali KCTC 22429T and A. aestuarii B11T were all reported to have the ability of degrading pectin and possess pectin degradation genes [811]. However, unlike strains BL06T, KCTC 22429T and B11T, strain WH16-1 was unable to degrade pectin and the pectin degradation genes are not found in its genome. Since strain WH16-1 was isolated from a heavy metal rich environment, it may be more relevant for bioremediation of heavy metal contamination. The pectin degradation genes may be lost during the evolution.

Conclusions

The genomic results of Alishewanella sp. WH16-1 reveal correlation between the gene types and some phenotypes. The strain harbors various genes responsible for sulfate transport and reduction, chromate reduction and resistance of multi-heavy metals. These observations provide insights into understand the molecular mechanisms of heavy metals. In addition, all of the analyzed Alishewanella genomes have putative sulfate and chromate reduction genes, which indicates that sulfate and chromate reduction may be the important characters of the Alishewanella strains. Thus, these strains have a great potential for application in bioremediation of heavy metal or other industrial wastes.

Abbreviation

PGAP: 

Prokaryotic Genome Annotation Pipeline

Declarations

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31470226).

Authors’ contributions

XX carried out biochemical tests, sequence analysis and preparation of the draft. JL participated in the metal resistance test and phylogenetic analysis. GZ and LL did metal reduction and metal removing tests. HW and BX conducted strain isolation. GW and SL participated in research design and helped to draft the manuscript. All authors read and approved the final manuscript.

Competing interests

The abilities to reduce Cr6+ and immobilize Pb2+ and Cd2+ of strain WH16-1 were described in China Patent, 2015; CN 104,928,213 A [14]. Due to these abilities, strain WH16-1 has a great potential for application in bioremediation of heavy metal. All the authors of this paper and the inventors of the patent [14] declare that they have no commercial or non-commercial competing interests.

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Authors’ Affiliations

(1)
State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University
(2)
College of Basic Sciences, Huazhong Agricultural University

References

  1. Vogel BF, Venkateswaran K, Christensen H, Falsen E, Christiansen G, Gram L. Polyphasic taxonomic approach in the description of Alishewanella fetalis gen. nov., sp. nov., isolated from a human foetus. Int J Syst Evol Microbiol. 2000;50:1133–42. PMID: 10843055.View ArticlePubMedGoogle Scholar
  2. Roh SW, Nam YD, Chang HW, Kim KH, Kim SM, Oh HM, Bae JW. Alishewanella aestuarii sp. nov., isolated from tidal flat sediment, and emended description of the genus Alishewanella. Int J Syst Evol Microbiol. 2009;59:421–4. doi:10.1099/ijs.0.65643-0. PMID: 19196789.View ArticlePubMedGoogle Scholar
  3. Kim MS, Roh SW, Nam YD, Chang HW, Kim KH, Jung MJ, et al. Alishewanella jeotgali sp. nov., isolated from traditional fermented food, and emended description of the genus Alishewanella. Int J Syst Evol Microbiol. 2009;59:2313–6. doi:10.1099/ijs.0.007260-0. PMID: 19620373.View ArticlePubMedGoogle Scholar
  4. Kim MS, Jo SK, Roh SW, Bae JW. Alishewanella agri sp. nov., isolated from landfill soil. Int J Syst Evol Microbiol. 2010;60:2199–203. doi:10.1099/ijs.0.011684-0. PMID: 19897613.View ArticlePubMedGoogle Scholar
  5. Tarhriz V, Nematzadeh G, Vahed SZ, Hejazi MA, Hejazi MS. Alishewanella tabrizica sp. nov., isolated from Qurugöl Lake. Int J Syst Evol Microbiol. 2012;62:1986–91. doi:10.1099/ijs.0.031567-0. PMID: 22003035.View ArticlePubMedGoogle Scholar
  6. Kolekar YM, Pawar SP, Adav SS, Zheng LQ, Li WJ, et al. Alishewanella solinquinati sp. nov., isolated from soil contaminated with textile dyes. Curr Microbiol. 2013;67(4):454–9. doi:10.1007/s00284-013-0385-7. PMID: 23689942.View ArticlePubMedGoogle Scholar
  7. Miran W, Nawaz M, Jang J, Lee DS. Conversion of orange peel waste biomass to bioelectricity using a mediator-less microbial fuel cell. Sci Total Environ. 2016;547:197–205. doi:10.1016/j.scitotenv.2016.01.004. PMID: 26780146.View ArticlePubMedGoogle Scholar
  8. Jung J, Choi S, Chun J, Park W. Genome sequence of pectin-degrading Alishewanella aestuarii strain B11T, isolated from tidal flat sediment. J Bacteriol. 2012;194(19):5476. doi:10.1128/JB.01255-12. PMID: 22965096.View ArticlePubMedPubMed CentralGoogle Scholar
  9. Kim J, Jung J, Sung JS, Chun J, Park W. Genome sequence of pectin-degrading Alishewanella agri, isolated from landfill soil. J Bacteriol. 2012;194(18):5135–6. doi:10.1128/JB.01129-12. PMID: 22933763.View ArticlePubMedPubMed CentralGoogle Scholar
  10. Jung J, Chun J, Park W. Genome sequence of extracellular-protease-producing Alishewanella jeotgali isolated from traditional Korean fermented seafood. J Bacteriol. 2012;194(8):2097. doi:10.1128/JB.00153-12. PMID: 22461542.View ArticlePubMedPubMed CentralGoogle Scholar
  11. Jung J, Park W. Comparative genomic and transcriptomic analyses reveal habitat differentiation and different transcriptional responses during pectin metabolism in Alishewanella species. Appl Environ Microbiol. 2013;79:6351–61. doi:10.1128/AEM.02350-13. PMID: 23934491.View ArticlePubMedPubMed CentralGoogle Scholar
  12. Shah R, Jha S. Alishewanella sp. strain GIDC-5, Arsenite hyper-tolerant bacteria isolated from industrial effluent of South Gujarat, India. Chem Ecol. 2013;29(5):427–36. doi:10.1080/02757540.2013.774379.View ArticleGoogle Scholar
  13. Li P, Wang Y, Dai X, Zhang R, Jiang Z, Jiang D, et al. Microbial community in high arsenic shallow groundwater aquifers in Hetao Basin of Inner Mongolia, China. PLoS One. 2015;10(5):e0125844. doi:10.1371/journal.pone.0125844. PMID: 25970606.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Liao S, Wang G, Zhou G, Xia X, Wang H. An Alishewanella strain with the ability to bioremediate heavy metal contamination. China Patent. 2015; CN 104,928,213 A.Google Scholar
  15. Yamamoto S, Harayama S. PCR Amplification and direct sequencing of gyrB genes with universal primers and their application to the detection and taxonomic analysis of Pseudomonas putida strains. Appl Environ Microbiol. 1995;61(10):3768. PMID: 7793912.PubMedPubMed CentralGoogle Scholar
  16. Yamamoto S, Harayama S. Phylogenetic analysis of Acinetobacter strains based on the nucleotide sequences of gyrB genes and on the amino acid sequences of their products. Int J Syst Bacteriol. 1996;46(2):506–11. PMID: 8934907.View ArticlePubMedGoogle Scholar
  17. Venkateswaran K, Dohmoto N, Harayama S. Cloning and nucleotide sequence of the gyrB gene of Vibrio parahaemolyticus and its application in detection of this pathogen in shrimp. Appl Environ Microbiol. 1998;64(2):681–7. PMID: 9464408.PubMedPubMed CentralGoogle Scholar
  18. Yamada S, Ohashi E, Agata N, Venkateswaran K. Cloning and nucleotide sequence analysis of gyrB of Bacillus cereus, B. thuringiensis, B. mycoides, and B. anthracis and their application to the detection of B. cereus in rice. Appl Environ Microbiol. 1999;65(4):1483–90. PMID: 10103241.PubMedPubMed CentralGoogle Scholar
  19. Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, et al. Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol. 1999;49:705–24. PMID: 10319494.View ArticlePubMedGoogle Scholar
  20. Pagnanelli F, Cruz Viggi C, Toro L. Isolation and quantification of cadmium removal mechanisms in batch reactors inoculated by sulphate reducing bacteria: biosorption versus bioprecipitation. Bioresour Technol. 2010;101(9):2981–7. doi:10.1016/j.biortech.2009.12.009. PMID: 20053554.View ArticlePubMedGoogle Scholar
  21. Bennett S. Solexa Ltd. Pharmacogenomics. 2004;5:433–8.View ArticlePubMedGoogle Scholar
  22. The NCBI Sequence Read Archive (SRA). [http://www.ncbi.nlm.nih.gov/Traces/sra/].Google Scholar
  23. Li R, Li Y, Kristiansen K, Wang J. SOAP: short oligonucleotide alignment program. Bioinformatics. 2008;24:713–4. doi:10.1093/bioinformatics/btn025. PMID: 18227114.View ArticlePubMedGoogle Scholar
  24. Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res. 2001;29(12):2607–18. PMID: 11410670.View ArticlePubMedPubMed CentralGoogle Scholar
  25. Wu S, Zhu Z, Fu L, Niu B, Li W. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics. 2011;12:444. doi:10.1186/1471-2164-12-444. PMID: 21899761.View ArticlePubMedPubMed CentralGoogle Scholar
  26. Krogh A, Larsson BÈ, Von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305:567–80. PMID: 11152613.View ArticlePubMedGoogle Scholar
  27. Petersen TN, Brunak S, Heijne GV, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785–6. doi:10.1038/nmeth.1701. PMID: 21959131.View ArticlePubMedGoogle Scholar
  28. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42:222–30. doi:10.1093/nar/gkt1223. PMID: 24288371.View ArticleGoogle Scholar
  29. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res. 2004;32:277–80. PMID: 14681412.View ArticleGoogle Scholar
  30. Li L, Stoeckert Jr CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13:2178–89. PMID: 12952885.View ArticlePubMedPubMed CentralGoogle Scholar
  31. Fischer S, Brunk B P, Chen F, Gao X, Harb OS, Iodice JB, et al. Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new ortholog groups. Curr Protoc Bioinformatics. 2011:6–12. doi: 10.1002/0471250953.bi0612s35. PMID: 21901743Google Scholar
  32. Sirko A, Zatyka M, Sadowy E, Hulanicka D. Sulfate and thiosulfate transport in Escherichia coli K-12: evidence for a functional overlapping of sulfate- and thiosulfate-binding proteins. J Bacteriol. 1995;177(14):4134–6. PMID: 7608089.PubMedPubMed CentralGoogle Scholar
  33. Sekowska A, Kung HF, Danchin A. Sulfur metabolism in Escherichia coli and related bacteria: facts and fiction. J Mol Microbiol Biotechnol. 2000;2(2):145–77. PMID: 10939241.PubMedGoogle Scholar
  34. Ackerley DF, Gonzalez CF, Park CH, Blake R, Keyhan M, Matin A. Chromate-reducing properties of soluble flavoproteins from Pseudomonas putida and Escherichia coli. Appl Environ Microbiol. 2004;70(2):873–82. PMID: 14766567.View ArticlePubMedPubMed CentralGoogle Scholar
  35. Branco R, Chung AP, Johnston T, Gurel V, Morais P, Zhitkovich A. The chromate-inducible chrBACF operon from the transposable element TnOtChr confers resistance to chromium (VI) and superoxide. J Bacteriol. 2008;190:6996–7003. doi:10.1128/JB.00289-08. PMID: 18776016.View ArticlePubMedPubMed CentralGoogle Scholar
  36. Henne KL, Nakatsu CH, Thompson DK, Konopka AE. High-level chromate resistance in Arthrobacter sp. strain FB24 requires previously uncharacterized accessory genes. BMC Microbiol. 2009;9:199. doi:10.1186/1471-2180-9-199. PMID: 19758450.View ArticlePubMedPubMed CentralGoogle Scholar
  37. Makui H, Roig E, Cole ST, Helmann JD, Gros P, Cellier MF. Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol Microbiol. 2000;35(5):1065–78. PMID: 10712688.View ArticlePubMedGoogle Scholar
  38. Nies DH, Nies A, Chu L, Silver S. Expression and nucleotide sequence of a plasmid-determined divalent cation efflux system from Alcaligenes eutrophus. Proc Natl Acad Sci U S A. 1989;86(19):7351–5. PMID: 2678100.View ArticlePubMedPubMed CentralGoogle Scholar
  39. Rensing C, Mitra B, Rosen BP. The zntA gene of Escherichia coli encodes a Zn (II)-translocating P-type ATPase. Proc Natl Acad Sci U S A. 1997;94(26):14326–31. PMID: 9405611.View ArticlePubMedPubMed CentralGoogle Scholar
  40. Odermatt A, Suter H, Krapf R, Solioz M. Primary structure of two P-type ATPases involved in copper homeostasis in Enterococcus hirae. J Biol Chem. 1993;268(17):12775–9. PMID: 8048974.PubMedGoogle Scholar
  41. Adaikkalam V, Swarup S. Characterization of copABCD operon from a copper-sensitive Pseudomonas putida strain. Can J Microbiol. 2005;51(3):209–16. PMID: 15920618.View ArticlePubMedGoogle Scholar
  42. Kruger MC, Bertin PN, Heipieper HJ, Arsène-Ploetze F. Bacterial metabolism of environmental arsenic--mechanisms and biotechnological applications. Appl Microbiol Biotechnol. 2013;97(9):3827–41. doi:10.1007/s00253-013-4838-5. PMID: 23546422.View ArticlePubMedGoogle Scholar
  43. Rosen BP, Ajees AA, McDermott TR. Life and death with arsenic. Arsenic life: an analysis of the recent report “A bacterium that can grow by using arsenic instead of phosphorus”. Bioessays. 2011;33(5):350–7. doi:10.1002/bies.201100012. PMID: 21387349.View ArticlePubMedPubMed CentralGoogle Scholar
  44. Nascimento AM, Chartone-Souza E. Operon mer: bacterial resistance to mercury and potential for bioremediation of contaminated environments. Genet Mol Res. 2003;2(1):92–101. PMID: 12917805.PubMedGoogle Scholar
  45. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9. doi:10.1093/molbev/mst197. PMID: 24132122.View ArticlePubMedPubMed CentralGoogle Scholar
  46. Monteiro MI, Fraga IC, Yallouz AV, de Oliveira NM, Ribeiro SH. Determination of total chromium traces in tannery effluents by electrothermal atomic absorption spectrometry, flame atomic absorption spectrometry and UV-visible spectrophotometric methods. Talanta. 2002;58(4):629–33. PMID: 18968791.View ArticlePubMedGoogle Scholar
  47. Field D, Garrity GM, Gray T, Morrison N, Selengut J, Sterk P, et al. The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol. 2008;26:541–7. doi:10.1038/nbt1360. PMID: 18464787.View ArticlePubMedPubMed CentralGoogle Scholar
  48. Woese CR, Kandler O, Weelis ML. Towards a natural system of organisms: proposal for the domains archaea, bacteria and eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–9. PMID: 2112744.View ArticlePubMedPubMed CentralGoogle Scholar
  49. Garrity GM, Bell JA, Phylum Lilburn T, XIV. Proteobacteria phyl nov. In: Brenner DJ, Krieg NR, Stanley JT, Garrity GM, editors. Bergey’s Manual of Sytematic Bacteriology, second edition. Vol. 2 (The Proteobacteria), part B (The Gammaproteobacteria). New York: Springer; 2005. p. 1.Google Scholar
  50. Stackebrandt E, Murray RGE, Trüper HG. Proteobacteria classis nov., a name for the phylogenetic taxon that includes the “purple bacteria and their relatives”. Int J Syst Evol Microbiol. 1988;38(3):321–5.Google Scholar
  51. Garrity GM, Bell JA, Class LT, III. Gammaproteobacteria class. nov. In: Brenner DJ, Krieg NR, Stanley JT, Garrity GM, editors. Bergey’s Manual of Sytematic Bacteriology, second edition. Vol. 2 (The Proteobacteria), part B (The Gammaproteobacteria). New York: Springer; 2005. p. 1.Google Scholar
  52. Validation of publication of new names and newcombinations previously effectively published outside the IJSEM. List no. 106. Int J Syst Evol Microbiol. 2005;55:2235–38.Google Scholar
  53. Williams KP, Kelly DP. Proposal for a new class within the phylum Proteobacteria, Acidithiobacillia classis nov., with the type order Acidithiobacillales, and emended description of the class Gammaproteobacteria. Int J Syst Evol Microbiol. 2013;63:2901–6. doi:10.1099/ijs.0.049270-0. PMID: 23334881.View ArticlePubMedGoogle Scholar
  54. Bowman JP, Mcmeekin TA, Order X. Alteromonadales ord. nov. In: Brenner DJ, Krieg NR, Stanley JT, Garrity GM, editors. Bergey’s Manual of Sytematic Bacteriology, second edition. Vol. 2 (The Proteobacteria), part B (The Gammaproteobacteria). New York: Springer; 2005. p. 443.Google Scholar
  55. Ivanova EP, Mikhaĭlov VV. A new family of Alteromonadaceae fam. nov., including the marine proteobacteria species Alteromonas, Pseudoalteromonas, Idiomarina and Colwellia. Microbiology. 2001;70(1):10–7.View ArticleGoogle Scholar
  56. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet. 2000;25:25–9. PMID: 10802651.View ArticlePubMedPubMed CentralGoogle Scholar

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