Skip to content

Advertisement

  • Short genome report
  • Open Access

High-quality-draft genome sequence of the heavy metal resistant and exopolysaccharides producing bacterium Mucilaginibacter pedocola TBZ30T

Standards in Genomic Sciences201813:34

https://doi.org/10.1186/s40793-018-0337-8

  • Received: 22 March 2018
  • Accepted: 10 November 2018
  • Published:

Abstract

Mucilaginibacter pedocola TBZ30T (= CCTCC AB 2015301T = KCTC 42833T) is a Gram- negative, rod-shaped, non-motile and non-spore-forming bacterium isolated from a heavy metal contaminated paddy field. It shows resistance to multiple heavy metals and can adsorb/remove Zn2+ and Cd2+ during cultivation. In addition, strain TBZ30T produces exopolysaccharides (EPS). These features make it a great potential to bioremediate heavy metal contamination and biotechnical application. Here we describe the genome sequence and annotation of strain TBZ30T. The genome size is 7,035,113 bp, contains 3132 protein-coding genes (2736 with predicted functions), 50 tRNA encoding genes and 14 rRNA encoding genes. Putative heavy metal resistant genes and EPS associated genes are found in the genome.

Keywords

  • Mucilaginibacter pedocola
  • Genome sequence
  • Heavy metal resistance
  • Exopolysaccharides

Introduction

The genus Mucilaginibacter was first established by Pankratov et al. in 2007 and the type species is Mucilaginibacter paludis [1]. The common characteristics of this genus are Gram-negative, non-spore-forming, non-motile, rod-shaped and producing exopolysaccharides (EPS) [1, 2]. EPS are long-chain polysaccharides and consist of branched, repeating units of sugars or sugar derivatives [3]. EPS producing bacteria play an important role in environmental bioremediation such as water treatment, sludge dewatering and metal removal [4]. So far, genomic features of Mucilaginibacter strains are less studied.

Mucilaginibacter pedocola TBZ30T (= CCTCC AB 2015301T = KCTC 42833T) was isolated from a heavy metal contaminated paddy field in Hunan Province, P. R. China [5]. Here we show that strain TBZ30T is resistant to multiple heavy metals and remove Zn2+ and Cd2+. In addition, strain TBZ30T is able to produce EPS. The genomic information of strain TBZ30T are provided.

Organism information

Classification and features

Similarity analysis was performed using neighbor-joining method based on the 16S rRNA gene sequences and a phylogenetic tree was constructed using MEGA version 6.0 software (Fig. 1). Bootstrap analysis with 1000 replications was conducted to obtain confidence levels of the branches. Strain TBZ30T showed the highest 16S rRNA gene sequence similarity with Mucilaginibacter gynuensis YC7003T (95.8%), Mucilaginibacter mallensis MP1X4T (95.4%) and Mucilaginibacter litoreus BR-18T (95.4%) [68] and grouped together with M. gynuensis YC7003T (95.8%) and M. mallensis MP1X4T (Fig. 1).
Fig. 1
Fig. 1

A neighbor-joining phylogenetic tree based on 16S rRNA gene sequences showing the phylogenetic relationships of strain TBZ30T and the related species. The bootstrap value less than 50% are not shown. Bar, 0.005 substitutions per nucleotide position

Strain TBZ30T is Gram-negative, non-motile, and non-spore-forming. Cells are rod-shaped (0.3–0.4 × 1.1–1.3 μm) (Fig. 2). Colonies are circular, pink, convex and smooth on R2A agar. Growth occurs aerobically at 4–28 °C (optimum, 25 °C), pH 5.0–8.5 (optimum, pH 7.0), and in the presence of 0–1.0 (w/v) NaCl (optimum, without NaCl) (Table 1) [5]. Oxidase- and catalase-positive [5]. It can use glucose, mannose, L-arabinose, maltose, melibiose, rhamnose and glycogen as the sole carbon sources [5]. Strain TBZ30T can produce EPS testing by aniline blue staining method [9] (Fig. 3). The colonies of strain TBZ30T and the known EPS producing strain M. litoreus BR-18T are pink on LB plates (Fig. 3a and b), while the colonies are blue on LB-aniline blue plate (Fig. 3d and e). However, the colonies are always white for the negative control Nocardioides albus KCTC 9186T [10, 11] on either LB or LB-aniline blue plates (Fig. 3c and f). All of the above strains were incubated at 28 °C for 7 days. In addition, strain TBZ30T is resistant to multiple heavy metals. The minimal inhibition concentration (MIC) tests for different heavy metals were performed on R2A agar plates at 28 °C for 7 days. The MICs for ZnSO4, CdCl2, PbSO4, CuSO4 and NaAsO2 are 3.5 mM, 1.5 mM, 0.4 mM, 1.2 mM and 0.35 mM, respectively. Furthermore, strain TBZ30T could adsorb/remove nearly 60% of Zn2+ and 55% of Cd2+ in the R2A liquid medium (added with 0.3 mM ZnSO4 and 0.25 mM CdCl2, respectively) (Fig. 4). The amount of the heavy metals were detected by an atomic absorption spectrometer.
Fig. 2
Fig. 2

A scanning electron microscope (SEM) image of Mucilaginibacter pedocola TBZ30T cells. The bar scale represents 0.5 μm

Table 1

Classification and general features of Mucilaginibacter pedocola TBZ30T [39]

MIGS ID

Property

Term

Evidence codea

 

Classification

Domain Bacteria

TAS [40]

Phylum Actinobacteria

TAS [41, 42]

Class Sphingobacteria

TAS [43, 44]

Order Sphingobacteriales

TAS [45, 46]

Family Sphingobacteriaceae

TAS [47]

Genus Mucilaginibacter

TAS [1]

Species pedocola

TAS [5]

Strain TBZ30T (= CCTCC AB 2015301T = KCTC 42833T)

 

Gram stain

negative

TAS [5]

Cell shape

rod

TAS [5]

Motility

non

TAS [5]

Sporulation

non-sporulating

NAS

Temperature range

4–28 °C

TAS [5]

Optimum temperature

25 °C

TAS [5]

pH range; Optimum

5.0–8.5, 7.0

TAS [5]

Carbon source

glucose, mannose, L-arabinose, maltose, melibiose, rhamnose, rhamnose and glycogen

TAS [5]

MIGS-6

Habitat

paddy field with heavy metal

TAS [5]

MIGS-6.3

Salinity

0–1% NaCl (w/v), optimal at 0%

TAS [5]

MIGS-22

Oxygen requirement

aerobic

TAS [5]

MIGS-15

Biotic relationship

free-living

TAS [5]

MIGS-14

Pathogenicity

non-pathogen

NAS

MIGS-4

Geographic location

Linxiang city, Hunan province, China

TAS [5]

MIGS-5

Sample collection

2014

TAS [5]

MIGS-4.1

Latitude

N30°17′54”

TAS [5]

MIGS-4.2

Longitude

E109°28′16”

TAS [5]

MIGS-4.4

Altitude

not reported

 

aEvidence code-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) [48]

Fig. 3
Fig. 3

EPS detection using the aniline blue staining method [9]. a, b and c strain TBZ30T, positive control Mucilaginibacter litoreus BR-18T and negative control Nocardioides albus KCTC 9186T cultivated in LB plates, respectively; (d, e and f) the above three strains cultivated in LB-aniline blue plates, respectively

Fig. 4
Fig. 4

Zn2+ and Cd2+ removal by strain TBZ30T in R2A liquid media. a Zn2+ removal by strain TBZ30T; (b) Cd2+ removal by strain TBZ30T. The control represents R2A liquid medium with 0.3 mM Zn2+ or 0.25 mM Cd2+ without the inoculation of strain TBZ30T. Data are shown as the mean of three replicates

Genome information

Genome project history

M. pedocola TBZ30T was sequenced on the basis of its abilities of heavy metals resistance and removal, which has a great potential for bioremediation. The draft genome was sequenced by Wuhan Bio-Broad Co., Ltd., Wuhan, China. The high-quality-draft genome sequence has been deposited at DDBJ/EMBL/GenBank under the accession number MBTF00000000.1. 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

377.50×

MIGS-30

Assemblers

SOAPdenovo v2.04

MIGS-32

Gene calling method

GeneMarkS+

Locus TAG

BC343

Genbank ID

MBTF00000000.1

Genbank Date of Release

04, 25, 2017

GOLD ID

Gs0134261

Bioproject

PRJNA331061

MIGS-13

Source material identifier

Strain CCTCC AB 2015301

Project relevance

Bioremediation

Growth condition and DNA isolation

M. pedocola TBZ30T was grown in R2A medium at 28 °C for 36 h with continuous shaking at 120 rpm. Bacterial cells were harvested through centrifugation (13,400×g for 5 min at 4 °C) and the total genomic DNA was extracted using the QiAamp kit (Qiagen, Germany). The quality and quantity of the DNA were determined using a spectrophotometer (NanoDrop 2000, Thermo).

Genome sequencing and assembly

Whole-genome DNA sequencing was performed in Bio-broad Co., Ltd., Wuhan, China using Illumina standard shotgun library and Hiseq2000 pair-end sequencing strategy [12]. For accuracy of assembly, low quality of the original sequence data reads were removed. The assembly of TBZ30T genome is based on 16,967,512 quality reads totaling 2,523,391,653 bases with a 377.50× average genome coverage. The final reads were assembled into 39 contigs (> 200 bp) using SOAPdenovo v2.04 [13]. The part gaps of assembly were filled and the error bases were revised using GapCloser v1.12 [14].

Genome annotation

The genome of strain TBZ30T was annotated through the NCBI PGAP, which combined the gene caller GeneMarkS+ with the similarity-based gene detection approach [15]. Pseudo genes were predicted using the NCBI PGAP. Internal gene clustering was performed by the OrthoMCL program using Match cutoff of 50% and E-value Exponent cutoff of 1-e5 [16, 17]. The COGs functional categories were assigned by the WebMGA server with E-value cutoff of 1-e10 [18]. The translations of the predicted CDSs were used to search against the Pfam protein family database and the KEGG database [19, 20]. The transmembrane helices and signal peptides were predicted by TMHMM v. 2.0 and SignalP 4.1, respectively [21, 22].

Genome properties

The genome size of strain TBZ30T is 7,035,113 bp with an average G + C content of 46.1% (Table 3). It has 6072 genes including 5935 protein-coding genes, 70 pseudo genes and 14 rRNA, 50 tRNA, and 3 ncRNA genes. The information of the genome statistics is shown in Table 3 and the classification of genes into COGs functional categories is summarized in Table 4. The graphical genome map is provided in Fig. 5.
Table 3

Nucleotide content and gene count levels of the genome

Attribute

Value

% of total

Genome size (bp)

7,035,113

100

DNA coding (bp)

6,126,065

87.1

DNA G + C (bp)

46.1%

100

DNA scaffolds

38

100

Total genes

6072

100

Protein-coding genes

5935

97.7

RNA genes

67

1.1

Pseudo genes

70

1.2

Genes in internal clusters

587

9.7

Genes with function prediction

2736

45.1

Genes assigned to COGs

4046

66.6

Genes with Pfam domains

4434

73.0

Genes with signal peptides

1005

16.6

Genes with transmembrane helices

1407

23.2

CRISPR repeats

11

0.2

The total is based on the size of the genome in base pairs and the total number of protein coding genes in the annotated genome

Table 4

Number of genes associated with the 21 general COG functional categories

COG class

count

% of total

description

J

160

2.70

Translation, ribosomal structure and biogenesis

A

1

0.02

RNA processing and modification

K

406

6.84

Transcription

L

224

3.77

Replication, recombination and repair

B

1

0.02

Chromatin structure and dynamics

D

35

0.59

Cell cycle control, cell division, chromosome partitioning

V

88

1.48

Defense mechanisms

T

459

7.73

Signal transduction mechanisms

M

389

6.55

Cell wall/membrane/envelope biogenesis

N

23

0.39

Cell motility

U

87

1.47

Intracellular trafficking, secretion, and vesicular transport

O

123

2.07

Posttranslational modification, protein turnover, chaperones

C

185

3.12

Energy production and conversion

G

337

5.68

Carbohydrate transport and metabolism

E

247

4.16

Amino acid transport and metabolism

F

73

1.23

Nucleotide transport and metabolism

H

156

2.63

Coenzyme transport and metabolism

I

162

2.73

Lipid transport and metabolism

P

200

3.37

Inorganic ion transport and metabolism

Q

106

1.79

Secondary metabolites biosynthesis, transport and catabolism

R

593

9.99

General function prediction only

S

431

7.26

Function unknown

1449

24.41

Not in COGs

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

Fig. 5
Fig. 5

A graphical circular map of Mucilaginibacter pedocola TBZ30T. 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 show G + C % content; ring 6 shows G + C % content plot and the innermost ring shows GC skew

Insights from the genome sequence

Strain TBZ30T could be resistant to multiple heavy metals (Zn2+, Cd2+, Pb2+, Cu2+ and As3+) and adsorb/remove Zn2+ and Cd2+ during cultivation. Analyzing of its genome, various putative proteins related to multiple heavy metals resistance are found (Table 5). RND efflux systems (CzcABC), CDF efflux systems (CzcD and YieF) and P-type ATPases (HMA and ZntA) are responsible for the efflux of Zn2+, Cd2+ and Pb2+ [2327]. Zip family metal transporter and P-type ATPase ZosA are associated with the efflux of Zn2+, Cd2+ or Cu2+ [2830], and CutC is involved in Cu2+ homeostasis [3032]. Moreover, As3+ resistant proteins including arsenite efflux pump ACR3, arsenate reductase ArsC, arsenite S-adenosylmethyltransferase ArsM and arsenic resistance repressor ArsR are also found [3335] (Table 5).
Table 5

Putative protein involved in heavy metals resistance and EPS production

Heavy metals or EPS production

Putative function

Locus_tag of the predicted protein

Zinc-Cadmium-Lead resistance

 RND efflux systems

CusA/CzcA heavy metal efflux RND transporter

BC343_14685, BC343_14785

Efflux RND transporter periplasmic adaptor subunit CzcB

BC343_14680, BC343_14795

Outer membrane protein CzcC

BC343_14800

 CDF efflux systems

Cation transporter CzcD

BC343_11185

Cation transporter FieF

BC343_27530

 P-type ATPase

Heavy metal translocating P-type ATPase HMA

BC343_08790

Heavy metal translocating P-type ATPase ZosA

BC343_14675

Cadmium-translocating P-type ATPase ZntA

BC343_00930

 Zip super family

Zip family metal transporter

BC343_14670

 Copper resistance

Zip family metal transporter

BC343_14670

Heavy metal translocating P-type ATPase ZosA

BC343_14675

Copper homeostasis protein CutC

BC343_23340

 Arsenic resistance

Arsenite efflux pump ACR3

BC343_02735

Arsenate reductase ArsC

BC343_02740, BC343_24635

Arsenite S-adenosylmethyltransferase ArsM

BC343_24640

Arsenical resistance repressor ArsR

BC343_24645, BC343_02755

Nucleotide sugars biosynthesis for EPS production

 CDP-Glc

Sugar kinase

BC343_21040, BC343_04390

Phosphoglucomutas

BC343_18360

Gucose-1-phosphate cytidylyltransferase RfbF

BC343_04660

 ADP-Glc

Glucose-1-phosphate adenylyltransferase

BC343_23820

 GDP-D-man

Glucose-6-phosphate isomerase

BC343_14065

6-phosphofructokinase

BC343_20710, BC343_25175

Mannose-6-phosphate isomerase ManA

BC343_15810, BC343_21400

Phosphoglucosamine mutase phosphomannomutase

BC343_21600

Mannose-1-phosphate guanylyltransferase

BC343_03170

 EPS biosynthesis

3-Deoxy-D-manno-octulosonic-acid transferase KdtA

BC343_09425

Priming glycosyltransferase CpsE

BC343_04560

Glycosyltransferase

BC343_04600, BC343_09445

ABC transporter KpsMT

BC343_09400, BC343_09585

Polysaccharide co-polymerase protein PCP

BC343_04670

Outer membrane polysaccharide protein OPX

BC343_04675

Flippase Wzx

BC343_08105

Capsular biosynthesis protein PHP

BC343_09405

Strain TBZ30T produces EPS during cultivation. According to KEGG analysis, the complete biosynthesis pathway of repeating units of nucleotide sugars are identified in the genome, including the biosynthesis of CDP-Glc, ADP-Glc and GDP-D-man (Table 5). Genes related to long-chain polysaccharide assembly are also found (Table 5). The EPS production pathway in strain TBZ30T appears to belong to ABC transporter dependent pathway [36]. First, the 3-deoxy-D-manno-octulosonic-acid transferase (KdtA) is responsible for the synthesis of poly-Kdo linker using either diacyl or monoacyl phosphatidylglycerol as the substrate [36]; Then priming glycosyltransferase (CpsE) catalyzes the transformation of the first repeating unit to the poly-Kdo linker; Next, glycosyltransferases catalyze the synthesis of EPS repeat-unit; Finally, the polymerized repeat-units are exported through an envelope-spanning complex consisting of ABC transporter (KpsMT), polysaccharide co-polymerase protein (PCP) and outer membrane polysaccharide protein (OPX) [37, 38]. In addition, strain TBZ30T genome owns a flippase (Wzx) which catalyzes the translocation of repeat-units crossing the cytoplasmic membrane. EPS have been reported to play an important role in metal removal [3]. Therefore, it is possible that the EPS of strain TBZ30T participate in Zn2+ and Cd2+ removal by adsorption.

Conclusions

To the best of our knowledge, this study presents the first genomic information of a Mucilaginibacter type strain. The data reveal good correlation between genotypes and phenotypes. The genome information and the features provide insights for further theoretical and applied analysis of M. pedocola TBZ30T and the related Mucilaginibacter members.

Abbreviations

EPS: 

Exopolysaccharides

MIC: 

Minimal inhibition concentration

Declarations

Funding

This study was supported by National key research and development program of China (2016YFD0800702).

Authors’ contributions

XF and JT performed the phenotypic characterization, the data analysis and wrote the manuscript. LN participated in phenotypic experiments. JH participated in data analysis. GW was responsible for 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.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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 of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, 430070, People’s Republic of China

References

  1. Pankratov TA, Tindall BJ, Liesack W, Dedysh SN. Mucilaginibacter paludis gen. nov., sp. nov. and Mucilaginibacter gracilis sp. nov., pectin-, xylan- and laminarin-degrading members of the family Sphingobacteriaceae from acidic Sphagnum peat bog. Int J Syst Evol Microbiol. 2007;57(10):2349–54.View ArticlePubMedGoogle Scholar
  2. Baik KS, Park SC, Kim EM, Lim CH, Seong CN. Mucilaginibacter rigui sp. nov., isolated from wetland freshwater, and emended description of the genus Mucilaginibacter. Int J Syst Evol Microbiol. 2010;60(1):134–9.View ArticlePubMedGoogle Scholar
  3. Cui Y, Xu T, Qu X, Hu T, Jiang X, Zhao C. New insights into various production characteristics of Streptococcus thermophilus strains. Int J Mol Sci. 2016;17(10):1701.View ArticlePubMed CentralGoogle Scholar
  4. More TT, Yadav JS, Yan S, Tyagi RD, Surampalli RY. Extracellular polymeric substances of bacteria and their potential environmental applications. J Environ Manag. 2014;144:1–25.View ArticleGoogle Scholar
  5. Tang J, Huang J, Qiao Z, Wang R, Wang G. Mucilaginibacter pedocola sp. nov., isolated from a heavy-metal-contaminated paddy field. Int J Syst Evol Microbiol. 2016;66(10):4033–8.View ArticlePubMedGoogle Scholar
  6. Khan H, Chung EJ, Jeon CO, Chung YR. Mucilaginibacter gynuensis sp. nov., isolated from rotten wood. Int J Syst Evol Microbiol. 2013;63(9):3225–31.View ArticlePubMedGoogle Scholar
  7. Mannisto MK, Tiirola M, McConnell J, Haggblom MM. Mucilaginibacter frigoritolerans sp. nov., Mucilaginibacter lappiensis sp. nov. and Mucilaginibacter mallensis sp. nov., isolated from soil and lichen samples. Int J Syst Evol Microbiol. 2010;60(12):2849–56.View ArticlePubMedGoogle Scholar
  8. Yoon JH, Kang SJ, Park S, Oh TK. Mucilaginibacter litoreus sp. nov., isolated from marine sand. Int J Syst Evol Microbiol. 2012;62(12):2822–7.View ArticlePubMedGoogle Scholar
  9. K N, Devasya RP, Bhagwath AA. Exopolysaccharide produced by Enterobacter sp. YG4 reduces uranium induced nephrotoxicity. Int J Biol Macromol. 2016;82:557–61.View ArticlePubMedGoogle Scholar
  10. Prauser H. Nocardioides, a new genus of the order actinomycetales. Int J Syst Evol Microbiol. 1976;26:58–65.Google Scholar
  11. Skerman VBD, McGowan V, Sneath PHA. Approved lists of bacterial names. Int J Syst Bacteriol. 1980;30:225–420.View ArticleGoogle Scholar
  12. Bennett S. Solexa Ltd. Pharmacogenomics. 2004;5(4):433–8.View ArticlePubMedGoogle Scholar
  13. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, et al. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience. 2012;1(1):18.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 2010;20(2):265–72.View ArticlePubMedPubMed CentralGoogle Scholar
  15. 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.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Li L, Stoeckert CJ Jr, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13(9):2178–89.View ArticlePubMedPubMed CentralGoogle Scholar
  17. Fischer S, Brunk BP, 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;6:1–19.View ArticleGoogle Scholar
  18. 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.View ArticlePubMedPubMed CentralGoogle Scholar
  19. 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.View ArticleGoogle Scholar
  20. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res. 2004;32:277–80.View ArticleGoogle Scholar
  21. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305(3):567–80.View ArticleGoogle Scholar
  22. Petersen TN, Brunak S, Von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8(10):785–6.View ArticlePubMedGoogle Scholar
  23. Nies DH. CzcR and CzcD, gene products affecting regulation of resistance to cobalt, zinc, and cadmium (czc system) in Alcaligenes eutrophus. J Bacteriol. 1992;174(24):8102–10.View ArticlePubMedPubMed CentralGoogle Scholar
  24. Nies DH. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev. 2003;27(2–3):313–39.View ArticlePubMedGoogle Scholar
  25. Xiong J, Li D, Li H, Susan J, Miller LY, et al. Genome analysis and characterization of zinc efflux systems of a highly zinc-resistant bacterium, Comamonas testosteroni S44. Res Microbiol. 2011;162(7):671–9.View ArticlePubMedGoogle Scholar
  26. Rakesh S, Christopher R, Barry PR, Bharati M. The ATP hydrolytic activity of purified ZntA, a Pb(II)/cd(II)/Zn(II)-translocating ATPase from Escherichia coli. J Biol Chem. 2000;275:3873–8.View ArticleGoogle Scholar
  27. Solioz M, Vulpe C. CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem Sci. 1996;21(7):237–41.View ArticlePubMedGoogle Scholar
  28. Li S, Zhou X, Huang Y, Zhu L, Zhang S, Zhao Y, et al. Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize. BMC Plant Biol. 2013;13:114.View ArticlePubMedPubMed CentralGoogle Scholar
  29. Potocki S, Valensin D, Kozlowski H. The specificity of interaction of Zn(2+), Ni(2+) and cu(2+) ions with the histidine-rich domain of the TjZNT1 ZIP family transporter. Dalton Trans. 2014;43(26):10215–23.View ArticlePubMedGoogle Scholar
  30. Guan G, Pinochet-Barros A, Gaballa A, Patel SJ, Argüello JM, Helmann JD. PfeT, a P1B4 -type ATPase, effluxes ferrous iron and protects Bacillus subtilis against iron intoxication. Mol Microbiol. 2015;98(4):787–803.View ArticlePubMedPubMed CentralGoogle Scholar
  31. Yong-Qun Z, De-Yu Z, Hong-Xia L, Na Y, Gen-Pei L, Da-Cheng W. Purification and preliminary crystallographic studies of CutC, a novel copper homeostasis protein from Shigella flexneri. Protein Pept Lett. 2005;12:823–82.View ArticleGoogle Scholar
  32. Mauricio L, Felipe O, Reyes-Jara A, Guadalupe L, Mauricio G. CutC is induced late during copper exposure and can modify intracellular copper content in Enterococcus faecalis. Biochem Biophys Res Commun. 2011;406:633–7.View ArticleGoogle Scholar
  33. Liu G, Liu M, Kim EH, Maaty WS, Bothner B, Lei B, et al. A periplasmic arsenite-binding protein involved in regulating arsenite oxidation. Environ Microbiol. 2012;14(7):1624–34.View ArticlePubMedGoogle Scholar
  34. Li X, Zhang L, Wang G. Genomic evidence reveals the extreme diversity and wide distribution of arsenic-related genes in Burkholderides. PLoS One. 2014;9(3):e92236.View ArticlePubMedPubMed CentralGoogle Scholar
  35. Qin J, Zhang Y, Barry R, Wang G, Franke S, Rensing C. Arsenic detoxification and evolution of trimethylarsine gas by microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci. 2006;103(7):2075–80.View ArticlePubMedGoogle Scholar
  36. Schmid J, Sieber V, Rehm B. Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol. 2015;6:496.View ArticlePubMedPubMed CentralGoogle Scholar
  37. Cuthbertson L, Mainprize IL, Naismith JH, Whitfield C. Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in gram-negative bacteria. Microbiol Mol Biol Rev. 2009;73(1):155–77.View ArticlePubMedPubMed CentralGoogle Scholar
  38. Willis LM, Whitfield C. Structure, biosynthesis, and function of bacterial capsular polysaccharides synthesized by ABC transporter-dependent pathways. Carbohydr Res. 2013;378:35–44.View ArticlePubMedPubMed CentralGoogle Scholar
  39. Field D, Garrity G, 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.View ArticlePubMedPubMed CentralGoogle Scholar
  40. Woese CR, Kandler O, Wheelis 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.View ArticlePubMedPubMed CentralGoogle Scholar
  41. Goodfellow M. Phylum XXVI. Actinobacteria phyl. nov. Bergey’s Manual of Systematic Bacteriology 2012;5; Part A:33.View ArticleGoogle Scholar
  42. Stackebrandt E, Rainey FA, Ward-Rainey NL. Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Evol Microbiol. 1997;47:479–91.Google Scholar
  43. Smith C. The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol. 2002;52:7–76.View ArticleGoogle Scholar
  44. Euzéby J. Validation list no. 143. List of new names and new combinations previously effectively, but not validly, published. Int J Syst Evol Microbiol. 2012;62:1–4.View ArticleGoogle Scholar
  45. Kämpfer P. Class III. Sphingobacteriia class. nov. Bergey’s Manual of Systematic Bacteriology, vol. 4; 2011. p. 330.Google Scholar
  46. Kämpfer P. Order I. Sphingobacteriales ord nov Bergey’s Manual of Systematic Bacteriology, vol. 4; 2011. p. 330.Google Scholar
  47. Steyn PL, Segers P, Vancanneyt M, Sandra P, Kersters K, Joubert JJ. Classification of heparinolytic bacteria into a new genus, Pedobacter, comprising four species: Pedobacter heparinus comb. nov., Pedobacter piscium comb. nov., Pedobacter africanus sp. nov. and Pedobacter saltans sp. nov. Proposal of the family Sphingobacteriaceae fam. nov. Int J Syst Bacteriol. 1998;48:165–77.View ArticlePubMedGoogle Scholar
  48. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Geneontology: tool for the unification of biology. The gene ontology consortium. Nat Genet. 2000;25:25–9.View ArticlePubMedPubMed CentralGoogle Scholar

Copyright

© The Author(s). 2018

Advertisement