Skip to main content

Advertisement

High-quality-draft genome sequence of the multiple heavy metal resistant bacterium Pseudaminobacter manganicus JH-7T

Article metrics

  • 868 Accesses

  • 1 Citations

Abstract

Pseudaminobacter manganicus JH-7T (= KCTC 52258T = CCTCC AB 2016107T) is a Gram-staining-negative, aerobic and non-motile strain that was isolated from a manganese mine. The strain JH-7T shows multiple heavy metal resistance and can effectively remove Mn2+ and Cd2+. In addition, it is able to produce exopolysaccharides (EPS), which may contribute to metal remove/adsorption. Thus, strain JH-7T shows a great potential in bioremediation of heavy metal-contaminated environment. In this study, we report the draft genomic sequence of P. manganicus JH-7T and compare it to related genomes. Strain JH-7T has a 4,842,937 bp genome size with a G + C content of 61.2%, containing 4504 protein-coding genes and 71 RNA genes. A large number of putative genes associated with heavy metal resistance and EPS synthesis are found in the genome.

Introduction

Genus Pseudaminobacter was established by Kämpfer et al. in 1999 and contains three species represented by Pseudaminobacter salicylatoxidans BN12T (type species) [1], Pseudaminobacter defluvii THI 051T [1] and Pseudaminobacter manganicus JH-7T [2]. The common characteristics of Pseudaminobacter strains are Gram-staining-negative, rod-shaped and aerobic [1, 2]. P. salicylatoxidans BN12T contains a peculiar ring-fission dioxygenase with the ability to cleave salicylate in 1, 2-position to 2-oxohepta-3, 5-dienedioic acid [3].

P. manganicus JH-7T was isolated from a sludge sample of a wastewater ditch in Dalong manganese mine in 2015 [2]. It shows multiple heavy metal resistance and can effectively remove Mn2+ and Cd2+. In addition, the strain produces EPS, which may facilitate heavy metal resistance and adsorption [4,5,6]. These features show great interests because of its potential applications in bioremediation of heavy metal contaminated environments. So far, only the genome of an atypical Pseudaminobacter strain Pseudaminobacter salicylatoxidans KCT001 has been sequenced [7]. Strain KCT001 can utilize tetrathionate as the substrate for sulfur-oxidizing chemolithotrophic growth [8]. For better understanding the mechanism of bacterial resistance and removal of heavy metals, here we analyze the genome of P. manganicus JH-7T.

Organism information

Classification and features

The phylogenetic relationship of P. manganicus JH-7T to the related members is shown in a 16S rRNA gene based neighbor-joining tree. Strain JH-7T is closely related to P. salicylatoxidans BN12T, P. defluvii THI 051T and P. salicylatoxidans KCT001 (Fig. 1). Strain JH-7T is Gram-staining-negative, aerobic, non-motile and rod-shaped (0.3–0.8 × 1–2 μm) (Fig. 2). The colonies are white, circular, entire, slightly raised and smooth on LB agar plates. It is positive for oxidase and catalase activities and hydrolysis of casein [2]. The major fatty acids are C18:1 ω7c, C19:0 cyclo ω8c and C16:0 and the G + C content is 61.2 mol% [2]. The major polyamine is sym-homospermidine and the respiratory quinone is ubiquinone-10. The polar lipids are phosphatidylmonomethylethanolamine, diphosphatidylglycerol, phosphatidylglycerol, phosphatidylcholine, two aminolipids and two lipids [2]. Table 1 shows the general features of P. manganicus JH-7T.

Fig. 1
figure1

Phylogenetic tree highlighting the phylogenetic position of Pseudaminobacter manganicus JH-7T. The phylogenetic tree was constructed based on the 16S rRNA gene sequences. The analysis was inferred by MEGA 6.0 [41] with neighbor-joining algorithm and 1000 bootstrap repetitions were computed to estimate the reliability of the tree. Bar, 0.005 substitutions per nucleotide position

Fig. 2
figure2

Transmission electron micrograph image of strain JH-7T. Bar, 0.5 μm

Table 1 Classification and general features of P. manganicus JH-7T [42]

The resistant levels of P. manganicus JH-7T to multiple metal(loid)s were tested with the MIC on LB agar plates incubated at 28 °C for 7 days. The MICs for MnCl2, CdCl2, PbCl2, CuCl2, ZnSO4 and NiSO4 are100, 2, 10, 5, 5 and 5 mmol/L respectively. The MICs for K2CrO4 and Na3AsO3 are both 0.1 mmol/L that are lower than the above six metals. Specifically, strain JH-7T could remove nearly 60% of 5 mmol/L Mn2+ and nearly 80% of 0.1 mmol/L Cd2+ (Fig. 3), respectively. In addition, strain JH-7T could produce EPS based on the aniline blue reaction incubated on LB agar in 3–7 days [9] (data not shown). This phenomenon is consistent with the cell image observed by TEM (Fig. 2). A lay of shadow around the strain was similar to the EPS observed in strain Bifidobacterium longum 35,624 [10].

Fig. 3
figure3

Mn2+ and Cd2+ removed by P. manganicus JH-7T. Control stands for null LB medium. Strain JH-7T was incubated until OD600 reach 1.0, and then amended with 5000 μmol/L MnCl2 (a) and 100 μmol/L CdCl2 (b), respectively. The cultures were removed at 24 h intervals. After centrifuging at 12,000 rpm for 10 min, the supernatant was used to determine the residual concentration of Mn2+ and Cd2+ by the atomic absorption spectrometry AAS (AAS; 986A, Beijing Puxi General Instrument 197 Co., Beijing, China). Bars represent the mean ± SD of three biological replicates

Genome sequencing information

Genome project history

This organism was selected for sequencing particularly due to its multiple heavy metals resistance and heavy metal removal ability. Genome sequencing was performed by Wuhan Bio-Broad Co., Ltd., Wuhan, China in 2016. The draft genome sequence of strain P. manganicus JH-7T has been deposited at DDBJ/EMBL/GenBank under accession number MDET00000000. The project information is summarized in Table 2.

Table 2 Project information

Growth conditions and genomic DNA preparation

P. manganicus JH-7T was grown under aerobic conditions in LB medium at 28 °C for 40 h. DNA extraction was performed using the QiAamp kit (Qiagen, Germany) as the manufacturer’s instructions. A NanoDrop Spectrophotometer 2000 was used to determine the quality and quantity of the DNA. Seven microgram of DNA was sent to Bio-broad Technogoly Co., Ltd., Wuhan, China for sequencing.

Genome sequencing and assembly

The genome of strain JH-7T was sequenced on Illumina Hiseq2000 [11] and assembled by Bio-broad Technogoly Co., Ltd., Wuhan using SOAPdenovo v2.04 [12]. An Illumina standard shotgun library was constructed and sequenced, which generated 19,404,755 reads totaling 2,885,684,230 bp and average of 625 times genome coverage. The total size of the genome is 4,842,937 bp and a total of 60 scaffolds were obtained after arranging 68 contigs together. The part gaps of assembly were filled and the error bases were revised using GapCloser v1.12 [13].

Genome annotation

The draft genome was annotated through the NCBI Prokaryotic Genome Annotation Pipeline (PGAP), and genes were identified using the gene caller GeneMarkS+ with the similarity-based gene detection approach [14]. The predicted CDSs were translated and were submitted to the Pfam protein family database [15] and KEGG database [16]. The genes in internal clusters were performed by OrthoMCL [17, 18]. The protein function classification, transmembrane helices and signal peptides were predicted by WebMGA [19], TMHMM v. 2.0 [20] and SignalP 4.1 [21], respectively. In addition, the CRISPRfinder program [22] was used to predict CRISPRs in the genome.

Genome properties

The draft genome size of strain JH-7T is 4,842,937 bp with 61.2 mol% G + C content and contains 60 scaffolds. The genome properties and statistics are shown in Table 3. From a total of 4685 genes, 4504 (96.2%) are protein coding genes, 110 (2.3%) are pseudo genes and the rest are 71 predicted RNA genes, including 54 tRNA, 12 rRNAs and 5 ncRNA. In addition, 3729 (82.8%) protein coding genes are distributed into COG functional categories (Table 4).

Table 3 Genome statistics
Table 4 Number of genes associated with the 25 general COG functional categories

Insights from the genome sequence

Strain JH-7T could tolerant multiple heavy metals (Mn2+, Cd2+, Pb2+, Cu2+, Zn2+ and Ni2+) and remove Mn2+ and Cd2+, suggesting that it has developed a number of evolutionary strategies to adapt the mine environment. According to the genome annotation results, strain JH-7T harbors various putative proteins related to heavy metal(loid)s resistance including transporters, resistance proteins and metal reductases (Additional file 1: Table S1). MntH [23] and metal ABC transport system [24] are involved in cation uptake. Heavy metal-transporting ATPase is responsible for the efflux of Pb2+, Zn2+, Cd2+ and Ni2+ [25,26,27,28]. The genome contains Cu2+ efflux system CopABC [29], mercuric reductase MerA and regulator MerR [30]. Athough the MICs for Cr6+ and As3+ are not high, the Cr6+ efflux protein ChrA [27, 31] and As3+ resistant proteins (ArsRHC and ACR3) [32,33,34] are present.

EPS are long-chain polysaccharides consisting of branched, repeating units of sugars or sugar derivatives [35]. Stain JH-7T could produce EPS and all essential proteins for EPS production are found in the genome. Four complete nucleotide sugar synthesis (EPS precursor) pathways are identified based on KEGG analysis (Additional file 1: Table S2) including the syntheses of UDP-glucose, UDP-galactose, UDP-GlcNAc and GDP-D-mannose (Fig. 4a). EPS assembly gene clusters were also found in the genome of strain JH-7T [36] (Additional file 1: Table S3, Fig. 4b). Based on gene analysis, it is suggested that the EPS assembly in strain JH-7T might belong to Wzx/Wzy-dependent pathway [37], e.g., repeat units are assembled by glycosyltransferases (EpsI) and translocated across the cytoplasmic membrane to periplasm by flippase (Wzx) [37] and WbaP [38]. Next, Wzy (RfaL), polysaccharide co-polymerase (GumC) and the outer membrane polysaccharide exporter (GumB) transports the polymerized repeat units to cell surface [37, 39]. EPS has been reported to contribute to heavy metal removal/adsorption in bacteria [3,4,5,6]. Hence, the ability of EPS may contribute to Mn2+ and Cd2+ removal.

Fig. 4
figure4

Putative nucleotide sugars biosynthesis pathway and EPS synthesis gens in P. manganicus JH-7T. a The predicted nucleotide sugars biosynthesis pathway. The numbers refer to the enzymes involved: 1, Glucokinase; 2, α-D-glucose phosphate-specific phosphoglucomutase; 3, UTP--glucose-1-phosphate uridylyltransferase; 4, UDP-glucose 4-epimerase GalE; 5, Glucose-6-phosphate isomerase; 6, Fructokinase; 7, Glutamine--fructose-6-phosphate aminotransferase; 8, Phosphoglucosamine mutase; 9, UDP-N-acetylglucosamine; 10, Glucose-6-phosphate isomerase; 11, Mannose-6-phosphate isomerase; 12, PTS-Man-EIIA, ManX; 13, Phosphoglucomutase; 14, Mannose-1-phosphate guanylyltransferase. b The EPS synthesis gene cluster in strain JH-7T

To gain more insight, the genomic features of strain JH-7T is compared with the available genome P. salicylatoxidans KCT001 [7]. Strain JH-7T has similar genome size (4.84 Mbp) and G + C content (61.2 mol%) compared to strain KCT001 (4.61 Mbp; 62.8 mol%). A total of 2408 core proteins are shared between the two strains. Strain JH-7T has 1724 strain-specific CDSs. Figure 5 shows the genome comparison results of strain JH-7T and strain KCT001 using CGview comparison tool [40]. Comparing to P. salicylatoxidans KCT001, strain JH-7T was unable to utilize tetrathionate for chemolithoautotrophy (data not shown). However, it harbors high quantitative and diverse heavy metal resistance genes.

Fig. 5
figure5

A graphical circular map of the comparison between strain P. manganicus JH-7T and P. salicylatoxidans KCT001. 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 the CDS vs CDS BLAST results of strain JH-7T with strain KCT001; ring 6 shows G + C % content plot and the innermost ring shows GC skew

Conclusions

To the best of our knowledge, this study provides the first typical strain genomic information of the genus Pseudaminobacter and revealed a consistency of important characters between genotypes and phenotypes. Strain JH-7T is resistant to multiple heavy metals and capable of removal Mn2+/Cd2+. Genome analysis reveal various genes responsible for multiple heavy metal resistance, which provides the genomic basis for this strain to adapt the harmful environment.

Abbreviations

EPS:

Exopolysaccharides

MIC:

Minimal inhibition concentration

References

  1. 1.

    Kämpfer P, Müller C, Mau M, Neef A, Auling G, Busse HJ, et al. Description of Pseudaminobacter gen. Nov. with two new species, Pseudaminobacter salicylatoxidans sp. nov. and Pseudaminobacter defluvii sp. nov. Intl J Syst Bacteriol. 1999;149:887–97.

  2. 2.

    Li J, Huang J, Liao S, Wang G. Pseudaminobacter manganicus sp. nov., isolated from sludge of a manganese mine. Int J Syst Evol Microbiol. 2017;67(5):1589–94.

  3. 3.

    Hintner JP, Lechner C, Riegert U, Kuhm AE, Storm T, Reemtsma T, et al. Direct ring fission of salicylate by a salicylate 1,2-dioxygenase activity from Pseudaminobacter salicylatoxidans. J Bacteriol. 2001;183(23):6936–42.

  4. 4.

    Natalia N, Bogino PC, Banchio E, Giordano W. Roles of extracellular polysaccharides and biofilm formation in heavy metal resistance of rhizobia. Materials. 2016;9(6):418.

  5. 5.

    Bhunia B, Prasad Uday US, Oinam G, Mondal A, Bandyopadhyay TK, Tiwari ON. Characterization, genetic regulation and production of cyanobacterial exopolysaccharides and its applicability for heavy metal removal. Carbohydr Polym. 2018;179:228–43.

  6. 6.

    Nouha K, Kumar RS, Tyagi RD. Heavy metals removal from wastewater using extracellular polymeric substances produced by Cloacibacterium normanense in wastewater sludge supplemented with crude glycerol and study of extracellular polymeric substances extraction by different methods. Bioresour Technol. 2016;212:120–9.

  7. 7.

    Alam M, Roy C, Pyne P, Agarwal A, George A, Ghosh W. Whole-genome shotgun sequence of the sulfur-oxidizing chemoautotroph Pseudaminobacter salicylatoxidans KCT001. J Bacteriol. 2012;194(17):4743–4.

  8. 8.

    Deb C, Stackebrandt E, Pradella S, Saha A, Roy P. Phylogenetically diverse new sulfur chemolithotrophs of α-proteobacteria isolated from Indian soils. Curr Microbiol. 2004;48(6):452–8.

  9. 9.

    Nagaraj K, Rekha PD, Arun AB. Exopolysaccharide produced by Enterobacter sp. YG4 reduces uranium induced nephrotoxicity. Int J Biol Macromol. 2016;82:557–61.

  10. 10.

    Altmann F, Kosma P, O’Callaghan A, Leahy S, Bottacini F, Molloy E, et al. Genome analysis and characterisation of the exopolysaccharide produced by Bifidobacterium longum subsp. longum 35624™. PLoS One. 2016;11(9):e0162983.

  11. 11.

    Bennett S. Solexa Ltd. Pharmacogenomics. 2004;5:433–8.

  12. 12.

    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.

  13. 13.

    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.

  14. 14.

    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;29:2607–18.

  15. 15.

    Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 2016;44(1):279–85.

  16. 16.

    Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res. 2004;32:277–80.

  17. 17.

    Li L, Stoeckert CJ Jr, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13(9):2178.

  18. 18.

    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;36(1).

  19. 19.

    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.

  20. 20.

    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.

  21. 21.

    Petersen TN, Brunak S, Von HG, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8(10):785–6.

  22. 22.

    Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007;35:52–7.

  23. 23.

    Kehres DG, Zaharik ML, Finlay BB, Maguire ME. The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol. 2000;36(5):1085–100.

  24. 24.

    Gabbianelli R, Scotti R, Ammendola S, Petrarca P, Nicolini L, Battistoni A. Role of ZnuABC and ZinT in Escherichia coli O157: H7 zinc acquisition and interaction with epithelial cells. BMC Microbiol. 2011;11(1):36.

  25. 25.

    Sharma R, Rensing C, Rosen BP, Mitra B. The ATP hydrolytic activity of purified ZntA, a Pb (II)/cd (II)/Zn (II)-translocating ATPase from Escherichia coli. J Biol Chem. 2000;275(6):3873–8.

  26. 26.

    Nies DH, Silver S. Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol. 1995;14(2):186–99.

  27. 27.

    Xia X, Li J, Liao S, Zhou G, Wang H, Li L, et al. Draft genomic sequence of a chromate-and sulfate-reducing Alishewanella strain with the ability to bioremediate Cr and cd contamination. Stand Genomic Sci. 2016;11(1):48.

  28. 28.

    Xiong J, Li D, Li H, He M, Miller S, Yu L, 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.

  29. 29.

    Adaikkalam V, Swarup S. Characterization of copABCD operon from a copper-sensitive Pseudomonas putida strain. Can J Microbiol. 2005;51(3):209–16.

  30. 30.

    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.

  31. 31.

    Viti C, Marchi E, Decorosi F, Giovannetti L. Molecular mechanisms of Cr (VI) resistance in bacteria and fungi. FEMS Microbiol Rev. 2014;38(4):633–59.

  32. 32.

    Li X, Zhang L, Wang G. Genomic evidence reveals the extreme diversity and wide distribution of the arsenic-related genes in Burkholderiales. PLoS One. 2014;9(3):e92236.

  33. 33.

    Kang YS, Shi Z, Bothner B, Wang G, McDermott TR. Involvement of the Acr3 and DctA anti-porters in arsenite oxidation in Agrobacterium tumefaciens 5A. Environ Microbiol. 2015;17(6):1950–62.

  34. 34.

    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.

  35. 35.

    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.

  36. 36.

    Wu Q, Tun HM, Leung FC, Shah NP. Genomic insights into high exopolysaccharide-producing dairy starter bacterium Streptococcus thermophilus ASCC 1275. Sci Rep. 2014;4:4974.

  37. 37.

    Schmid J, Sieber V, Rehm B. Bacterial exopolysaccharides: biosynthesis pathways and engineering strategies. Front Microbiol. 2015;6:496.

  38. 38.

    Schäffer C, Wugeditsch T, Messner P, Whitfield C. Functional expression of enterobacterial O-polysaccharide biosynthesis enzymes in Bacillus subtilis. Appl Environ Microbiol. 2002;68(10):4722–30.

  39. 39.

    Klena JD, Pradel E, Schnaitman CA. Comparison of lipopolysaccharide biosynthesis genes rfaK, rfaL, rfaY, and rfaZ of Escherichia coli K-12 and Salmonella typhimurium. J Bacteriol. 1992;174(14):4746–52.

  40. 40.

    Grant JR, Arantes AS, Stothard P. Comparing thousands of circular genomes using the CGView comparison tool. BMC Genomics. 2012;13:202.

  41. 41.

    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.

  42. 42.

    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. https://doi.org/10.1038/nbt1360 PMID: 18464787.

  43. 43.

    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.

  44. 44.

    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.

  45. 45.

    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.

  46. 46.

    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 C (the Alpha-, Beta-, Delta-, and Epsilonproteobacteria). New York: Springer; 2005. p. 1.

  47. 47.

    List of new names and new combinations previously effectively, but not validly, published. List no. 106. Int J Syst Evol Microbiol. 2006;56:677.

  48. 48.

    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.

Download references

Funding

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

Author information

XX and JL performed the sequence annotation and genomic analysis and prepared the draft manuscript. ZZ, DW and JH performed the heavy metals resistance and removal tests. GW designed the study and revised the manuscript. All authors read and approved the final manuscript.

Correspondence to Gejiao Wang.

Ethics declarations

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.

Additional file

Additional file 1:

Table S1. Putative heavy metal(loid)s resistance proteins. Table S2. Putative nucleotide sugars biosynthesis proteins for EPS production. Table S3. Putative proteins for EPS production. (XLSX 11 kb)

Rights and permissions

Open Access This 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.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Keywords

  • Cadmium
  • Exopolysaccharides
  • Heavy metal resistance and adsorption
  • Manganese,Pseudaminobacter