Cited by 11Genomics and Phylogenetic StudiesMetal Extraction and BioleachingBacterial Genetics and Biotechnology

Whole Genome Sequence Analysis of Cupriavidus necator C39, a Multiple Heavy Metal(loid) and Antibiotic Resistant Bacterium Isolated from a Gold/Copper Mine

Open access

Abstract

Here a multiple heavy metal and antibiotic resistant bacterium Cupriavidus necator C39 (C. necator C39) was isolated from a Gold-Copper mine in Zijin, Fujian, China. C. necator C39 was able to tolerate intermediate concentrations of heavy metal(loid)s in Tris Minimal (TMM) Medium (Cu(II) 2 mM, Zn(II) 2 mM, Ni(II) 0.2 mM, Au(III) 70 μM and As(III) 2.5 mM). In addition, high resistance to multiple antibiotics was experimentally observed. Moreover, strain C39 was able to grow on TMM medium containing aromatic compounds such as benzoate, phenol, indole, p-hydroxybenzoic acid or phloroglucinol anhydrous as the sole carbon sources. The complete genome of this strain revealed 2 circular chromosomes and 1 plasmid, and showed the closest type strain is C. necator N-1T based on Genome BLAST Distance Phylogeny. The arsenic-resistance (ars) cluster GST-arsR-arsICBR-yciI and a scattered gene encoding the putative arsenite efflux pump ArsB were identified on the genome of strain C39, which thereby may provide the bacterium a robust capability for arsenic resistance. Genes encoding multidrug resistance efflux pump may confer high antibiotic resistance to strain C39. Key genes encoding functions in degradation pathways of benzene compounds, including benzoate, phenol, benzamide, catechol, 3- or 4-fluorobenzoate, 3- or 4-hydroxybenzoate and 3,4-dihydroxybenzoate, indicated its potential for degrading those benzene compounds.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/microorganisms11061518

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Cupriavidus necator exhibits significant resistance to heavy metals and demonstrates enhanced growth in the presence of Cu.

    “An example is Cupriavidus necator, which exhibits significant resistance to heavy metals and demonstrates enhanced growth in the presence of Cu [382].”

    From Harnessing bacterial consortia for effective bioremediation: targeted removal of heavy metals, hydrocarbons, and persistent pollutants (2025) · cites this paper as [382]

    Section 3.1 reports that C. necator strain C39 tolerates several heavy metals, including Cu(II) at 2 mM, though it is less tolerant than the comparison strains. The paper does not report enhanced growth in the presence of Cu: its copper experiments measure tolerance, not improved growth relative to a copper-free condition (Sections 2.3 and 3.1). (LLM, conf=0.88)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 53

  1. [1]Lee S. Khanal A. Cho A.H. Lee H. Kang M.S. Unno T. Hur H.G. Lee J.H. Cupriavidus sp. strain Ni-2 resistant to high concentration of nickel and its genes responsible for the tolerance by genome comparison Arch. Microbiol. 2019 201 1323 1331 10.1007/s00203-019-01700-5 31297579 · DOI
  2. [2]Perez-Pantoja D. De la Lglesia R. Pieper D.H. Gonzalez B. Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134 Fems Microbiol. Rev. 2008 32 736 794 10.1111/j.1574-6976.2008.00122.x 18691224 · DOI
  3. [3]Sohn Y.J. Son J. Jo S.Y. Park S.Y. Yoo J.I. Baritugo K.A. Na J.G. Choi J.I. Kim H.T. Joo J.C. Chemoautotroph Cupriavidus necator as a potential game-changer for global warming and plastic waste problem: A review Bioresour. Technol. 2021 340 e125693 10.1016/j.biortech.2021.125693 34365298 · DOI
  4. [4]Makkar N.S. Casida L.E. Cupriavidus necator gen. nov., sp. nov.; a nonobligate bacterial predator of bacteria in soil Int. J. Syst. Evol. Microbiol. 1987 37 323 326 10.1099/00207713-37-4-323 · DOI
  5. [5]Budde C.F. Mahan A.E. Lu J.N. Rha C. Sinskey A.J. Roles of multiple acetoacetyl coenzyme a reductases in polyhydroxybutyrate biosynthesis in Ralstonia eutropha H16 J. Bacteriol. 2010 192 5319 5328 10.1128/JB.00207-10 20729355 PMC2950492 · DOI
  6. [6]Brigham C.J. Gai C.S. Lu J. Speth D.R. Worden R.M. Sinskey A.J. Engineering Ralstonia eutropha for production of isobutanol from CO2, H2, and O2 Advanced Biofuels and Bioproducts Lee J. Springer New York, NY, USA 2013 Volume 3 1065 1090 10.1007/978-1-4614-3348-4_39 · DOI
  7. [7]Lee H.M. Jeon B.Y. Oh M.K. Microbial production of ethanol from acetate by engineered Ralstonia eutropha Biotechnol. Bioprocess Eng. 2016 21 402 407 10.1007/s12257-016-0197-2 · DOI
  8. [8]Lu J.N. Brigham C.J. Gai C.S. Sinskey A.J. Studies on the production of branched-chain alcohols in engineered Ralstonia eutropha Appl. Microbiol. Biotechnol. 2012 96 283 297 10.1007/s00253-012-4320-9 22864971 · DOI
  9. [9]Grousseau E. Lu J.N. Gorret N. Guillouet S.E. Sinskey A.J. Isopropanol production with engineered Cupriavidus necator as bioproduction platform Appl. Microbiol. Biotechnol. 2014 98 4277 4290 10.1007/s00253-014-5591-0 24604499 · DOI
  10. [10]Muller J. MacEachran D. Burd H. Sathitsuksanoh N. Bi C.H. Yeh Y.C. Lee T.S. Hillson N.J. Chhabra S.R. Singer S.W. Engineering of Ralstonia eutropha H16 for autotrophic and heterotrophic production of methyl ketones Appl. Environ. Microbiol. 2013 79 4433 4439 10.1128/AEM.00973-13 23686271 PMC3697500 · DOI
  11. [11]Przybylski D. Rohwerder T. Dilssner C. Maskow T. Harms H. Muller R.H. Exploiting mixtures of H2, CO2, and O2 for improved production of methacrylate precursor 2-hydroxyisobutyric acid by engineered Cupriavidus necator strains Appl. Microbiol. Biotechnol. 2015 99 2131 2145 10.1007/s00253-014-6266-6 25503317 · DOI
  12. [12]Park J.M. Kim T.Y. Lee S.Y. Genome-scale reconstruction and in silico analysis of the Ralstonia eutropha H16 for polyhydroxyalkanoate synthesis, lithoautotrophic growth, and 2-methyl citric acid production BMC Syst. Biol. 2011 5 101 10.1186/1752-0509-5-101 21711532 PMC3154180 · DOI
  13. [13]Poehlein A. Kusian B. Friedrich B. Daniel R. Bowien B. Complete genome sequence of the type strain Cupriavidus necator N-1 J. Bacteriol. 2011 193 5017 10.1128/JB.05660-11 21742890 PMC3165677 · DOI
  14. [14]Lykidis A. Perez-Pantoja D. Ledger T. Mavromatis K. Anderson I.J. Ivanova N.N. Hooper S.D. Lapidus A. Lucas S. Gonzalez B. The complete multipartite genome sequence of Cupriavidus necator JMP134, a versatile pollutant degrader PLoS ONE 2010 5 e9729 10.1371/journal.pone.0009729 20339589 PMC2842291 · DOI
  15. [15]Xin Y.F. Gao R. Cui F.F. Lu C.J. Liu H.L. Liu H.W. Xia Y.Z. Xun L.Y. The heterotrophic bacterium Cupriavidus pinatubonensis JMP134 oxidizes sulfide to sulfate with thiosulfate as a key intermediate Appl. Environ. Microbiol. 2020 86 e01835-e20 10.1128/AEM.01835-20 32917752 PMC7642071 · DOI
  16. [16]Little G.T. Ehsaan M. Arenas-Lopez C. Jawed K. Winzer K. Kovacs K. Minton N.P. Complete genome sequence of Cupriavidus necator H16 (DSM 428) Microbiol. Resour. Ann. 2019 8 e00814 e00819 10.1128/MRA.00814-19 PMC6742796 31515345 · DOI
  17. [17]Mori J.F. Nagai M. Kanaly R.A. Complete genome sequence of Cupriavidus necator KK10, an azaarene-degrading and polyhydroxyalkanoate-producing soil bacterium Microbiol. Resour. Ann. 2021 10 e0042321 10.1128/MRA.00423-21 PMC8280871 34264105 · DOI
  18. [18]Moriuchi R. Dohra H. Kanesaki Y. Ogawa N. Complete genome sequence of 3-chlorobenzoate-degrading bacterium Cupriavidus necator NH9 and reclassification of the strains of the genera Cupriavidus and Ralstonia based on phylogenetic and whole-genome sequence analyses Front. Microbiol. 2019 10 133 10.3389/fmicb.2019.00133 30809202 PMC6379261 · DOI
  19. [19]Rodriguez-Esperon M.C. Eastman G. Sandes L. Garabato F. Eastman I. Iriarte A. Fabiano E. Sotelo-Silveira J.R. Platero R. Genomics and transcriptomics insights into luteolin effects on the beta-rhizobial strain Cupriavidus necator UYPR2.512 Environ. Microbiol. 2022 24 240 264 10.1111/1462-2920.15845 34811861 · DOI
  20. [20]Yonezuka K. Shimodaira J. Tabata M. Nagase S. Kasai D. Hosoyama A. Yamazoe A. Fujita N. Fukuda M. Draft genome sequence of a chlorinated-ethene degrader, Cupriavidus necator strain PHE3-6 (NBRC 110655) Genome Announc. 2016 4 e01743-e15 10.1128/genomeA.01743-15 26941158 PMC4777769 · DOI
  21. [21]Margaryan A. Diversity and application of heavy-metal resistant microbes Microbes in Microbial Communities Singh R.P. Manchanda G. Bhattacharjee K. Panosyan H. Springer Singapore 2021 153 174 10.1007/978-981-16-5617-0_7 · DOI
  22. [22]Cai X. Zheng X. Zhang D. Iqbal W. Liu C. Yang B. Zhao X. Lu X. Mao Y. Microbial characterization of heavy metal resistant bacterial strains isolated from an electroplating wastewater treatment plant Ecotoxicol. Environ. Saf. 2019 181 472 480 10.1016/j.ecoenv.2019.06.036 31228823 · DOI · Paper page
  23. [23]Tuffin I.M. Hector S.B. Deane S.M. Rawlings D.E. Resistance determinants of a highly arsenic-resistant strain of Leptospirillum ferriphilum isolated from a commercial biooxidation tank Appl. Environ. Microbiol. 2006 72 2247 2253 10.1128/AEM.72.3.2247-2253.2006 16517682 PMC1393207 · DOI
  24. [24]Fashola M.O. Ngole-Jeme V.M. Babalola O.O. Heavy metal pollution from gold mines: Environmental effects and bacterial strategies for resistance Int. J. Environ. Res. Public Health 2016 13 1047 10.3390/ijerph13111047 27792205 PMC5129257 · DOI
  25. [25]Mergeay M. Nies D. Schlegel H.G. Gerits J. Charles P. Van Gijsegem F. Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals J. Bacteriol. 1985 162 328 334 10.1128/jb.162.1.328-334.1985 3884593 PMC218993 · DOI
  26. [26]Tatusova T. DiCuccio M. Badretdin A. Chetvernin V. Nawrocki E.P. Zaslavsky L. Lomsadze A. Pruitt K.D. Borodovsky M. Ostell J. NCBI prokaryotic genome annotation pipeline Nucleic Acids Res. 2016 44 6614 6624 10.1093/nar/gkw569 27342282 PMC5001611 · DOI
  27. [27]Cantarel B.L. Coutinho P.M. Rancurel C. Bernard T. Lombard V. Henrissat B. The carbohydrate-active enzymes database (CAZy): An expert resource for glycogenomics Nucleic Acids Res. 2009 37 D233 D238 10.1093/nar/gkn663 18838391 PMC2686590 · DOI
  28. [28]Galperin M.Y. Makarova K.S. Wolf Y.I. Koonin E.V. Expanded microbial genome coverage and improved protein family annotation in the COG database Nucleic Acids Res. 2015 43 D261 D269 10.1093/nar/gku1223 25428365 PMC4383993 · DOI
  29. [29]Moriya Y. Itoh M. Okuda S. Yoshizawa A.C. Kanehisa M. KAAS: An automatic genome annotation and pathway reconstruction server Nucleic Acids Res. 2007 35 W182 W185 10.1093/nar/gkm321 17526522 PMC1933193 · DOI
  30. [30]Delcher A.L. Harmon D. Kasif S. White O. Salzberg S.L. Improved microbial gene identification with GLIMMER Nucleic Acids Res. 1999 27 4636 4641 10.1093/nar/27.23.4636 10556321 PMC148753 · DOI
  31. [31]Overbeek R. Olson R. Pusch G.D. Olsen G.J. Davis J.J. Disz T. Edwards R.A. Gerdes S. Parrello B. Shukla M. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST) Nucleic Acids Res. 2014 42 D206 D214 10.1093/nar/gkt1226 24293654 PMC3965101 · DOI
  32. [32]Stothard P. Wishart D.S. Circular genome visualization and exploration using CGView Bioinformatics 2005 21 537 539 10.1093/bioinformatics/bti054 15479716 · DOI
  33. [33]Altschul S.F. Madden T.L. Schaffer A.A. Zhang J. Zhang Z. Miller W. Lipman D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res. 1997 25 3389 3402 10.1093/nar/25.17.3389 9254694 PMC146917 · DOI · Paper page
  34. [34]Madeira F. Park Y.M. Lee J. Buso N. Gur T. Madhusoodanan N. Basutkar P. Tivey A.R.N. Potter S.C. Finn R.D. The EMBL-EBI search and sequence analysis tools APIs in 2019 Nucleic Acids Res. 2019 47 W636 W641 10.1093/nar/gkz268 30976793 PMC6602479 · DOI · Paper page
  35. [35]Meier-Kolthoff J.P. Goker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy Nat. Commun. 2019 10 2182 10.1038/s41467-019-10210-3 31097708 PMC6522516 · DOI
  36. [36]Ondov B.D. Treangen T.J. Melsted P. Mallonee A.B. Bergman N.H. Koren S. Phillippy A.M. Mash: Fast genome and metagenome distance estimation using MinHash Genome Biol. 2016 17 132 10.1186/s13059-016-0997-x 27323842 PMC4915045 · DOI · Paper page
  37. [37]Lagesen K. Hallin P. Rodland E.A. Staerfeldt H.H. Rognes T. Ussery D.W. RNAmmer: Consistent and rapid annotation of ribosomal RNA genes Nucleic Acids Res. 2007 35 3100 3108 10.1093/nar/gkm160 17452365 PMC1888812 · DOI
  38. [38]Camacho C. Coulouris G. Avagyan V. Ma N. Papadopoulos J. Bealer K. Madden T.L. BLAST plus: Architecture and applications BMC Bioinform. 2009 10 421 10.1186/1471-2105-10-421 PMC2803857 20003500 · DOI · Paper page
  39. [39]Meier-Kolthoff J.P. Auch A.F. Klenk H.P. Goker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions BMC Bioinform. 2013 14 60 10.1186/1471-2105-14-60 23432962 PMC3665452 · DOI
  40. [40]Richter M. Rossello-Mora R. Glockner F.O. Peplies J. JSpeciesWS: A web server for prokaryotic species circumscription based on pairwise genome comparison Bioinformatics 2016 32 929 931 10.1093/bioinformatics/btv681 26576653 PMC5939971 · DOI
  41. [41]Livak K.J. Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method Methods 2001 25 402 408 10.1006/meth.2001.1262 11846609 · DOI · Paper page
  42. [42]Mazhar S.H. Herzberg M. Ben Fekih I. Zhang C.K. Bello S.K. Li Y.P. Su J.M. Xu J.Q. Feng R.W. Zhou S.G. Comparative insights into the complete genome sequence of highly metal resistant Cupriavidus metallidurans strain BS1 isolated from a gold-copper mine Front. Microbiol. 2020 11 47 10.3389/fmicb.2020.00047 32117100 PMC7019866 · DOI
  43. [43]Amadou C. Pascal G. Mangenot S. Glew M. Bontemps C. Capela D. Carrere S. Cruveiller S. Dossat C. Lajus A. Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia Genome Res. 2008 18 1472 1483 10.1101/gr.076448.108 18490699 PMC2527706 · DOI
  44. [44]Janssen P.J. Van Houdt R. Moors H. Monsieurs P. Morin N. Michaux A. Benotmane M.A. Leys N. Vallaeys T. Lapidus A. The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments PLoS ONE 2010 5 e10433 10.1371/journal.pone.0010433 20463976 PMC2864759 · DOI
  45. [45]Wang X. Chen M. Xiao J. Hao L. Crowley D.E. Zhang Z. Yu J. Huang N. Huo M. Wu J. Genome sequence analysis of the naphthenic acid degrading and metal resistant bacterium Cupriavidus gilardii CR3 PLoS ONE 2015 10 e0132881 10.1371/journal.pone.0132881 26301592 PMC4547698 · DOI
  46. [46]Feng T. Kim K.H. Oh J. Jeon C.O. Cupriavidus lacunae sp. nov., isolated from pond-side soil Antonie Van Leeuwenhoek 2019 112 543 551 10.1007/s10482-018-1187-5 30317454 · DOI
  47. [47]Abbaszade G. Szabo A. Vajna B. Farkas R. Szabo C. Toth E. Whole genome sequence analysis of Cupriavidus campinensis S14E4C, a heavy metal resistant bacterium Mol. Biol. Rep. 2020 47 3973 3985 10.1007/s11033-020-05490-8 32406019 PMC7239810 · DOI
  48. [48]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 e92236 10.1371/journal.pone.0092236 24632831 PMC3954881 · DOI
  49. [49]Khan A.A. Ellis D.R. Huang X. Norton G.J. Meharg A.A. Salt D.E. Csonka L.N. Glutathione-S-transferase from the arsenic hyperaccumulator fern Pteris vittata can confer increased arsenate resistance in Escherichia coli bioRxiv 2018 10.1101/379511 · DOI
  50. [50]Lopez-Maury L. Sanchez-Riego A.M. Reyes J.C. Florencio F.J. The glutathione/glutaredoxin system is essential for arsenate reduction in Synechocystis sp. strain PCC 6803 J. Bacteriol. 2009 191 3534 3543 10.1128/JB.01798-08 19304854 PMC2681892 · DOI
  51. [51]Hayes R.P. Lewis K.M. Xun L. Kang C. Catalytic mechanism of 5-chlorohydroxyhydroquinone dehydrochlorinase from the YCII superfamily of largely unknown function J. Biol. Chem. 2013 288 28447 28456 10.1074/jbc.M113.499368 23955343 PMC3789946 · DOI
  52. [52]Willis M.A. Song F. Zhuang Z. Krajewski W. Chalamasetty V.R. Reddy P. Howard A. Dunaway-Mariano D. Herzberg O. Structure of YciI from Haemophilus influenzae (HI0828) reveals a ferredoxin-like alpha/beta-fold with a histidine/aspartate centered catalytic site Proteins 2005 59 648 652 10.1002/prot.20411 15779043 · DOI
  53. [53]Baker-Austin C. Wright M.S. Stepanauskas R. McArthur J.V. Co-selection of antibiotic and metal resistance Trends Microbiol. 2006 14 176 182 10.1016/j.tim.2006.02.006 16537105 · DOI

Authors
Xie, Z., Wang, D., Ben Fekih, I., Yu, Y., Li, Y., Alwathnani, H., Herzberg, M., & Rensing, C.
Affiliations
  • Fujian Agriculture and Forestry University (CN)
  • Shenzhen University (CN)
  • Institute of Environmental Microbiology, College of Resource and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China
  • King Saud University (SA)
  • Martin Luther University Halle-Wittenberg (DE)
Corresponding author
Rensing, Christopher
Venue
Microorganisms
Publisher
MDPI AG
Published
2023-06-07
Volume
11
Issue
6
Pages
1518
ISSN
2076-2607 (ISSN-L)
OpenAlex
W4380051606
Cited by
11
References
0
Citations by year
2026: 4 · 2025: 4 · 2024: 2 · 2023: 1
FWCI
0.95
Type
journal article
Language
en
Open access
Locations
  • Microorganisms (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Open Repository and Bibliography (University of Liège) (submittedVersion, other-oa)
  • Digitalen Hochschulbibliothek Sachsen-Anhalt (Universitäts- und Landesbibliothek Sachsen-Anhalt) (cc-by)
Funders
  • NSFC (31770123, 2018J01668, RSP-2023/205)
  • Natural Science Foundation of Fujian province (31770123, 2018J01668, RSP-2023/205)
  • King Saud University (31770123, 2018J01668, RSP-2023/205)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Physical Sciences › Engineering › Biomedical Engineering › Metal Extraction and Bioleaching
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
heavy metal resistance, antibiotic resistance, arsenic resistance, multidrug efflux pumps, aromatic compound degradation, benzoate degradation, bacterial genomes, plasmids

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review