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Assessing nickel tolerance of bacteria isolated from serpentine soils

  • Environmental Microbiology - Research Paper
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Abstract

Serpentine soils present unique characteristics such as a low Ca/Mg ratio, low concentration of nutrients, and a high concentration of heavy metals, especially nickel. Soil bacterial isolates from an ultramafic complex located in the tropical savanna known as the Brazilian Cerrado were studied. Nickel-tolerant bacteria were obtained, and their ability to remove nickel from a culture medium was assessed. Bacterial isolates presented higher tolerance to nickel salts than previously reported for bacteria obtained from serpentine environments in other regions of the world. In addition, the quantification of nickel in cell pellets indicated that at least four isolates may adsorb soluble forms of nickel. It is expected that information gathered in this study will support future efforts to exploit serpentine soil bacteria for biotechnological processes involving nickel decontamination from environmental samples.

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References

  1. Raous S, Becquer T, Garnier J, de Souza Martins É, Echevarria G, Sterckeman T (2010) Mobility of metals in nickel mine spoil materials. Appl Geochem 25(11):1746–1755

    Article  CAS  Google Scholar 

  2. Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG (2007) The flora and biogeochemistry of the ultramafic soils of Goiás state, Brazil. Plant Soil 293(1–2):107–119

    Article  CAS  Google Scholar 

  3. Rajakaruna N (2018) Lessons on evolution from the study of edaphic specialization. Bot Rev 84(1):39–78

    Article  Google Scholar 

  4. Venter A, Siebert S, Rajakaruna N et al (2018) Biological crusts of serpentine and non-serpentine soils from the Barberton Greenstone Belt of South Africa. Ecol Res: 33(3): 629-640. 

  5. Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38(9):2882–2889

    Article  CAS  Google Scholar 

  6. Abou-Shanab RI, Delorme TA, Angle JS, Chaney RL, Ghanem K, Moawad H, Ghozlan HA (2003) Phenotypic characterization of microbes in the rhizosphere of Alyssum murale. Int J Phytoremediation 5(4):367–379

    Article  CAS  Google Scholar 

  7. Ma Y, Rajkumar M, Freitas H (2009) Improvement of plant growth and nickel uptake by nickel resistant-plant-growth promoting bacteria. J Hazard Mater 166(2–3):1154–1161

    Article  CAS  Google Scholar 

  8. Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere. 77(2):153–160

    Article  CAS  Google Scholar 

  9. Mengoni A, Schat H, Vangronsveld J (2010) Plants as extreme environments? Ni-resistant bacteria and Ni-hyperaccumulators of serpentine flora. Plant Soil 331(1–2):5–16

    Article  CAS  Google Scholar 

  10. Oline DK (2006) Phylogenetic comparisons of bacterial communities from serpentine and nonserpentine soils. Appl Environ Microbiol 72(11):6965–6971

    Article  CAS  Google Scholar 

  11. Pessoa-Filho M, Barreto CC, dos Reis Junior FB, Fragoso RR, Costa FS, de Carvalho Mendes I, de Andrade LRM (2015) Microbiological functioning, diversity, and structure of bacterial communities in ultramafic soils from a tropical savanna. Antonie Van Leeuwenhoek 107(4):935–949. https://doi.org/10.1007/s10482-015-0386-6

    Article  CAS  PubMed  Google Scholar 

  12. Abou-Shanab RAI, van Berkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere. 68(2):360–367. https://doi.org/10.1016/J.CHEMOSPHERE.2006.12.051

    Article  CAS  PubMed  Google Scholar 

  13. Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70(5):2667–2677

    Article  CAS  Google Scholar 

  14. Mengoni A, Barzanti R, Gonnelli C, Gabbrielli R, Bazzicalupo M (2001) Characterization of nickel-resistant bacteria isolated from serpentine soil. Environ Microbiol 3(11):691–698

    Article  CAS  Google Scholar 

  15. Schlegel HG, Cosson J, Baker AJM (1991) Nickel-hyperaccumulating plants provide a niche for nickel-resistant bacteria. Bot acta 104(1):18–25

    Article  CAS  Google Scholar 

  16. Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45(3):198–207

    Article  CAS  Google Scholar 

  17. Fashola M, Ngole-Jeme V, Babalola O (2016) Heavy metal pollution from gold mines: environmental effects and bacterial strategies for resistance. Int J Environ Res Public Health 13(11):1047

    Article  Google Scholar 

  18. Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. J Basic Microbiol 47(6):453–467

    Article  CAS  Google Scholar 

  19. Malkoc S, Kaynak E, Guven K (2016) Biosorption of zinc (II) on dead and living biomass of Variovorax paradoxus and Arthrobacter viscosus. Desalin Water Treat 57(33):15445–15454

    Article  CAS  Google Scholar 

  20. Ahmed MMA, El-Bondkly AMA (2016) Evaluation and enhancement of heavy metals bioremediation in aqueous solutions by Nocardiopsis sp. MORSY1948, and Nocardia sp. MORSY2014. Braz J Microbiol 47(3):571

    Article  Google Scholar 

  21. Pollmann K, Raff J, Merroun M, Fahmy K, Selenska-Pobell S (2006) Metal binding by bacteria from uranium mining waste piles and its technological applications. Biotechnol Adv 24(1):58–68

    Article  CAS  Google Scholar 

  22. Li H, Lin Y, Guan W, Chang J, Xu L, Guo J, Wei G (2010) Biosorption of Zn (II) by live and dead cells of Streptomyces ciscaucasicus strain CCNWHX 72-14. J Hazard Mater 179(1–3):151–159

    CAS  PubMed  Google Scholar 

  23. Polti MA, Aparicio JD, Benimeli CS, Amoroso MJ (2014) Simultaneous bioremediation of Cr (VI) and lindane in soil by actinobacteria. Int Biodeterior Biodegradation 88:48–55

    Article  CAS  Google Scholar 

  24. Tabaraki R, Ahmady-Asbchin S, Abdi O (2013) Biosorption of Zn (II) from aqueous solutions by Acinetobacter sp. isolated from petroleum spilled soil. J Environ Chem Eng 1(3):604–608

    Article  CAS  Google Scholar 

  25. Johnson DB, Grail BM, Hallberg KB (2013) A new direction for biomining: extraction of metals by reductive dissolution of oxidized ores. Minerals. 3(1):49–58

    Article  CAS  Google Scholar 

  26. Reasoner DJ, Geldreich EE (1985) A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 49(1):1–7

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Joseph SJ, Hugenholtz P, Sangwan P, Osborne CA, Janssen PH (2003) Laboratory cultivation of widespread and previously uncultured soil bacteria. Appl Environ Microbiol 69(12):7210–7215. https://doi.org/10.1128/AEM.69.12.7210-7215.2003

  28. Kielak AMAM, Barreto CCCC, Kowalchuk GAGA, van Veen JAJA, Kuramae EEEE (2016) The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 7(MAY). https://doi.org/10.3389/fmicb.2016.00744

  29. de Castro VHL, Schroeder LF, Quirino BF, Kruger RH, Barreto CC (2013) Acidobacteria from oligotrophic soil from the Cerrado can grow in a wide range of carbon source concentrations. Can J Microbiol 59(11):746–753. https://doi.org/10.1139/cjm-2013-0331

    Article  CAS  PubMed  Google Scholar 

  30. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor, N.Y.: Cold Spring Harbor laboratory press

  31. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt, E. and Goodfellow, M., Eds., Nucleic Acid Techniques in Bacterial Systematic, John Wiley and Sons, New York, 115-175

  32. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  33. Cole JR, Wang Q, Cardenas E et al (2008) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37(suppl_1):D141–D145

    PubMed  PubMed Central  Google Scholar 

  34. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

    Article  CAS  Google Scholar 

  35. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    Article  CAS  Google Scholar 

  36. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526

    CAS  PubMed  Google Scholar 

  37. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution (N Y) 39(4):783–791

    Google Scholar 

  38. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci 101(30):11030–11035

    Article  CAS  Google Scholar 

  39. McNaught, A. D., & Wilkinson, A. (1997). Compendium of chemical terminology. IUPAC recommendations.

  40. Mergeay M (1995) Heavy metal resistances in microbial ecosystems. In: Molecular Microbial Ecology Manual (pp. 439-455). Springer, Dordrecht.

  41. Thomsen V, Schatzlein D, Mercuro D (2003) Limits of detection in spectroscopy. Spectroscopy. 18(12):112–114

    CAS  Google Scholar 

  42. Pal A, Wauters G, Paul AK (2007) Nickel tolerance and accumulation by bacteria from rhizosphere of nickel hyperaccumulators in serpentine soil ecosystem of Andaman, India. Plant Soil 293(1–2):37–48

    Article  CAS  Google Scholar 

  43. Abou-Shanab RAI, Van Berkum P, Angle JS et al (2010) Characterization of Ni-resistant bacteria in the rhizosphere of the hyperaccumulator Alyssum murale by 16S rRNA gene sequence analysis. World J Microbiol Biotechnol 26(1):101–108

    Article  CAS  Google Scholar 

  44. Turgay OC, Görmez A, Bilen S (2012) Isolation and characterization of metal resistant-tolerant rhizosphere bacteria from the serpentine soils in Turkey. Environ Monit Assess 184(1):515–526

    Article  CAS  Google Scholar 

  45. Saintpierre D, Amir H, Pineau R, Sembiring L, Goodfellow M (2003) Streptomyces yatensis sp. nov., a novel bioactive streptomycete isolated from a New-Caledonian ultramafic soil. Antonie Van Leeuwenhoek 83(1):21–26

    Article  CAS  Google Scholar 

  46. Saintpierre-Bonaccio D, Amir H, Pineau R, Lemriss S, Goodfellow M (2004) Streptomyces ferralitis sp. nov., a novel streptomycete isolated from a New-Caledonian ultramafic soil. Int J Syst Evol Microbiol 54(6):2061–2065

    Article  Google Scholar 

  47. Saintpierre-Bonaccio D, Amir H, Pineau R, Tan GYA, Goodfellow M (2005) Amycolatopsis plumensis sp. nov., a novel bioactive actinomycete isolated from a New-Caledonian brown hypermagnesian ultramafic soil. Int J Syst Evol Microbiol 55(5):2057–2061

    Article  CAS  Google Scholar 

  48. Saintpierre-Bonaccio D, Maldonado LA, Amir H, Pineau R, Goodfellow M (2004) Nocardia neocaledoniensis sp. nov., a novel actinomycete isolated from a New-Caledonian brown hypermagnesian ultramafic soil. Int J Syst Evol Microbiol 54(2):599–603

    Article  CAS  Google Scholar 

  49. Rajkumar M, Freitas H (2008) Effects of inoculation of plant-growth promoting bacteria on Ni uptake by Indian mustard. Bioresour Technol 99(9):3491–3498

    Article  CAS  Google Scholar 

  50. Ma Y, Rajkumar M, Freitas H (2009) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere. 75(6):719–725

    Article  CAS  Google Scholar 

  51. Barzanti R, Ozino F, Bazzicalupo M, Gabbrielli R, Galardi F, Gonnelli C, Mengoni A (2007) Isolation and characterization of endophytic bacteria from the nickel hyperaccumulator plant Alyssum bertolonii. Microb Ecol 53(2):306–316

    Article  CAS  Google Scholar 

  52. Pal A, Choudhuri P, Dutta S, Mukherjee PK, Paul AK (2004) Isolation and characterization of nickel-resistant microflora from serpentine soils of Andaman. World J Microbiol Biotechnol 20(9):881–886

    Article  CAS  Google Scholar 

  53. Dopson M, Baker-Austin C, Koppineedi PR, Bond PL (2003) Growth in sulfidic mineral environments: metal resistance mechanisms in acidophilic micro-organisms. Microbiology. 149(8):1959–1970

    Article  CAS  Google Scholar 

  54. Chaintreuil C, Rigault F, Moulin L, Jaffre T, Fardoux J, Giraud E, Dreyfus B, Bailly X (2007) Nickel resistance determinants in Bradyrhizobium strains from nodules of the endemic New Caledonia legume Serianthes calycina. Appl Environ Microbiol 73(24):8018–8022

    Article  CAS  Google Scholar 

  55. Kim DW, Cha DK, Wang J, Huang CP (2002) Heavy metal removal by activated sludge: influence of Nocardia amarae. Chemosphere. 46(1):137–142

    Article  CAS  Google Scholar 

  56. Schmidt A, Haferburg G, Schmidt A, Lischke U, Merten D, Ghergel F, Büchel G, Kothe E (2009) Heavy metal resistance to the extreme: Streptomyces strains from a former uranium mining area. Chem Erde-Geochem 69:35–44

    Article  CAS  Google Scholar 

  57. Nosanchuk JD, Casadevall A (2003) The contribution of melanin to microbial pathogenesis. Cell Microbiol 5(4):203–223

    Article  CAS  Google Scholar 

  58. Coisne S, Bechet M, Blondeau R (1999) Actinorhodin production by Streptomyces coelicolor A3 (2) in iron-restricted media. Lett Appl Microbiol 28(3):199–202

    Article  CAS  Google Scholar 

  59. Grafe U, Radics L (1986) Isolation and structure elucidation of 6-(3′-methylbuten-2′-yl) isatin, an unusual metabolite from Streptomyces albus. J Antibiot (Tokyo) 39(1):162–163

    Article  CAS  Google Scholar 

  60. Pankratov TA, Tindall BJ, Liesack W, Dedysh SN (2007) 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 57(10):2349–2354. https://doi.org/10.1099/ijs.0.65100-0

    Article  CAS  PubMed  Google Scholar 

  61. Scott JA, Palmer SJ (1988) Cadmium bio-sorption by bacterial exopolysaccharide. Biotechnol Lett 10(1):21–24

    Article  CAS  Google Scholar 

  62. Vu B, Chen M, Crawford R, Ivanova E (2009) Bacterial extracellular polysaccharides involved in biofilm formation. Molecules. 14(7):2535–2554

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Anglo American and their team at the Barro Alto plant for their support.

Funding

This work was supported by FAP-DF, the Federal District Research Foundation (Grant 193.000.197/2014); CNPq, the National Council for Scientific and Technological Development, Brazil (Grant 830009/2003-5); EMBRAPA Macroprograma 3 (Grant 03.09.06.016.00.00); and CAPES, Coordination for the Improvement of Higher Education Personnel, Brazil (Grant 8881.062152/2014-1). Publication number 6641 of The Netherlands Institute of Ecology (NIOO-KNAW).

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Correspondence to Cristine Chaves Barreto.

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Figure S1

Schematic representation of the experimental design. (PNG 122 kb)

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Figure S2

Phylogenetic tree based on 16S rRNA gene sequences of thirteen elected isolates that were evaluated for nickel tolerance. The evolutionary history was inferred using the Maximum-likelihood method. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) are shown next to the branches. The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. (PDF 74 kb)

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Costa, F.S., Macedo, M.W.F.S., Araújo, A.C.M. et al. Assessing nickel tolerance of bacteria isolated from serpentine soils. Braz J Microbiol 50, 705–713 (2019). https://doi.org/10.1007/s42770-019-00111-4

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