Export file:


  • RIS(for EndNote,Reference Manager,ProCite)
  • BibTex
  • Text


  • Citation Only
  • Citation and Abstract

Manganese-II oxidation and Copper-II resistance in endospore forming Firmicutes isolated from uncontaminated environmental sites

1 Laboratory of Microbiology, Institute of Biology, University of Neuchâtel, Emile-Argand 11, CH-2000 Neuchâtel, Switzerland
2 Vital-IT group, Swiss Institute of Bioinformatics, CH-1000 Lausanne, Switzerland
3 Laboratorio de Complejidad Microbiana y Ecología Funcional; Departamento de Biotecnología; Facultad de Ciencias del Mar y Recursos Biológicos, Universidad de Antofagasta; CL-, 1270190, Antofagasta, Chile

Special Issues: Metal Contamination in the Environment

The accumulation of metals in natural environments is a growing concern of modern societies since they constitute persistent, non-degradable contaminants. Microorganisms are involved in redox processes and participate to the biogeochemical cycling of metals. Some endospore-forming Firmicutes (EFF) are known to oxidize and reduce specific metals and have been isolated from metal-contaminated sites. However, whether EFF isolated from uncontaminated sites have the same capabilities has not been thoroughly studied. In this study, we measured manganese oxidation and copper resistance of aerobic EFF from uncontaminated sites. For the purposes of this study we have sampled 22 natural habitats and isolated 109 EFF strains. Manganese oxidation and copper resistance were evaluated by growth tests as well as by molecular biology. Overall, manganese oxidation and tolerance to over 2 mM copper was widespread among the isolates (more than 44% of the isolates exhibited Mn (II)-oxidizing activity through visible Birnessite formation and 9.1% tolerate over 2 mM copper). The co-occurrence of these properties in the isolates was also studied. Manganese oxidation and tolerance to copper were not consistently found among phylogenetically related isolates. Additional analysis correlating the physicochemical parameters measured on the sampling sites and the metabolic capabilities of the isolates showed a positive correlation between in situ alkaline conditions and the ability of the strains to perform manganese oxidation. Likewise, a negative correlation between temperature in the habitat and copper tolerance of the strains was observed. Our results lead to the conclusion that metal tolerance is a wide spread phenomenon in unrelated aerobic EFF from natural uncontaminated environments.
  Article Metrics


1. Fu F, Wang Q (2011) Removal of heavy metal ions from wastewaters: A review. J Environ Manage 92: 407-418.    

2. Simsek I, Karatas M, Basturk E (2013) Cu (II) removal from aqueous solution by ureolytic mixed culture (UMC). Colloid Surf B 102: 479-483.

3. Zouboulis A, Loukidou M, Matis K (2004) Biosorption of toxic metals from aqueous solutions by bacteria strains isolated from metal-polluted soils. Process Biochem 39: 909-916.    

4. Berg JM, Tymoczko JL, Stryer L, et al. (2002) Biochemistry, 5th ed. W H Freeman.

5. Gadd GM, Griffiths AJ (1977) Microorganisms and heavy metal toxicity. Microb Ecol 4: 303-317.    

6. Ghosh A, Saha PD (2013) Optimization of copper bioremediation by Stenotrophomonas maltophilia PD2. J Environ Chem Eng 1: 159-163.    

7. Pradhan AA, Levine AD (1995) Microbial biosorption of copper and lead from aqueous systems. Sci Total Environ 170: 209-220.    

8. Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27: 195-226.    

9. Zhou W, Zhang H, Ma Y, et al. (2013) Bio-removal of cadmium by growing deep-sea bacterium Pseudoalteromonas sp. SCSE709-6. Extremophiles 17: 723-731.    

10. Tebo BM, Johnson HA, McCarthy JK, et al. (2005) Geomicrobiology of manganese (II) oxidation. Trends Microbiol 13: 421-428.    

11. Dick GJ, Torpey JW, Beveridge TJ, et al. (2008) Direct identification of a bacterial manganese(ii) oxidase, the multicopper oxidase MnxG, from spores of several different marine Bacillus species. Appl Environ Microbiol 74: 1527-1534.    

12. Waasbergen LG van, Hildebrand M, Tebo BM (1996) Identification and characterization of a gene cluster involved in manganese oxidation by spores of the marine Bacillus sp. strain SG-1. J Bacteriol 178: 3517-3530.

13. Rensing C, Grass G (2003) Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol Rev 27: 197-213    

14. Taylor AB, Stoj CS, Ziegler L, et al. (2005) The copper-iron connection in biology: Structure of the metallo-oxidase Fet3p. Proc Natl Acad Sci 102: 15459-15464.    

15. Altimira F, Yáñez C, Bravo G, et al. (2012) Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol 12: 193.    

16. Andreazza R, Pieniz S, Wolf L, et al. (2010) Characterization of copper bioreduction and biosorption by a highly copper resistant bacterium isolated from copper-contaminated vineyard soil. Sci Total Environ 408: 1501-1507.    

17. Chen G, Chen X, Yang Y, et al. (2011) Sorption and distribution of copper in unsaturated Pseudomonas putida CZ1 biofilms as determined by X-Ray fluorescence microscopy. Appl Environ Microbiol 77: 4719-4727.    

18. Fan LM, Ma ZQ, Liang JQ, et al. (2011) Characterization of a copper-resistant symbiotic bacterium isolated from Medicago lupulina growing in mine tailings. Bioresour Technol 102: 703-709.    

19. Besaury L, Bodilis J, Delgas F, et al. (2013) Abundance and diversity of copper resistance genes cusA and copA in microbial communities in relation to the impact of copper on Chilean marine sediments. Mar Pollut Bull 67: 16-25.    

20. Bueche M, Wunderlin T, Roussel-Delif L, et al. (2013) Quantification of endospore-forming firmicutes by quantitative PCR with the functional gene spo0A. Appl Environ Microbiol 79: 5302-5312.    

21. Vreeland RH, Rosenzweig WD, Powers DW (2000) Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal. Nature 407: 897-900    

22. Francis CA, Tebo BM (2002) Enzymatic Manganese(II) oxidation by metabolically dormant spores of diverse Bacillus species. Appl Environ Microbiol 68: 874-880.    

23. Nealson KH, Myers CR (1992) Microbial reduction of manganese and iron: new approaches to carbon cycling. Appl Environ Microbiol 58: 439-443.

24. Junier P, Frutschi M, Wigginton NS, et al. (2009) Metal reduction by spores of Desulfotomaculum reducens. Environ Microbiol 11: 3007-3017.    

25. Logan NA, Berge O, Bishop AH, et al (2009) Proposed minimal standards for describing new taxa of aerobic, endospore-forming bacteria. Int J Syst Evol Microbiol 59: 2114-2121.    

26. Liesack W, Weyland H, Stackebrandt E (1991) Potential risks of gene amplification by PCR as determined by 16S rDNA analysis of a mixed-culture of strict barophilic bacteria. Microb Ecol 21: 191-198.    

27. Muyzer G, Teske A, Wirsen C, et al. (1995) Phylogenetic-relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel-electrophoresis of 16S rDNA fragments. Arch Microbiol 164: 165-172.    

28. Wunderlin T, Junier T, Roussel-Delif L, et al. (2013) Stage 0 sporulation gene A as a molecular marker to study diversity of endospore-forming Firmicutes. Environ Microbiol Rep 5: 911-924.    

29. Ovreas L, Forney L, Daae FL, et al. (1997) Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol 63: 3367-3373.

30. Kim OS, Cho YJ, Lee K, et al (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62: 716-721.    

31. Pena J, Kwon KD, Refson K, et al. (2010) Mechanisms of nickel sorption by a bacteriogenic birnessite. Geochim Cosmochim Acta 74: 3076-3089.    

32. Ahmed N, Nawaz A, Badar U (2005) Screening of copper tolerant bacterial strains and their potential to remove copper from the environment. Bull Environ Contam Toxicol 74: 219-226.    

33. Katoh K, Misawa K, Kuma K, et al. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.    

34. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30: 772-780.    

35. Guindon S, Dufayard J-F, Lefort V, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321.    

36. Junier T, Zdobnov EM (2010) The Newick utilities: high-throughput phylogenetic tree processing in the Unix shell. Bioinformatics: btq243.

37. Tebo BM, Bargar JR, Clement BG, et al. (2004) Biogenic manganese oxides: properties and mechanisms of formation. Annu Rev Earth Planet Sci 32: 287-328.    

38. Villalobos M, Bargar J, Sposito G (2005) Trace metal retention on biogenic manganese oxide nanoparticles. Elements 1: 223-226.    

39. Johnson K, Purvis G, Lopez-Capel E, et al (2015) Towards a mechanistic understanding of carbon stabilization in manganese oxides. Nat Commun 6: 7628.    

40. Geszvain K, Butterfield C, Davis RE, et al. (2012) The molecular biogeochemistry of manganese(II) oxidation. Biochem Soc Trans 40: 1244-1248.    

41. Soldatova AV, Butterfield C, Oyerinde OF, et al. (2012) Multicopper oxidase involvement in both Mn (II) and Mn(III) oxidation during bacterial formation of MnO2. J Biol Inorg Chem 17: 1151-1158    

42. Sravani M, Sridevi V, Vijay kumar K, et al. (2012) A comparative study on determination of physicochemical parameters of biosorption of lead (II) by Aspergillus niger NCIM 616 using AAS & ICPMS. IOSR J Pharm IOSRPHR 2: 60-64.

43. Babarinde A, Babalola JO, Adegoke J, et al. (2012) Biosorption of Ni(II), Cr(III), and Co(II) from solutions using acalypha hispida leaf: kinetics, equilibrium, and thermodynamics. J Chem 2013: e460635.

44. Komy ZR, Abdelraheem WH, Ismail NM (2013) Biosorption of Cu2+ by Eichhornia crassipes: Physicochemical characterization, biosorption modeling and mechanism. J King Saud Univ Sci 25: 47-56.    

45. Philip L, Iyengar L, Venkobachar C (2000) Site of Interaction of Copper on Bacillus Polymyxa. Water Air Soil Pollut 119: 11-21.    

Copyright Info: © 2016, Pilar Junier, et al., licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

Download full text in PDF

Export Citation

Article outline

Show full outline
Copyright © AIMS Press All Rights Reserved