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Relationship between microbial community dynamics and process performance during thermophilic sludge bioleaching

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Abstract

Heavy metals can be removed from the sludge using bioleaching technologies at thermophilic condition, thereby providing an option for biotreatment of wasted sludge generated from wastewater treatment. The purposes of this study were to establish a molecular biology technique, real-time PCR, for the detection and enumeration of the sulfur-oxidizing bacteria during the thermophilic sludge bioleaching. The 16S rRNA gene for real-time PCR quantification targeted the bioleaching bacteria: Sulfobacillus thermosulfidooxidans, Sulfobacillus acidophilus, and Acidithiobacillus caldus. The specificity and stringency for thermophilic sulfur-oxidizing bacteria were tested before the experiments of monitoring the bacterial community, bacterial number during the thermophilic sludge bioleaching and the future application on testing various environmental samples. The results showed that S. acidophilus was identified as the dominant sulfur-oxidizing bacteria, while A. caldus and S. thermosulfidooxidans occurred in relatively low numbers. The total number of the sulfur-oxidizing bacteria increased during the thermophilic bioleaching process. Meanwhile, the decrease of pH, production of sulfate, degradation of SS/VSS, and solubilization of heavy metal were found to correlate well with the population of thermophilic sulfur-oxidizing bacteria during the bioleaching process. The real-time PCR used in this study is a suitable method to monitor numbers of thermophilic sulfur-oxidizing bacteria during the bioleaching process.

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References

  • APHA (2005) Standard methods for examination of water and wastewater, 21st edn. American Public Health Association, Washington

    Google Scholar 

  • Babel S, del Mundo DD (2006) Heavy metal removal from contaminated sludge for land application: a review. Waste Manage 26:988–1004

    Article  CAS  Google Scholar 

  • Babu BK, Mesapogu S, Sharma A, Somasani SR, Arora DK (2011) Quantitative real-time PCR assay for rapid detection of plant and human pathogenic Macrophomina phaseolina from field and environmental samples. Mycologia 103:466–473

    Article  Google Scholar 

  • Chen SY, Huang QY (2014) Heavy metals recovery from wastewater sludge of printed circuit board industry by thermophilic bioleaching process. J Chem Technol Biotechnol 89:158–164

    Article  CAS  Google Scholar 

  • Chen SY, Lin JG (2009) Enhancement of metal bioleaching from contaminated sediment using silver ion. J Hazard Mater 161:893–899

    Article  CAS  Google Scholar 

  • Chen SY, Lin PL (2010) Optimization of operating parameters for the metal bioleaching process of contaminated soil. Sep Purif Technol 71:178–185

    Article  CAS  Google Scholar 

  • Chen SY, Pan SH (2010) Simultaneous metal leaching and sludge digestion by thermophilic microorganisms: effect of solids content. J Hazard Mater 179:340–347

    Article  CAS  Google Scholar 

  • Chen SY, Chiu YC, Chang PL, Lin JG (2003) Assessment of recoverable forms of sulfur particles used in bioleaching of contaminated sediments. Water Res 37:450–458

    Article  CAS  Google Scholar 

  • d’Hugues P, Foucher S, Galle-Cavalloni P, Morin D (2002) Continuous bioleaching of chalcopyrite using a novel extremely thermophilic mixed culture. Int J Miner Process 66:107–119

    Article  Google Scholar 

  • de La Rochebrochard S, Naffrechoux E, Drogui P, Mercier G, Blais JF (2013) Low frequency ultrasound-assisted leaching of sewage sludge for toxic metal removal, dewatering and fertilizing properties preservation. Ultrason Sonochem 20:109–117

    Article  Google Scholar 

  • Dopson M, Lindstrom EB (2004) Analysis of community composition during moderately thermophilic bioleaching of pyrite, arsenical pyrite, and chalcopyrite. Microb Ecol 48:19–28

    Article  CAS  Google Scholar 

  • Evaristo AAA, Santos KCR, Costa LC, Marques MRC (2013) Evaluation of ion exchange resins for recovery of metals from electroplating sludges. Polymer Bull 70:2239–2255

    Article  CAS  Google Scholar 

  • Gao J, Luo QS, Zhang CB, Li BZ, Meng L (2013) Enhanced electrokinetic removal of cadmium from sludge using a coupled catholyte circulation system with multilayer of anion exchange resin. Chem Eng J 234:1–8

    Article  CAS  Google Scholar 

  • Gerayeli F, Ghojavand F, Mousavi SM, Yaghmaei S, Amiri F (2013) Screening and optimization of effective parameters in biological extraction of heavy metals from refinery spent catalysts using a thermophilic bacterium. Sep Purif Technol 118:151–161

    Article  CAS  Google Scholar 

  • Ilyas S, Lee J, Kim B (2014) Bioremoval of heavy metals from recycling industry electronic waste by a consortium of moderate thermophiles: process development and optimization. J Clean Prod 70:194–202

    Article  CAS  Google Scholar 

  • Ito A, Umita T, Aizawa J, Takachi T, Morinaga K (2000) Removal of heavy metals from anaerobically digested sewage sludge by a new chemical method using ferric sulfate. Water Res 34:751–758

    Article  CAS  Google Scholar 

  • Kirk JL, Beaudette LA, Hart M, Moutoglis P, Klironomos JN, Lee H, Trevors JT (2004) Methods of studying soil microbial diversity. J Microbiol Methods 58:169–188

    Article  CAS  Google Scholar 

  • Liu CQ, Plumb J, Hendry P (2006) Rapid specific detection and quantification of bacteria and archaea involved in mineral sulfide bioleaching using real-time PCR. Biotechnol Bioeng 94:330–336

    Article  CAS  Google Scholar 

  • Mousavi SM, Yaghmaei S, Vossoughi M, Jafari A, Hoseini SA (2005) Comparison of bioleaching ability of two native mesophilic and thermophilic bacteria on copper recovery from chalcopyrite concentrate in an airlift bioreactor. Hydrometallurgy 80:139–144

    Article  CAS  Google Scholar 

  • Mudhoo A, Kumar S (2013) Effects of heavy metals as stress factors on anaerobic digestion processes and biogas production from biomass. Int J Environ Sci Technol 10:1383–1398

    Article  CAS  Google Scholar 

  • Naocum C, Fatta D, Haralambous KJ, Loizidou M (2001) Removal of heavy metals from sewage sludge by acid treatment. J Environ Sci Health A 36:873–881

    Article  Google Scholar 

  • Okibe N, Johnson DB (2004) Biooxidation of pyrite by defined mixed cultures of moderately thermophilic acidophiles in pH-controlled bioreactors: significance of microbial interactions. Biotechnol Bioeng 87:574–583

    Article  CAS  Google Scholar 

  • Paivi HM, Kinunen J, Puhakka A (2004) Characterization of iron- and sulphide mineral-oxidizing moderately thermophilic acidophilic bacteria from an Indonesian auto-heating copper mine waste heap and a deep South African gold mine. J Ind Microbiol Biotechnol 31:409–414

    Article  Google Scholar 

  • Park HS, Lee JU, Ahn JW (2007) The effects of Acidithiobacillus ferrooxidans on the leaching of cobalt and strontium adsorbed onto soil particles. Environ Geochem Health 29:303–312

    Article  CAS  Google Scholar 

  • Pina PS, Oliveira VA, Cruz FLS, Leão VA (2010) Kinetics of ferrous iron oxidation. Biochem Eng J 51:194–197

    Article  CAS  Google Scholar 

  • Plumb JJ, Gibbs B, Stott MB, Robertson WJ, Gibson JAE, Nichols PD, Watling HR, Franzmann PD (2002) Enrichment and characterization of thermophilic acidophiles for the bioleaching of mineral sulphides. Min Eng 15:787–794

    Article  CAS  Google Scholar 

  • Plumb JJ, Muddle R, Franzmann PD (2008) Effect of pH on rates of iron and sulfur oxidation by bioleaching organisms. Miner Eng 21:76–82

    Article  CAS  Google Scholar 

  • Robertson WJ, Kinnunen PHM, Plumb JJ, Franzmann PD, Puhakka JA, Gibson JAE, Nichols PD (2002) Moderately thermophilic iron oxidizing bacteria isolated from a pyritic coal deposit showing spontaneous combustion. Min Eng 15:815–822

    Article  CAS  Google Scholar 

  • Rompre A, Servais P, Baudart J, de-Roubin MR, Laurent P (2002) Detection and enumeration of coliforms in drinking water: current methods and emerging approaches. J Microbiol Methods 49:31–54

    Article  Google Scholar 

  • Salo-Zieman VLA, Kinnunen PHM, Puhakka JA (2006) Bioleaching of acid-consuming low-grade nickel ore with elemental sulfur addition and subsequent acid generation. J Chem Technol Biotechnol 81:34–40

    Article  CAS  Google Scholar 

  • Schabereiter-Gurtner C, Piñar G, Lubitz W, Rölleke S (2001) An advanced molecular strategy to identify bacterial communities on art objects. J Microbiol Methods 45:77–87

    Article  CAS  Google Scholar 

  • Schippers A, Nagy AA, Kock D, Melcher F, Gock ED (2008) The use of FISH and real-time PCR to monitor the biooxidation and cyanidation for gold and silver recovery from a mine tailings concentrate (Ticapampa, Peru). Hydrometallurgy 94:77–84

    Article  CAS  Google Scholar 

  • Shiers D, Ralph D, Watling H (2010) A comparative study of substrate utilization by Sulfobacillus species in mixed ferrous ion and tetrathionate growth medium. Hydrometallurgy 104:363–369

    Article  CAS  Google Scholar 

  • USEPA (1995) Microwave assisted acid digestion of sediments, sludge, and oils. Test methods for evaluating solid waste, method 3052. USEPA, USA

    Google Scholar 

  • USEPA (2004) Physical/chemical methods: soil and waste pH. Test methods for evaluating solid waste, method 9045D. USEPA, USA

    Google Scholar 

  • Wang X, Chen L, Xia S, Zhao J (2008) Changes of Cu, Zn, and Ni chemical speciation in sewage sludge co-composted with sodium sulfide and lime. J Environ Sci 20:156–160

    Article  CAS  Google Scholar 

  • Wang Q, Ye L, Jiang G, Jensen PD, Batstone DJ, Yuan Z (2013) Free nitrous acid (FNA)-based pretreatment enhances methane production from waste activated sludge. Environ Sci Technol 47:11897–11904

    Article  CAS  Google Scholar 

  • Wang Y, Zeng W, Qiu G, Chen X, Zhou H (2014) A moderately thermophilic mixed microbial culture for bioleaching of chalcopyrite concentrate at high pulp density. Appl Environ Microbiol 80:741–750

    Article  Google Scholar 

  • Wang D, Zeng G, Chen Y, Li X (2015) Effect of polyhydroxyalkanoates on dark fermentative hydrogen production from waste activated sludge. Water Res 73:311–322

    Article  CAS  Google Scholar 

  • Watling HR, Perrot FA, Shiers DW (2008) Comparison of selected characteristics of Sulfobacillus species and review of their occurrence in acidic and bioleaching environments. Hydrometallurgy 93:57–65

    Article  CAS  Google Scholar 

  • Watling HR, Collinson DM, Fjastad S, Kaksonen AH, Li J, Morris C, Perrot FA, Rea SM, Shiers DW (2014) Column bioleaching of a polymetallic ore: Effects of pH and temperature on metal extraction and microbial community structure. Min Eng 58:90–99

    Article  CAS  Google Scholar 

  • Wong JWC, Xiang L, Gu XY, Zhou LX (2004) Bioleaching of heavy metals from anaerobically digested sewage sludge using FeS2 as an energy source. Chemosphere 55:101–107

    Article  CAS  Google Scholar 

  • Yabalak E, Gizir AM (2013) Subcritical and supercritical fluid extraction of heavy metals from sewage sludge. J Serb Chem Soc 78:1013–1022

    Article  CAS  Google Scholar 

  • Zaleckas E, Paulaukas V, Sendzikiene E (2013) Fractionation of heavy metals in sewage sludge and their removal using low-molecular-weight organic acids. J Environ Eng Landsc Manag 21:189–198

    Article  Google Scholar 

  • Zammit CM, Mutch LA, Watling HR, Watkin ELJ (2008) Evaluation of quantitative real-time polymerase chain reaction for enumeration of biomining microorganisms in culture. Hydrometallurgy 94:185–189

    Article  CAS  Google Scholar 

  • Zhang R, Wei M, Ji H, Chen X, Qiu G, Zhou H (2009) Application of real-time PCR to monitor population dynamics of defined mixed cultures of moderate thermophiles involved in bioleaching of chalcopyrite. Appl Microbiol Biotechol 81:1161–1168

    Article  CAS  Google Scholar 

  • Zhao J, Wang D, Li X, Yang Q, Chen H, Zhong Y, Zeng G (2015) Free nitrous acid serving as a pretreatment method for alkaline fermentation to enhance short-chain fatty acid production from waste activated sludge. Water Res 78:111–120

    Article  CAS  Google Scholar 

  • Zhou HB, Zeng WM, Yang ZF, Xie YJ, Qiu GZ (2009) Bioleaching of chalcopyrite concentrate by a moderately thermophilic culture in a stirred tank reactor. Bioresour Technol 100:515–520

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The work described in this paper was fully supported by a Grant in Aid from the Ministry of Science and Technology, Executive Yuan, Taiwan (NSC 100-2622-E-327-018-CC3).

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Correspondence to Shen-Yi Chen.

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Responsible editor: Gerald Thouand

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Chen, SY., Chou, LC. Relationship between microbial community dynamics and process performance during thermophilic sludge bioleaching. Environ Sci Pollut Res 23, 16006–16014 (2016). https://doi.org/10.1007/s11356-016-6716-z

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