Skip to main content
Log in

Sulfide-oxidizing bacteria establishment in an innovative microaerobic reactor with an internal silicone membrane for sulfur recovery from wastewater

  • Original Paper
  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

A novel bioreactor, employing a silicone membrane for microaeration, was studied for partial sulfide oxidation to elemental sulfur. The objective of this study was to assess the feasibility of using an internal silicone membrane reactor (ISMR) to treat dissolved sulfide and to characterize its microbial community. The ISMR is an effective system to eliminate sulfide produced in anaerobic reactors. Sulfide removal efficiencies reached 96 % in a combined anaerobic/microaerobic reactor and significant sulfate production did not occur. The oxygen transfer was strongly influenced by air pressure and flow. Pyrosequencing analysis indicated various sulfide-oxidizing bacteria (SOB) affiliated to the species Acidithiobacillus thiooxidans, Sulfuricurvum kujiense and Pseudomonas stutzeri attached to the membrane and also indicated similarity between the biomass deposited on the membrane wall and the biomass drawn from the material support, supported the establishment of SOB in an anaerobic sludge under microaerobic conditions. Furthermore, these results showed that the reactor configuration can develop SOB under microaerobic conditions and can improve and reestablish the sulfide conversion to elemental sulfur.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alcantara S, Velasco A, Munoz A, Cid J, Revah S, Razo-Flores E (2004) Hydrogen sulfide oxidation by a microbial consortium in a recirculation reactor system: sulfur formation under oxygen limitation and removal of phenols. Environ Sci Technol 38:918–923. doi:10.1021/es034527y

    Article  CAS  PubMed  Google Scholar 

  • Annachhatre AP, Suktrakoolvait S (2001) Biological sulfide oxidation in a fluidized bed reactor. Environ Technol 22:661–672. doi:10.1080/09593332208618238

    Article  CAS  PubMed  Google Scholar 

  • APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. Water Environment Federation, Washington

    Google Scholar 

  • Atkison B, Mavituna F (1983) Biochemical engineering and biotechnology handbook. Macmillan Publishers Ltda, New York

    Google Scholar 

  • Bartlett JK, Skoog DA (1954) Colorimetric determination of elemental sulfur in hydrocarbons. Anal Chem 26:1008–1011. doi:10.1021/ac60090a014

    Article  CAS  Google Scholar 

  • Brookes PR, Livingston AG (1995) Aqueous–aqueous extraction of organic pollutants through tubular silicone rubber membranes. J Membr Sci 104:119–137. doi:10.1016/0376-7388(95)00020-D

    Article  CAS  Google Scholar 

  • Bruno WJ, Socci ND, Halpern AL (2000) Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol Biol Evol 17:9

    Article  Google Scholar 

  • Buisman CJN, Geraats BG, Ijspeert P, Lettinga G (1990) Optimization of sulfur production in a biotechnological sulfide-removing reactor. Biotechnol Bioeng 35:50–56

    Article  CAS  PubMed  Google Scholar 

  • Buisman CJN, Ijspeert P, Hof A, Janssen AJH, Tenhagen R, Lettinga G (1991) Kinetic-parameters of a mixed culture oxidizing sulfide and sulfur with oxygen. Biotechnol Bioeng 38:813–820

    Article  CAS  PubMed  Google Scholar 

  • Camiloti PR, Mockaitis G, Domingues Rodrigues JA, Rissato Zamariolli Damianovic MH, Foresti E, Zaiat M (2013) Innovative anaerobic bioreactor with fixed-structured bed (ABFSB) for simultaneous sulfate reduction and organic matter removal. J Chem Technol Biotechnol 89:1044–1050. doi:10.1002/jctb.4199

    Article  Google Scholar 

  • Camiloti PR, Oliveira GHD, Zaiat M (2015) Sulfur recovery from wastewater using a micro-aerobic external silicone membrane reactor (ESMR). Water Air Soil Pollut 227:1–10. doi:10.1007/s11270-015-2721-y

    Google Scholar 

  • Chen KY, Morris JC (1972) Kinetics of oxidation of aqueous sulfide by oxygen. Environ Sci Technol 6:529–537. doi:10.1021/es60065a008

    Article  CAS  Google Scholar 

  • Cole JR et al (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145. doi:10.1093/nar/gkn879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Côté P, Bersillon J-L, Huyard A (1989) Bubble-free aeration using membranes: mass transfer analysis. J Membr Sci 47:91–106. doi:10.1016/S0376-7388(00)80862-5

    Article  Google Scholar 

  • Cotter SW (2010) Partial nitrification and oxygen transfer analysis utilizing hollow fiber membrane aeration. Iowa State University, Ames

    Google Scholar 

  • de Graaff M, Klok JBM, Bijmans MFM, Muyzer G, Janssen AJH (2012) Application of a 2-step process for the biological treatment of sulfidic spent caustics. Water Res 46:723–730. doi:10.1016/j.watres.2011.11.044

    Article  PubMed  Google Scholar 

  • Díaz I, Lopes AC, Perez SI, Fdz-Polanco M (2011a) Determination of the optimal rate for the microaerobic treatment of several H2S concentrations in biogas from sludge digesters. Water Sci Technol 64:6

    Article  Google Scholar 

  • Díaz I, Pérez SI, Ferrero EM, Fdz-Polanco M (2011b) Effect of oxygen dosing point and mixing on the microaerobic removal of hydrogen sulphide in sludge digesters. Bioresour Technol 102:3768–3775. doi:10.1016/j.biortech.2010.12.016

    Article  PubMed  Google Scholar 

  • Dickie IA (2010) Insidious effects of sequencing errors on perceived diversity in molecular surveys. New Phytol 188:916–918. doi:10.1111/j.1469-8137.2010.03473.x

    Article  PubMed  Google Scholar 

  • Fdz-Polanco M, Díaz I, Pérez SI, Lopes AC, Fdz-Polanco F (2009) Hydrogen sulphide removal in the anaerobic digestion of sludge by micro-aerobic processes: pilot plant experience. Water Sci Technol 60:6

    Article  Google Scholar 

  • Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Janssen AJH, Sleyster R, Vanderkaa C, Jochemsen A, Bontsema J, Lettinga G (1995) Biological sulfide oxidation in a fed-batch reactor. Biotechnol Bioeng 47:327–333

    Article  CAS  PubMed  Google Scholar 

  • Janssen AJH, Lettinga G, de Keizer A (1999) Removal of hydrogen sulphide from wastewater and waste gases by biological conversion to elemental sulphur—colloidal and interfacial aspects of biologically produced sulphur particles. Colloids Surf a 151:389–397

    Article  CAS  Google Scholar 

  • Kelly DP, Wood AP (2000) Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol 50:6

    Google Scholar 

  • Kleinjan WE, de Keizer A, Janssen AJH (2005) Kinetics of the chemical oxidation of polysulfide anions in aqueous solution. Water Res 39:4093–4100. doi:10.1016/j.watres.2005.08.006

    Article  CAS  PubMed  Google Scholar 

  • Kodama Y, Watanabe K (2004) Sulfuricurvum kujiense gen. nov., sp. nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity. Int J Syst Evol Microbiol 54:4

    Article  Google Scholar 

  • Krayzelova L, Bartacek J, Kolesarova N, Jenicek P (2014) Microaeration for hydrogen sulfide removal in UASB reactor. Bioresour Technol 172:6

    Article  Google Scholar 

  • Krayzelova L, Bartacek J, Díaz I, Jeison D, Volcke EIP, Jenicek P (2015) Microaeration for hydrogen sulfide removal during anaerobic treatment: a review. Rev Environ Sci Biotechnol 14:23

    Article  Google Scholar 

  • Lens PNL, Visser A, Janssen AJH, Pol LWH, Lettinga G (1998) Biotechnological treatment of sulfate-rich wastewaters. Crit Rev Environ Sci Technol 28:41–88

    Article  CAS  Google Scholar 

  • Mahmood Q, Zeng P, Hu B, Jilani G, Azim MR, Wu D, Liu D (2009) Isolation and characterization of Pseudomonas stutzeri QZ1 from an anoxic sulfide-oxidizing bioreactor. Anaerobe 15:8

    Article  Google Scholar 

  • Manconi I, Lens PNL (2009) Removal of H2S and volatile organic sulfur compounds by silicone membrane extraction. J Chem Technol Biotechnol 84:69–77. doi:10.1002/jctb.2008

    Article  CAS  Google Scholar 

  • Nawrocki EP, Kolbe DL, Eddy SR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25:1335–1337. doi:10.1093/bioinformatics/btp157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura S, Yoda M (1997) Removal of hydrogen sulfide from an anaerobic biogas using a bio-scrubber. Water Sci Technol 36:349–356. doi:10.1016/S0273-1223(97)00542-8

    Article  CAS  Google Scholar 

  • Pokasoowan C, Kanitchaidecha W, Bal Krishna KC, Annachhatre AP (2009) Investigation on laboratory and pilot-scale airlift sulfide oxidation reactor under varying sulfide loading rate. J Environ Sci Health A 44:87–98. doi:10.1080/10934520802515426

    Article  CAS  Google Scholar 

  • Raghunath B, Hwang ST (1992) Effect of boundary layer mass transfer resistance in the pervaporation of dilute organics. J Membr Sci 65:147–161. doi:10.1016/0376-7388(92)87061-2

    Article  CAS  Google Scholar 

  • Ramos I, Diaz I, Fdz-Polanco M (2012) The role of the headspace in hydrogen sulfide removal during microaerobic digestion of sludge. Water Sci Technol 66:7

    Article  Google Scholar 

  • Sercu B, Núñez D, Van Langenhove H, Aroca G, Verstraete W (2005) Operational and microbiological aspects of a bioaugmented two-stage biotrickling filter removing hydrogen sulfide and dimethyl sulfide. Biotechnol Bioeng 90:259–269. doi:10.1002/bit.20443

    Article  CAS  PubMed  Google Scholar 

  • Wilderer PA, Bräutigam J, Sekoulov I (1985) Application of gas permeable membranes for auxiliary oxygenation of sequencing batch reactors. Conserv Recycl 8:181–192. doi:10.1016/0361-3658(85)90035-9

    Article  CAS  Google Scholar 

  • Wright ES, Yilmaz LS, Noguera DR (2012) DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl Environ Microbiol 78:9

    Article  Google Scholar 

  • Xu X-j, Chen C, A-j Wang, Fang N, Yuan Y, N-q Ren, Lee D-J (2012) Enhanced elementary sulfur recovery in integrated sulfate-reducing, sulfur-producing rector under micro-aerobic condition. Bioresour Technol 116:517–521. doi:10.1016/j.biortech.2012.03.095

    Article  CAS  PubMed  Google Scholar 

  • Zaiat M, Cabral AKA, Foresti E (1994) Reator anaeróbio horizontal de leito fixo para tratamento de águas residuárias: concepção e avaliação preliminar de desempenho. Rev Bras Engenh 11:33–42

    Google Scholar 

  • Zee FPvd, Villaverde S, García PA, Fdz-Polanco F (2007) Sulfide removal by moderate oxygenation of anaerobic sludge environments. Bioresour Technol 98:7

    Google Scholar 

Download references

Acknowledgments

The authors thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP—Project Number 2009/15984-0 and 2011/22904-3), and the Comisión Nacional de Investigación Científica y Tecnológica de Chile for their financial support and national doctoral scholarship. David Jeison would like to thank for support provided by CRHIAM Centre  (CONICYT/FONDAP/15130015).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. R. Camiloti.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 84 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valdés, F., Camiloti, P.R., Rodriguez, R.P. et al. Sulfide-oxidizing bacteria establishment in an innovative microaerobic reactor with an internal silicone membrane for sulfur recovery from wastewater. Biodegradation 27, 119–130 (2016). https://doi.org/10.1007/s10532-016-9760-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-016-9760-y

Keywords

Navigation