Skip to main content
SpringerLink
Log in

Electron donors and co-contaminants affect microbial community composition and activity in perchlorate degradation

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Although microbial reduction of perchlorate (ClO4 −) is a promising and effective method, our knowledge on the changes in microbial communities during ClO4 − degradation is limited, especially when different electron donors are supplied and/or other contaminants are present. Here, we examined the effects of acetate and hydrogen as electron donors and nitrate and ammonium as co-contaminants on ClO4 − degradation by anaerobic microcosms using six treatments. The process of degradation was divided into the lag stage (SI) and the accelerated stage (SII). Quantitative PCR was used to quantify four genes: pcrA (encoding perchlorate reductase), cld (encoding chlorite dismutase), nirS (encoding copper and cytochrome cd1 nitrite reductase), and 16S rRNA. While the degradation of ClO4 − with acetate, nitrate, and ammonia system (PNA) was the fastest with the highest abundance of the four genes, it was the slowest in the autotrophic system (HYP). The pcrA gene accumulated in SI and played a key role in initiating the accelerated degradation of ClO4 − when its abundance reached a peak. Degradation in SII was primarily maintained by the cld gene. Acetate inhibited the growth of perchlorate-reducing bacteria (PRB), but its effect was weakened by nitrate (NO3 −), which promoted the growth of PRB in SI, and therefore, accelerated the ClO4 − degradation rate. In addition, ammonia (NH4 +), as nitrogen sources, accelerated the growth of PRB. The bacterial communities’ structure and diversity were significantly affected by electron donors and co-contaminants. Under heterotrophic conditions, both ammonia and nitrate promoted Azospira as the most dominant genera, a fact that might significantly influence the rate of ClO4 − natural attenuation by degradation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Achenbach LA, Michaelidou U, Bruce RA, Fryman J, Coates JD (2001) Dechloromonas agitata gen. nov., sp. nov. and Dechlorosoma suillum gen. nov., sp. nov., two novel environmentally dominant (per)chlorate-reducing bacteria and their phylogenetic position. Int J Syst Evol Microbiol 51:527–533

    CAS  Google Scholar 

  • Bardiya N, Bae JH (2011) Dissimilatory perchlorate reduction: a review. Microbiol Res 166:237–254

    Article  CAS  Google Scholar 

  • Bender KS, Shang C, Chakraborty R, Belchik SM, Coates JD, Achenbach LA (2005) Identification, characterization, and classification of genes encoding perchlorate reductase. J Bacteriol 187:5090–5096

    Article  CAS  Google Scholar 

  • Bruce RA, Achenbach LA, Coates JD (1999) Reduction of (per)chlorate by a novel organism isolated from paper mill waste. Environ Microbiol 1:319–329

    Article  CAS  Google Scholar 

  • Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267

    Article  CAS  Google Scholar 

  • Caporaso JG et al (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  • Charnley G (2008) Perchlorate: overview of risks and regulation. Food Chem Toxicol 46:2307–2315

    Article  CAS  Google Scholar 

  • Chaudhuri SK, O’Connor SM, Gustavson RL, Achenbach LA, Coates JD (2002) Environmental factors that control microbial perchlorate reduction. Appl Environ Microbiol 68:4425–4430

    Article  CAS  Google Scholar 

  • Choi H, Silverstein J (2008) Inhibition of perchlorate reduction by nitrate in a fixed biofilm reactor. J Hazard Mater 159:440–445

    Article  CAS  Google Scholar 

  • Chung J, Nerenberg R, Rittmann BE (2007) Evaluation for biological reduction of nitrate and perchlorate in brine water using the hydrogen-based membrane biofilm reactor. J Environ Eng-Asce 133:157–164

    Article  CAS  Google Scholar 

  • Coates JD, Achenbach LA (2004) Microbial perchlorate reduction: rocket-fuelled metabolism. Nat Rev Microbiol 2:569–580

    Article  CAS  Google Scholar 

  • Coates JD, Michaelidou U, Bruce RA, O’Connor SM, Crespi JN, Achenbach LA (1999) Ubiquity and diversity of dissimilatory (per)chlorate-reducing bacteria. Appl Environ Microbiol 65:5234–5241

    CAS  Google Scholar 

  • De Long SK, Kinney KA, Kirisits MJ (2010) qPCR assays to quantify genes and gene expression associated with microbial perchlorate reduction. J Microbiol Meth 83:270–274

    Article  Google Scholar 

  • De Long SK, Li X, Bae S, Brown JC, Raskin L, Kinney KA, Kirisits MJ (2012) Quantification of genes and gene transcripts for microbial perchlorate reduction in fixed-bed bioreactors. J Appl Microbiol 112:579–592

    Article  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  Google Scholar 

  • Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10

    Article  Google Scholar 

  • Farhan YH, Hatzinger PB (2009) Modeling the biodegradation kinetics of perchlorate in the presence of oxygen and nitrate as competing electron acceptors. Bioremediat J 13:65–78

    Article  CAS  Google Scholar 

  • Giblin T, Frankenberger WT (2001) Perchlorate and nitrate reductase activity in the perchlorate-respiring bacterium perclace. Microbiol Res 156:311–315

    Article  CAS  Google Scholar 

  • Gingras TM, Batista JR (2002) Biological reduction of perchlorate in ion exchange regenerant solutions containing high salinity and ammonium levels. J Environ Monitor 4:96–101

    Article  CAS  Google Scholar 

  • Haas BJ et al (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504

    Article  CAS  Google Scholar 

  • Gal H, Ronen Z, Weisbrod N, Dahan O, Nativ R (2008) Perchlorate biodegradation in contaminated soils and the deep unsaturated zone. Soil Biol Biochem 40:1751–1757

    Article  CAS  Google Scholar 

  • Herman DC, Frankenberger WT (1999) Bacterial reduction of perchlorate and nitrate in water. J Environ Qual 28:1018–1024

    Article  CAS  Google Scholar 

  • Heylen K, Lebbe L, De Vos P (2008) Acidovorax caeni sp. nov., a denitrifying species with genetically diverse isolates from activated sludge. Int J Syst Evol Microbiol 58:73–77

    Article  CAS  Google Scholar 

  • Krauter P, Daily B Jr, Dibley V, Pinkart H, Legler T (2005) Perchlorate and nitrate remediation efficiency and microbial diversity in a containerized wetland bioreactor. Int J Phytoremediation 7:113–128

    Article  CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, West Sussex, United Kingdom, pp 115–175

    Google Scholar 

  • Li X, Yuen W, Morgenroth E, Raskin L (2012) Backwash intensity and frequency impact the microbial community structure and function in a fixed-bed biofilm reactor. Appl Microbiol Biotechnol 96:815–827

    Article  CAS  Google Scholar 

  • Logan BE (2001) Assessing the outlook for perchlorate remediation. Environ Sci Technol 35:482–487

    Article  Google Scholar 

  • London MR, De Long SK, Strahota MD, Katz LE, Speitel GE Jr (2011) Autohydrogenotrophic perchlorate reduction kinetics of a microbial consortium in the presence and absence of nitrate. Water Res 45:6593–6601

    Article  CAS  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  CAS  Google Scholar 

  • Matos CT, Velizarov S, Crespo JG, Reis MAM (2006) Simultaneous removal of perchlorate and nitrate from drinking water using the ion exchange membrane bioreactor concept. Water Res 40:231–240

    Article  CAS  Google Scholar 

  • Michaelidou U, Coates JD, Achenbach LA (2000) Isolation and characterization of two novel (per)chlorate-reducing bacteria from swine waste lagoons. Perchlorate in the Environment. Springer US, 271-283

  • Muyzer G (2004) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: G.A. Kowalchuk (ed.) Molecular microbial ecology manual. Dordrecht, Kluwer, pp 743–769

  • Nerenberg R, Rittmann BE (2004) Hydrogen-based, hollow-fiber membrane biofilm reactor for reduction of perchlorate and other oxidized contaminants. Water Sci Technol 49:223–230

    CAS  Google Scholar 

  • Nozawa-Inoue M, Jien M, Hamilton NS, Stewart V, Scow KM, Hristova KR (2008) Quantitative detection of perchlorate-reducing bacteria by real-time PCR targeting the perchlorate reductase gene. Appl Environ Microbiol 74:1941–1944

    Article  CAS  Google Scholar 

  • Nozawa-Inoue M, Jien M, Yang K, Rolston DE, Hristova KR, Scow KM (2011) Effect of nitrate, acetate, and hydrogen on native perchlorate-reducing microbial communities and their activity in vadose soil. Fems Microbiol Ecol 76:278–288

    Article  CAS  Google Scholar 

  • Nozawa-Inoue M, Scow KM, Rolston DE (2005) Reduction of perchlorate and nitrate by microbial communities in vadose soil. Appl Environ Microbiol 71:3928–3934

    Article  CAS  Google Scholar 

  • Oh J, Silverstein J (1999) Acetate limitation and nitrite accumulation during denitrification. J Environ Eng-Asce 125:234–242

    Article  CAS  Google Scholar 

  • Oosterkamp MJ, Boeren S, Plugge CM, Schaap PJ, Stams AJ (2013) Metabolic response of Alicycliphilus denitrificans strain BC towards electron acceptor variation. Proteomics 13:2886–2894

    CAS  Google Scholar 

  • Pielou E (1966) The measurement of diversity in different types of biological collections. Theor Biol 13:131–144

    Article  Google Scholar 

  • Price AL, Kryukov GV, de Bakker PI, Purcell SM, Staples J, Wei LJ, Sunyaev SR (2010) Pooled association tests for rare variants in exon-resequencing studies. Am J Hum Genet 86:832–838

    Article  Google Scholar 

  • Raj JRA, Muruganandam L (2012) Batch studies and effect of environmental parameters on microbial degradation of perchlorate using acclimatized effluent sludge research. J Chem Environ 16:44–50

    Google Scholar 

  • Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7:668–669

    Article  CAS  Google Scholar 

  • Sun Y, Gustavson RL, Ali N, Weber KA, Westphal LL, Coates JD (2009) Behavioral response of dissimilatory perchlorate-reducing bacteria to different electron acceptors. Appl Microbiol Biotechnol 84:955–963

    Article  CAS  Google Scholar 

  • Tipton DK, Rolston DE, Scow KM (2003) Transport and biodegradation of perchlorate in soils. J Environ Qual 32:40–46

    Article  CAS  Google Scholar 

  • Tran N et al (2008) Thyroid-stimulating hormone increases active transport of perchlorate into thyroid cells. Am J Physiol Endocrinol Metab 294:802–806

    Article  Google Scholar 

  • Urbansky ET (1998) Perchlorate chemistry: implications for analysis and remediation. Bioremediat J 2:81–95

    Article  CAS  Google Scholar 

  • Waller AS, Cox EE, Edwards EA (2004) Perchlorate-reducing microorganisms isolated from contaminated sites. Environ Microbiol 6:517–527

    Article  CAS  Google Scholar 

  • Wang C, Lippincott L, Meng X (2008) Kinetics of biological perchlorate reduction and pH effect. J Hazard Mater 153:663–669

    Article  CAS  Google Scholar 

  • Wang J, Soininen J, He J, Shen J (2012) Phylogenetic clustering increases with elevation for microbes. Environ Microbiol Rep 4:217–226

    Article  Google Scholar 

  • 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 73:5261–5267

    Article  CAS  Google Scholar 

  • Xiao Y, Roberts DJ, Zuo G, Badruzzaman M, Lehman GS (2010) Characterization of microbial populations in pilot-scale fluidized-bed reactors treating perchlorate- and nitrate-laden brine. Water Res 44:4029–4036

    Article  CAS  Google Scholar 

  • Xu J, Gao N, Tang Y, Deng Y, Sui M (2010) Perchlorate removal using granular activated carbon supported iron compounds: Synthesis, characterization and reactivity. J Environ Sci-China 22:1807–1813

    Article  CAS  Google Scholar 

  • Xu J, Trimble JJ, Steinberg L, Logan BE (2004) Chlorate and nitrate reduction pathways are separately induced in the perchlorate-respiring bacterium Dechlorosoma sp. KJ and the chlorate-respiring bacterium Pseudomonas sp. PDA. Water Res 38:673–680

    Article  CAS  Google Scholar 

  • Ye L, You H, Yao J, Kang X, Tang L (2013) Seasonal variation and factors influencing perchlorate in water, snow, soil and corns in Northeastern China. Chemosphere 90:2493–2498

    Article  CAS  Google Scholar 

  • Zhao HP, Van Ginkel S, Tang Y, Kang DW, Rittmann B, Krajmalnik-Brown R (2011) Interactions between perchlorate and nitrate reductions in the biofilm of a hydrogen-based membrane biofilm reactor. Environ Sci Technol 45:10155–10162

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by National Natural Science Foundation of China (40972162, granted to FL), Beijing Higher Education Young Elite Teacher Project (granted to XYG), and The Fundamental Research Funds for the Central Universities (2012071, granted to XYG).

Author information

Authors and Affiliations

  1. Beijing Key Laboratory of Water Resources and Environmental Engineering, China University of Geosciences, Beijing, 100083, China

    Xiangyu Guan, Yuxuan Xie & Fei Liu

  2. School of Ocean Sciences, China University of Geosciences, Beijing, 100083, China

    Xiangyu Guan & Jing Wang

  3. Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing, 100101, China

    Jinfeng Wang

  4. Graduate Department, Jilin Jianzhu University, Changchun, 130118, China

    Yuxuan Xie

Authors
  1. Xiangyu Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuxuan Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinfeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fei Liu.

Additional information

Responsible editor: Gerald Thouand

Xiangyu Guan and Yuxuan Xie equally contributed to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guan, X., Xie, Y., Wang, J. et al. Electron donors and co-contaminants affect microbial community composition and activity in perchlorate degradation. Environ Sci Pollut Res 22, 6057–6067 (2015). https://doi.org/10.1007/s11356-014-3792-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3792-9

Keywords

Search

Navigation