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Isolation and characterization of a heterotrophic nitrifier Proteus mirabilis strain V7 and its potential application in NH4 +-N removal

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Abstract

Ammonia (referring to both NH3 and NH4 +), is one of the most toxic nitrogen forms, and is toxic to many aquatic organisms. The present study identified a heterotrophic nitrifier Proteus mirabilis strain V7, isolated from the coastal seawater. Almost 100 % of 82 mg L–1 NH4 +-N was removed within 48 h, while 51.2 % of total inorganic nitrogen was removed within 96 h after inoculation of Proteus mirabilis strain V7. Moreover, Proteus mirabilis strain V7 could remove NH4 +-N in a seawater matrix, but with much lower efficiency. Three water samples containing NH4 +-N at concentrations of 64.40, 18.00 and 9.82 mg L–1 were chosen to further test the NH4 +-N removal ability of Proteus mirabilis strain V7. All of the NH4 +-N was removed, with only a trace production of NO2 and NO3 . A putative subunit of ammonia monooxygenase from Proteus mirabilis strain V7, amoA Pm, was cloned and its mRNA level in the presence of NH4 + was characterized by real time reverse transcriptase PCR (RT-PCR). A 1.8-fold increase in the mRNA level of amoA Pm was observed, which indicated that AmoA may be involved in NH4 + oxidization. Our results indicated that Proteus mirabilis strain V7 could potentially be used as new resource for the treatment of NH4 +-N contaminated environments.

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References

  • Alcaraz G, Espinoza V, Vanegas C, Carrara XC (1999) Acute effect of ammonia and nitrite on respiration of Penaeus setiferus postlarvae under different oxygen levels. J World Aquacult Soc 30:98–106

    Article  Google Scholar 

  • Alexander M (1977) Nitrification. In: Soil microbiology, 2nd edn. Wiley, New York, pp 251–271

  • Andrade do Canto CS, Rodrigues JA, Ratusznei SM, Zaiat M, Foresti E (2008) Feasibility of nitrification/denitrification in a sequencing batch biofilm reactor with liquid circulation applied to post-treatment. Bioresourc Technol 99:644–654

    Article  CAS  Google Scholar 

  • APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, AWWA, WEF , Washington, DC

  • Bergmann DG, Hooper AB (1994) Sequence of the gene, amo B, for the 43-kDa polypeptide of ammonia monooxygenase of Nitrosomonas europaea. Biochem Biophys Res Commun 204:759–762

    Article  CAS  PubMed  Google Scholar 

  • Castignetti D, Hollocher T (1982) Nitrogen redox metabolism of a heterotrophic, nitrifying-denitrifying Alcaligenes sp. from soil. Appl Environ Microbiol 44:923–928

    CAS  PubMed Central  PubMed  Google Scholar 

  • Castignetti D, Hollocher T (1984) Heterotrophic nitrification among denitrifiers. Appl Environ Microbiol 47:620–623

    CAS  PubMed Central  PubMed  Google Scholar 

  • Daum M, Zimmer W, Papen H, Kloos K, Nawrath K, Bothe H (1998) Physiological and molecular biological characterization of ammonia oxidation of the heterotrophic nitrifier Pseudomonas putida. Curr Microbiol 37:281–288

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Khare SK (2006) A protease stable in organic solvents from solvent tolerant strain of Pseudomonas aeruginosa. Bioresour Technol 97:1788–1793

    Article  CAS  PubMed  Google Scholar 

  • Hasan HA, Sheikh Abdullah SR, Kofli NT, Kamarudin SK (2012) Removal of ion in drinking water treatment using locally isolated heterotrophic nitrifier. Desalin Water Treat 50:294–301

    Article  CAS  Google Scholar 

  • Hirota R, Yamagata A, Kato J, Kuroda A, Ikeda T, Takiguchi N, Ohtake H (2000) Physical map location of the multicopy genes coding for ammonia monooxygenase and hydroxylamine oxidoreductase in the ammonia-oxidizing bacterium Nitrosomonas sp. strain ENI-11. J Bacteriol 182:825–828

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huertas M, Duque E (1998) Survival in soil of different toluene-degrading Pseudomonas strains after solvent shock. Appl Environ Microbiol 64:38–42

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jetten MS, Logemann S, Muyzer G, Robertson LA, de Vries S, van Loosdrecht MC, Kuenen JG (1997) Novel principles in the microbial conversion of nitrogen compounds. Antonie Van Leeuwenhoek 71:75–93

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen TC, Weatherley LR (2003) Ammonia removal from wastewater by ion exchange in the presence of organic contaminants. Water Res 37:1723–1728

    Article  CAS  PubMed  Google Scholar 

  • Khardenavis AA, Kapley A, Purohit KJ (2007) Simultaneous nitrification and denitrification by diverse Diaphorobacter sp. Appl Microbiol Biotechnol 77:403–409

    Article  CAS  PubMed  Google Scholar 

  • Kim JK, Park KJ, Cho KS, Nam SW, Park TJ, Bajpai R (2005) Aerobic nitrification–denitrification by heterotrophic Bacillus strains. Bioresour Technol 96:1897–1906

    Article  CAS  PubMed  Google Scholar 

  • Klotz MG, Alzerreca J, Norton JM (1997) A gene encoding a membrane protein exists upstream of the amoA/amoB genes in ammonia oxidising bacteria: a third member of the amo operon? FEMS Microbiol Lett 150:65–73

    Article  CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • McTavish H, Fuchs JA, Hooper AB (1993) Sequence of the gene coding for ammonia monooxygenase in Nitrosomonas europaea. J Bacteriol 175:2436–2444

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mevel G, Prieur D (2000) Heterotrophic nitrification by a thermophilic Bacillus species as influenced by different culture conditions. Can J Microbiol 46:465–473

    Article  CAS  PubMed  Google Scholar 

  • Otte S, Grobben NG, Robertson LA, Jetten MSM, Kuenen JG (1996) Nitrous oxide production by Alcaligenes faecalis under transient and dynamic aerobic and anaerobic conditions. Appl Environ Microbiol 62:2421–2426

    CAS  PubMed Central  PubMed  Google Scholar 

  • Papen H, von Berg R (1998) A most probable number method for the estimation of cell numbers of heterotrophic nitrifying bacteria in soil. Plant Soil 799:723–730

    Google Scholar 

  • Papen H, von Berg R, Hinkel I, Thoene B, Rennenberg H (1989) Heterotrophic nitrification by Alcaligenes faecalis: NO2 -, NO3 -, N2O, and NO production in exponentially growing cultures. Appl Environ Microbiol 55:2068–2072

    CAS  PubMed Central  PubMed  Google Scholar 

  • Patureau D, Bernet N, Moletta R (1997) Combined nitrification and denitrification in a single aerated reactor using the aerobic denitrifier Comamonas sp. strain SGLY2. Water Res 31:1363–1370

    Article  CAS  Google Scholar 

  • Richardson DJ, Wehrfritz JM, Keech A, Crossman LC, Roldan MD, Sears HJ, Butler CS, Reilly A, Moir JWB, Berks BC, Ferguson SJ, Thomson AJ, Spiro S (1998) The diversity of redox proteins involved in bacterial heterotrophic nitrification and aerobic denitrification. Biochem Soc Trans 26:401–408

    CAS  PubMed  Google Scholar 

  • Robertson LA, Gijs Kuenen J (1984) Aerobic denitrification: a controversy revived. Arch Microbiol 139:351–354

    Article  CAS  Google Scholar 

  • Robertson LA, Van Neil EWJ, Torremans RAM, Kuenen JG (1988) Simultaneous nitrification and denitrification in aerobic chemost at cultures of Thiosphaera pantotropha. Appl Environ Microbiol 54:2812–2818

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rostron WM, Stuckey DC, Young AA (2001) Nitrification of high strength ammonia wastewaters: comparative study of immobilization media. Water Res 35:1169–1178

    Article  CAS  PubMed  Google Scholar 

  • Sardessai Y, Bhosle S (2002) Organic solvent-tolerant bacteria in mangrove ecosystem. Curr Sci 82:622–623

    CAS  Google Scholar 

  • Sarioglu OF, Suluyayla R, Tekinay T (2012) Heterotrophic ammonium removal by a novel hatchery isolate Acinetobacter calcoaceticus STB1. Int Biodeter Biodegrad 71:67–71

    Article  CAS  Google Scholar 

  • Sayavedra-Soto LA, Hommes NG, Russell SA, Arp DJ (1996) Induction of ammonia monooxygenase and hydroxylamine oxidoreductase mRNAs by ammonium in Nitrosomonas europaea. Mol Microbiol 20:541–548

    Article  CAS  PubMed  Google Scholar 

  • Schaechter M (2009) Encyclopedia of microbiology, 3rd edn. Elsevier, Amsterdam

  • Su JJ, Liu BY, Liu CY (2001) Comparison of aerobic denitrification under high oxygen atmosphere by Thiosphaera pantotropha ATCC 35512 and Pseudomonas stutzeri SU2 newly isolated from the activated sludge of a piggery wastewater treatment system. J Appl Microbiol 90:457–462

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Taylor SM, He Y, Zhao B, Huang J (2009) Heterotrophic ammonium removal characteristics of an aerobic heterotrophic nitrifying denitrifying bacterium, Providencia rettgeri YL. J Environ Sci 21:1336–1341

    Article  CAS  Google Scholar 

  • Us EPA (1993) Process design manual for nitrogen control. United States Environmental Protection Agency. Washington, DC

    Google Scholar 

  • Us EPA (2009) Draft 2009 Update of aquatic life ambient water quality criteria for ammonia in freshwater. United States Environmental Protection Agency. Washington, DC

    Google Scholar 

  • Ward BB (1996) Nitrification and ammonification in aquatic systems. Life Support Biosphere Sci: Int J Earth Space 3:25–29

    CAS  Google Scholar 

  • Wehrfritz JM, Reilly A, Spiro S, Richardson DJ (1993) Purification of hydroxylamine oxidase from Thiosphaera pantotropha, identification of electron acceptors that couple heterotrophic nitrification to aerobic denitrification. FEBS Lett 335:246–250

    Article  CAS  PubMed  Google Scholar 

  • Whitfield M (1974) The hydrolysis of ammonium ions in sea water—a theoretical study. J Mar Biol Assoc UK 54:565–580

    Article  CAS  Google Scholar 

  • WHO (1990) Ammonia Health and Safety Guide. World Health Organization, Geneva. online at: http://www.inchem.org/documents/hsg/hsg/hsg037.htm#SubSectionNumber:1.3.2

  • Winogradsky S (1890) Recherches sur les organismes de la nitrification. Ann Inst Pasteur (Paris) 4:213–231

    Google Scholar 

  • Witzel KP, Overbeck HJ (1979) Heterotrophic nitrification by Arthrobacter sp. (strain 9006) as influenced by different cultural conditions, growth state and acetate metabolism. Arch Microbiol 122:137–114

    Article  CAS  Google Scholar 

  • Yang XP, Wang SM, Zhang DW, Zhou LX (2011) Isolation and nitrogen removal characteristics of an aerobic heterotrophic nitrifying-denitrifying bacterium, Bacillus subtilis A1. Bioresour Technol 102:854–862

    Article  CAS  PubMed  Google Scholar 

  • Zhang WW, Sun L (2007) Cloning, characterization, and molecular application of a beta-agarase gene from Vibrio sp. strain V134. Appl Environ Microbiol 73:2825–2831

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang WW, Sun K, Cheng S, Sun L (2008) Characterization of DegQVh, a serine protease and a protective immunogen from a pathogenic Vibrio harveyi strain. Appl Environ Microbiol 74:6254–6262

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao B, He YL, Hughes J, Zhang XF (2010) Heterotrophic nitrogen removal by a newly isolated Acinetobacter calcoaceticus HNR. Bioresour Technol 101:5194–5200

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported financially by the Innovation Projects of the Chinese Academy of Sciences grant KZCX2-EW-206, the Doctoral Foundation of Shandong Province grant BS2011SW056, the National Natural Science Foundation of China (NSFC) grant 31200041, and the 100 Talents Program of the Chinese Academy of Sciences.

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Correspondence to Ling Xin Chen.

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Zhang, W.W., Andong, Z.Y., Zhang, M. et al. Isolation and characterization of a heterotrophic nitrifier Proteus mirabilis strain V7 and its potential application in NH4 +-N removal. Ann Microbiol 64, 1231–1238 (2014). https://doi.org/10.1007/s13213-013-0764-0

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  • DOI: https://doi.org/10.1007/s13213-013-0764-0

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