Skip to main content

Advertisement

SpringerLink
Log in

Detection of human fecal contamination by nifH gene quantification of marine waters in the coastal beaches of Rio de Janeiro, Brazil

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

Abstract

The identification of fecal pollution in aquatic ecosystems is one of the requirements to assess the possible risks to human health. In this report, physicochemical parameters, Escherichia coli enumeration and Methanobrevibacter smithii nifH gene quantification were conducted at 13 marine waters in the coastal beaches of Rio de Janeiro, Brazil. The pH, turbidity, dissolved oxygen, temperature, and conductivity, carried out by mobile equipment, revealed varied levels due to specific conditions of the beaches. The bioindicators’ enumerations were done by defined substrate method, conventional, and real-time PCR. Six marine beach sites (46 %) presenting E. coli levels in compliance with Brazilian water quality guidelines (<2500 MPN/100 mL) showed nifH gene between 5.7 × 109 to 9.5 × 1011 copies. L−1 revealing poor correlation between the two approaches. To our knowledge, this is the first inquiry in qPCR using nifH gene as a biomarker of human-specific sources of sewage pollution in marine waters in Brazil. In addition, our data suggests that alternative indicator nifH gene could be used, in combination with other markers, for source tracking studies to measure the quality of marine ecosystems thereby contributing to improved microbial risk assessment.

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

Similar content being viewed by others

References

  • Ahmed W, Sidhu JPS, Toze S (2012) Evaluation of the nifH gene marker of Methanobrevibacter smithii for the detection of sewage pollution in environmental waters in Southeast Queensland, Australia. Environmental science & technology 46(1):543–550

    Article  CAS  Google Scholar 

  • American Public Health Association–APHA; American Water Works Association–AWWA; Water Environment Federation–WEF (2012). Standard methods for the examination of water and wastewater. 22th ed. Washington DC.

  • Ballesté E, Bonjoch X, Belanche LA, Blanch AR (2010) Molecular indicators used in the development of predictive models for microbial source tracking. Appl Environ Microbiol 76(6):1789–1795

    Article  Google Scholar 

  • Bernhard AE, Goyard T, Simonich MT, Field KG (2003) Application of a rapid method for identifying fecal pollution sources in a multi-use estuary. Water Res 37:909–913

    Article  CAS  Google Scholar 

  • Bianco K, Barreto C, Oliveira SS, Pinto LH, Albano RM, Miranda CC, Clementino MM (2015) Fecal pollution source tracking in waters intended for human supply based on archaeal and bacterial genectic markers. J Water Health 13(4):985–995

    Article  Google Scholar 

  • Boehm AB, Ashbolt NJ, Colford JM, Dunbar LE, Fleming LE, Gold MA, Hansel JA, Hunter PR et al (2009) A sea change ahead for recreational water quality criteria. J Water Health 7:9–20

    Article  Google Scholar 

  • Clementino MM, Fernandes CC, Vieira RP, Cardoso AM, Polycarpo CR, Martins OB (2007) Archaeal diversity in naturally occurring and impacted environments from a tropical region. J Appl Microbiol 103(1):141–151

    Article  CAS  Google Scholar 

  • Cole D, Long SC, Sobsey MD (2003) Evaluation of Fþ RNA and DNA coliphages as source-specific indicators of fecal contamination in surface waters. Appl Environ Microbiol 69(11):6507–6514

    Article  CAS  Google Scholar 

  • Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlesfsen L, Sargent M, Gill SR, Nelson KE et al (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638

    Article  Google Scholar 

  • Fewtrell L, Kay D (2015) Recreational water and infection: a review of recent findings. Current Environmental Health Reports 2(1):85–94

    Article  Google Scholar 

  • Field KG, Samadpour M (2007) Fecal source tracking, the indicator paradigm, and managing water quality. Water Res 41(16):3517–3538

    Article  CAS  Google Scholar 

  • Foley SL, Lynne AM, Nayak R (2009) Molecular typing methodologies for microbial source tracking and epidemiological investigations of Gram-negative bacterial foodborne pathogens. Infect Genet Evol 9(4):430–440

    Article  CAS  Google Scholar 

  • Fong TT, Griffin DW, Lipp EK (2005) Molecular assays for targeting human and bovine enteric viruses in coastal waters and their application for library-independent source tracking. Appl Environ Microbiol 71(4):2070–2078

    Article  CAS  Google Scholar 

  • Gourmelon M, Caprais MP, Ségura R, Le Mennec C, Lozach S, Piriou JY, Rincé A (2007) Evaluation of two library-independent microbial source tracking methods to identify sources of fecal contamination in French estuaries. Appl Environ Microbiol 73(15):4857–4866

    Article  CAS  Google Scholar 

  • Harwood VJ, Staley C, Badgley BD, Borges K, Korajkic A (2014) Microbial source tracking markers for detection of fecal contamination in environmental waters: relationships between pathogens and human health outcomes. FEMS Microbiol Rev 38(1):1–40

    Article  CAS  Google Scholar 

  • Haugland RA, Siefring SC, Wymer LJ, Brenner KP, Dufour AP (2005) Comparison of Enterococcus measurements in freshwater at two recreational beaches by quantitative polymerase change reaction and membrane filter culture analysis. Water Res 39:559–568

    Article  CAS  Google Scholar 

  • Jannasch HW (1968) Competitive elimination of Enterobacteriaceae from seawater. Appl Microbiol 16:1616–1618

    CAS  Google Scholar 

  • Johnston C, Ufnar JA, Griffith JF, Gooch JA, Stewart JR (2010) A real-time qPCR assay for the detection of the nifH gene of Methanobrevibacter smithii, a potential indicator of sewage pollution. J Appl Microbiol 109(6):1946–1956

    Article  CAS  Google Scholar 

  • Lai MC, Lin CC, Yu PH, Huang YF, Chen SC (2004) Methanocalculus chunghsingenisis sp. Nov., isolated from an estuary and a marine fishpond in Taiwan. Int J Syst Evol Microbiol 54:183–118

    Article  CAS  Google Scholar 

  • Layton BA, Cao Y, Ebentier DL, Hanley K, Ballesté E, Brandão J, Byappanahalli M, Converse R, Farnleitner AH, Gentry-Shields J, Gidley ML, Gourmelon M, Lee CS, Lee J, Lozach S, Madi T, Meijer WG, Noble R, Peed L, Reischer GH, Rodrigues R, Rose JB, Schriewer A, Sinigalliano C, Srinivasan S, Stewart J, Werfhorst LC, Wang D, Whitman R, Wuertz S, Jay J, Holden PA, Boehm AB, Shanks O, Griffith JF (2013) Performance of human fecal anaerobe-associated PCR-based assays in a multi-laboratory method evaluation study. Water Res 47(Issue 18):6897–6908

    Article  CAS  Google Scholar 

  • Lebaron P, Cournoyer B, Lemarchand K, Nazaret S, Servais P (2015) Environmental and human pathogenic microorganisms. In: Environmental microbiology: fundamentals and applications. Springer, Netherlands, pp. 619–658

    Google Scholar 

  • McQuaig SM, Scott TM, Lukasik JO, Paul JH, Harwood VJ (2009) Quantification of human polyomaviruses JC virus and BK virus by TaqMan quantitative PCR and comparison to other water quality indicators in water and fecal samples. Appl Environ Microbiol 75:3379–3388

    Article  CAS  Google Scholar 

  • Ogram A, Sayler GS, Barkay T (1987) The extraction and purification of microbial DNA from sediments. J Microbiol Methods 7:57–66

    Article  CAS  Google Scholar 

  • Oliveira BSSD, Cunha ACD (2014) Correlation between water quality and precipitation variability in the southern state of Amapá. Rev Ambient Água 9(2):261–275

    Google Scholar 

  • Rasmussen R (2001) In: Meuer S, Wittwer C, Nakagawara K (eds) Quantification on the LightCycler. Springer-Verlag, Berlin, pp. 21–34

    Google Scholar 

  • Rozen Y, Belkin S (2001) Survival of enteric bacteria in seawater. FEMS Microbiol Rev 25(5):513–529

    Article  CAS  Google Scholar 

  • Santo Domingo JW, Bambic DG, Edge TA, Wuertz S (2007) Quo vadis source tracking? Towards a strategic framework for environmental monitoring of fecal pollution. Wat Res 41:3539–3552

    Article  CAS  Google Scholar 

  • Savichtcheva O, Okabe S (2006) Alternative indicators of fecal pollution: relations with pathogens and conventional indicators, current methodologies for direct pathogen monitoring and future application perspectives. Water Res 40:2463–2476

    Article  CAS  Google Scholar 

  • Schmiegelow, J. M. M. (2004). The Blue Planet: An Introduction Marine Science. Brazil.

  • Scott TM, Rose JB, Jenkins TM, Farrah SR, Luhasik J (2002) Microbial source tracking: current methodology and future directions. Appl Environ Microbiol 68:5796–5803

    Article  CAS  Google Scholar 

  • Scott TM, Jenkins TM, Lukasik J, Rose JB (2005) Potential use of a host associated molecular marker in Enterococcus faecium as an index of human fecal pollution. Environ Sci Technol 1(39):283–287

    Article  Google Scholar 

  • Shanks OC, Nietch C, Simonich M, Younger M, Reynolds D, Field KG (2006) Basin-wide analysis of the dynamics of fecal contamination and fecal source identification in fecal pollution source tracking in waters intended for human supply journal of water and health in Tillamook Bay, Oregon. Appl Environ Microbiol 72(8):5537–5546

    Article  CAS  Google Scholar 

  • Smalla K, Cresswell N, Mendonca-Hagler LC, Wolters A, van Elsas JD (1993) Rapid DNA extraction protocol from soil for polymerase chain reaction-mediated amplification. J Appl Bacteriol 74:78–85

    Article  CAS  Google Scholar 

  • Stewart-Pullaro J, Daugomah JW, Chestnut DE, Graves DA, Sobsey MD, Scott GI (2006) F+ RNA coliphage typing for microbial source tracking in surface waters. J Appl Microbiol 101(5):1015–1026

    Article  CAS  Google Scholar 

  • Stoeckel DM, Harwood VJ (2007) Performance, design, and analysis in microbial source tracking studies. Appl Environ Microbiol 73(8):2405–2415

    Article  CAS  Google Scholar 

  • Ufnar JA, Wang SY, Christiansen JM, Yampara-Iquise H, Carson CA, Ellender RD (2006) Detection of the nifH gene of Methanobrevibacter smithii: a potential tool to identify sewage pollution in recreational waters. J Appl Microbiol 101(1):44–52

    Article  CAS  Google Scholar 

  • Walters SP, Yamahara KM, Boehm AB (2009) Persistence of nucleic acid markers of health-relevant organisms in seawater microcosms. Water Res 43:4929–4939

    Article  CAS  Google Scholar 

  • Whitman RL, Ge Z, Nevers MB, Boehm AB, Chern EC, Haugland RA, White EM (2010) Relationship and variation of qPCR and culturable enterococci estimates in ambient surface waters are predictable. Environ Sci Technol 44:5049–5054

    Article  CAS  Google Scholar 

  • Wimalawansa SA, Wimalawansa SJ (2014) Impact of changing agricultural practices on human health: chronic kidney disease of multi-factorial origin in Sri Lanka. Wudpecker J Agric Res 3(5):110–124

    Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the Genome Sequencing Core-PDTIS/FIOCRUZ. This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), and INCQS/FIOCRUZ.

Author information

Authors and Affiliations

  1. Fundação Oswaldo Cruz, Instituto Nacional de Controle de Qualidade em Saúde, Avenida Brasil, 4365, Maguinhos, Rio de Janeiro, Rio de Janeiro, Brazil

    Samara Sant’Anna Oliveira, Kayo Bianco, Camila Barreto & Maysa Mandetta Clementino

  2. Universidade Federal do Rio de Janeiro, Instituto de Bioquímica Médica, Ilha do Fundão, Cidade Universitária, Rio de Janeiro, Rio de Janeiro, Brazil

    Marcos Henrique Ferreira Sorgine

  3. Instituto de Biologia Roberto Alcântara Gomes, Universidade do Estado do Rio de Janeiro, Avenida 28 de setembro, 87, Vila Isabel, Rio de Janeiro, Rio de Janeiro, Brazil

    Leonardo Henriques Pinto & Rodolpho Mattos Albano

  4. Fundação Centro Universitário Estadual da Zona Oeste, UEZO, Av. Manuel Caldeira de Alvarenga, 1203, Campo Grande, Rio de Janeiro, Rio de Janeiro, Brazil

    Alexander Machado Cardoso

Authors
  1. Samara Sant’Anna Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marcos Henrique Ferreira Sorgine
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kayo Bianco
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leonardo Henriques Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Camila Barreto
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rodolpho Mattos Albano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alexander Machado Cardoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maysa Mandetta Clementino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maysa Mandetta Clementino.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oliveira, S.S., Sorgine, M.H.F., Bianco, K. et al. Detection of human fecal contamination by nifH gene quantification of marine waters in the coastal beaches of Rio de Janeiro, Brazil. Environ Sci Pollut Res 23, 25210–25217 (2016). https://doi.org/10.1007/s11356-016-7737-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7737-3

Keywords

Search

Navigation