Abstract
Five human-specific markers were detected in 59–74% of 27 human fecal-source samples collected in Yamanashi Prefecture, Japan. Similarly, potential human-specific markers, crAssphage, pepper mild mottle virus (PMMoV), and tobacco mosaic virus were detected in 96–100% of samples, with crAssphage showing the maximum concentration of 12.03 log copies/L. However, these markers were detected in 100% (3/3) of pig fecal-source samples, suggesting their applicability as general fecal pollution markers. Microbial source tracking analysis demonstrated that the rivers are contaminated by human and pig fecal sources. CrAssphage showed higher marker concentrations in river water samples than PMMoV, suggesting the preference of crAssphage to PMMoV as a marker of fecal pollution.
References
Ahmed, W., & Harwood, V. J. (2017). Human and animal enteric viral markers for tracking the sources of faecal pollution. In J. B. Rose & B. Jiménez-Cisneros (Eds.), Global water pathogen project. http://www.waterpathogens.org (A. Farnleitner, and A. Blanch (eds) Part 2 Indicators and Microbial Source Tracking Markers). https://doi.org/10.14321/waterpathogens.8.
Ahmed, W., Lobos, A., Senkbeil, J., Peraud, J., Gallard, J., & Harwood, V. J. (2018). Evaluation of the novel crAssphage marker for sewage pollution tracking in storm drain outfalls in Tampa, Florida. Water Research,131, 142–150. https://doi.org/10.1016/j.watres.2017.12.011.
Balique, F., Colson, P., Barry, A. O., Nappez, C., Ferretti, A., Al Moussawi, K., et al. (2013). Tobacco mosaic virus in the lungs of mice following intra-tracheal inoculation. PLoS ONE,8, 1–12. https://doi.org/10.1371/journal.pone.0054993.
Balleste, E., Bonjoch, X., Belanche, L. A., & Blanch, A. R. (2010). Molecular indicators used in the development of predictive models for microbial source tracking. Applied and Environmental Microbiology,76(6), 1789–1795. https://doi.org/10.1128/AEM.02350-09.
Garcia-Aljaro, C., Balleste, E., Muniesa, M., & Jofre, J. (2017). Determination of crAssphage in water samples and applicability for tracking human fecal pollution. Microbial Biotechnology,10, 1775–1780. https://doi.org/10.1111/1751-7915.12841.
Gawler, A. H., Beecher, J. E., Brandao, J., Carroll, N. M., Falcao, L., Gourmelon, M., et al. (2007). Validation of host-specific Bacteriodales 16S rRNA genes as markers to determine the origin of faecal pollution in Atlantic Rim countries of the European Union. Water Research,41(16), 3780–3784. https://doi.org/10.1016/j.watres.2007.01.028.
Hamza, I. A., Jurzik, L., Uberla, K., & Wilhelm, M. (2011). Evaluation of pepper mild mottle virus, human picobirnavirus and Torque teno virus as indicators of fecal contamination in river water. Water Research,45(3), 1358–1368. https://doi.org/10.1016/j.watres.2010.10.021.
Haramoto, E., Katayama, H., Asami, M., & Akiba, M. (2012). Development of a novel method for simultaneous concentration of viruses and protozoa from a single water sample. Journal of Virological Methods,182, 62–69. https://doi.org/10.1016/j.jviromet.2012.03.011.
Haramoto, E., Kitajima, M., Hata, A., Torrey, J. R., Masago, Y., Sano, D., et al. (2018). A review on recent progress in the detection methods and prevalence of human enteric viruses in water. Water Research,135, 168–186. https://doi.org/10.1016/j.watres.-2018.02.004.
Haramoto, E., Kitajima, M., Kishida, N., Konno, Y., Katayama, H., Asami, M., et al. (2013). Occurrence of pepper mild mottle virus in drinking water sources in Japan. Applied and Environmental Microbiology,79(23), 7413–7418. https://doi.org/10.1128/AEM.02354-13.
Haramoto, E., & Osada, R. (2018). Assessment and application of host-specific Bacteroidales genetic markers for microbial source tracking of river water in Japan. PLoS ONE,13(11), e0207727. https://doi.org/10.1371/journal.pone.0207727.
Haramoto, E., Yamada, K., & Nishida, K. (2011). Prevalence of protozoa, viruses, coliphages and indicator bacteria in groundwater and river water in the Kathmandu Valley, Nepal. Transaction of Royal Society of Tropical Medicine and Hygiene,105(12), 711–716. https://doi.org/10.1016/j.trstmh.2011.08.004.
Heim, A., Ebnet, C., Harste, G., & Pring-Åkerblom, P. (2003). Rapid and quantitative detection of human adenovirus DNA by real-time PCR. Journal of Medical Virology,70(2), 228–239. https://doi.org/10.1002/jmv.10382.
Hundesa, A., Bofill-Mas, S., Maluquer de Motes, C., Rodriguez-Manzano, J., Bach, A., Casas, M., et al. (2010). Development of a quantitative PCR assay for the quantitation of bovine polyomavirus as a microbial source-tracking tool. Journal of Virological Methods,163, 385–389. https://doi.org/10.1016/j.jviromet.2009.10.029.
Hundesa, A., de Motes, C. M., Albinana-Gimenez, N., Rodriguez-Manzano, J., Biofill-Mas, S., Sunen, E., et al. (2009). Development of a qPCR assay for the quantification of porcine adenoviruses as an MST tool for swine fecal contamination in the environment. Journal of Virological Methods,158(1–2), 130–135. https://doi.org/10.1016/j.jviromet.2009.02.006.
Jimenez-Clavero, M. A., Fernadez, C., Ortiz, J. A., Pro, J., Carbonell, G., Tarazona, J. V., et al. (2003). Teschoviruses as indicators of porcine fecal contamination of surface water. Applied and Environmental Microbiology,69, 6311–6315. https://doi.org/10.1128/aem.69.10.6311-6315.2003.
Kageyama, T., Kojima, S., Shinohara, M., Uchida, K., Fukushi, S., Hoshino, F. B., et al. (2003). Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. Journal of Clinical Microbiology,41, 1548–1557. https://doi.org/10.1128/JCM.41.4.1548-1557.2003.
Kitajima, M., Hata, A., Yamashita, T., Haramoto, E., Minagawa, H., & Katayama, H. (2013). Development of a reverse transcription-quantitative PCR system for detection and genotyping of aichi viruses in clinical and environmental samples. Applied and Environmental Microbiology,79(13), 3952–3958. https://doi.org/10.1128/AEM.00820-13.
Kitajima, M., Sassi, H. P., & Torrey, J. R. (2018). Pepper mild mottle virus as a water quality indicator. NPJ Clean Water. https://doi.org/10.1038/s41545-018-0019-5.
Kongprajug, A., Mongkolsuk, S., & Sirikanchana, K. (2019). CrAssphage as a potential human sewage marker for microbial source tracking in Southeast Asia. Environmental Science & Technology Letters,6(3), 159–164. https://doi.org/10.1021/acs.estlett.9b00041.
Kuroda, K., Nakada, N., Hanamoto, S., Inaba, M., Katayama, H., Do, A. T., et al. (2014). Pepper mild mottle virus as an indicator and a tracer of fecal pollution in water environments: Comparative evaluation with wastewater-tracer pharmaceuticals in Hanoi, Vietnam. Science of the Total Environment,506–507, 287–298. https://doi.org/10.1016/j.scitotenv.2014.11.021.
Malla, B., Ghaju Shrestha, R., Tandukar, S., Sherchand, J. B., & Haramoto, E. (2019). Performance evaluation of human-specific viral markers and application of pepper mild mottle virus and CrAssphage to environmental water samples as fecal pollution markers in the Kathmandu Valley, Nepal. Food and Environmental Virology. https://doi.org/10.1007/s12560-019-09389-x.
McQuaig, S. M., Scott, T. M., Lukasik, J. O., Paul, J. H., & Harwood, V. J. (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. Applied and Environmental Microbiology,75, 3379–3388. https://doi.org/10.1128/AEM.02302-08.
Nakamura, K., Saga, Y., Iwai, M., Obara, M., Horimoto, E., Hasegawa, S., et al. (2010). Frequent detection of noroviruses and sapoviruses in swine and high genetic diversity of porcine sapovirus in Japan during fiscal year 2008. Journal of Clinical Microbiology,48, 1215–1222.
Pal, A., Sirota, L., Maudru, T., Peden, K., & Lewis, A. M. (2006). Realtime, quantitative PCR assays for the detection of virus-specific DNA in samples with mixed populations of polyomaviruses. Journal of Virological Methods,135(1), 32–42. https://doi.org/10.1016/j.jviromet.2006.01.018.
Reischer, G. H., Ebdon, J. E., Bauer, J. M., Schuster, N., Ahmed, W., Åström, J., et al. (2013). Performance characteristics of qPCR assays targeting human- and ruminant-associated Bacteroidetes for microbial source tracking across sixteen countries on six continents. Environmental Science and Technology,47, 8548–8556. https://doi.org/10.1021/es304367t.
Rosario, K., Symonds, E. M., Sinigalliano, C., Stewart, J., & Breitbart, M. (2009). Pepper mild mottle virus as an indicator of fecal pollution. Applied and Environmental Microbiology,75(22), 7261–7267. https://doi.org/10.1128/AEM.00410-09.
Rusinol, M., Fernandez-Cassi, X., Hundesa, A., Vieira, C., Kern, A., Eriksson, I., et al. (2014). Application of human and animal viral microbial source tracking tools in fresh and marine waters from five different geographical areas. Water Research,59, 119–129. https://doi.org/10.1016/j.watres.2014.04.013.
Stachler, E., Akyon, B., de Carvalho, N. A., Ference, C., & Bibby, K. (2018). Correlation of crAssphage qPCR Markers with culturable and molecular indicators of human fecal pollution in an impacted urban watershed. Environmental Science and Technology,52(13), 7505–7512. https://doi.org/10.1021/acs.est.8b00638.
Stachler, E., & Bibby, K. (2014). Metagenomic evaluation of the highly abundant human gut bacteriophage crAssphage for source tracking of human fecal pollution. Environmental Science & Technology Letter,1, 405–409. https://doi.org/10.1021/ez500266s.
Stachler, E., Kelty, C., Sivaganesan, M., Li, X., Bibby, K., & Shanks, O. C. (2017). Quantitative crAssphage PCR assays for human fecal pollution measurement. Environmental Science and Technology,51(16), 9146–9154. https://doi.org/10.1021/acs.est.7b02703.
Wolf, S., Hewitt, J., & Greening, G. E. (2010). Viral multiplex quantitative PCR assays for tracking sources of fecal contamination. Applied and Environmental Microbiology,76, 1388–1394. https://doi.org/10.1128/AEM.02249-09.
Wong, K., & Xagoraraki, I. (2011). Evaluating the prevalence and genetic diversity of adenovirus and polyomavirus in bovine waste for microbial source tracking. Applied Microbiology and Biotechnology,90, 1521–1526. https://doi.org/10.1007/s00253-011-3156-z.
Yahya, M., Blanch, A. R., Meijer, W. G., Antoniou, K., Hmaied, F., & Balleste, E. (2017). Comparison of the performance of different microbial source tracking markers among European and North African Regions. Journal of Environmental Quality,46, 760–766. https://doi.org/10.2134/jeq2016.11.0432.
Zhang, T., Breitbart, M., Lee, W. H., Run, J. Q., Wei, C. L., Soh, S. W., et al. (2006). RNA viral community in human feces: Prevalence of plant pathogenic viruses. PLoS Biology,4(1), 0108–0118. https://doi.org/10.1371/journal.pbio.0040003.
Acknowledgements
This study was financially supported by the Environmental Restoration and Conservation Agency of Japan through the Environment Research and Technology Development Fund (Grant No. 5-1603), the Japan Society for the Promotion of Science (JSPS) through Grant-in-Aid for Scientific Research (B) (Grant No. JP17H03332), and the River Foundation (Grant No. 26-1263-011). The authors acknowledge Mr. Rui Osada, Ms. Ruriko Ito, Ms. Kotomi Furukawa, Ms. Sayaka Sugiyama, Mr. Masaaki Ito, Mr. Kosei Koga, Mr. Toshiki Amemiya, Mr. Ryo Koshiishi, and Mr. Kazuki Yamamoto (University of Yamanashi, Japan) for their support in water sampling and/or laboratory analysis.
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Malla, B., Makise, K., Nakaya, K. et al. Evaluation of Human- and Animal-Specific Viral Markers and Application of CrAssphage, Pepper Mild Mottle Virus, and Tobacco Mosaic Virus as Potential Fecal Pollution Markers to River Water in Japan. Food Environ Virol 11, 446–452 (2019). https://doi.org/10.1007/s12560-019-09398-w
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DOI: https://doi.org/10.1007/s12560-019-09398-w