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First report of predation of Giardia sp. cysts by ciliated protozoa and confirmation of predation of Cryptosporidium spp. oocysts by ciliate species

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Abstract

Ciliated protozoa are important components of the microbial food web in various habitats, especially aquatic environments. These organisms are useful bioindicators for both environmental quality assessment and the wastewater purification process. The pathogenic parasitic protozoan species Giardia and Cryptosporidium represent a significant concern for human health, being responsible for numerous disease outbreaks worldwide. The predation of cysts and oocysts in 15 ciliate species from water and sewage samples collected in Campinas, São Paulo, Brazil were verified under laboratory conditions. The ciliated protozoan species were selected based on their mode of nutrition, and only bacterivorous and suspension-feeders were considered for the experiments. The species Blepharisma sinuosum, Euplotes aediculatus, Sterkiella cavicola, Oxytricha granulifera, Vorticella infusionum, Spirostomum minus, and Stentor coeruleus ingested cysts and oocysts, the resistance forms of Giardia spp. and Cryptosporidium spp., respectively. This is the first time that the ingestion of Giardia cysts by ciliated protozoa has been reported. These findings may contribute to a better understanding of the biological removal of these pathogens from aquatic environments.

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References

  • Bagatini IL, Spínola ALG, Peres BM, Mansano AS, Rodrigues MAA, Batalha MA, Lucca JV, Godinho MJL, Tundisi TM, Seleghim MHR (2013) Protozooplâncton e suas relações com as condições ambientais em 13 corpos d’água da bacia do Rio Mogi-Guaçu – SP, Brasil. Biota Neotrop 13:152–163 (In Portuguese)

    Article  Google Scholar 

  • Baldursson S, Karanis P (2011) Waterborne transmission of protozoan parasites: review of worldwide outbreaks—an update 2004–2010. Water Res 45:6603–6614

    Article  CAS  Google Scholar 

  • Berger H (1999) Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biologicae. Springer Science+Business Media Dordrecht. Kluwer Academic Publishers

  • Berger H (2006) Monograph of the Urostyloidea (Ciliophora, Hypotrichia). Monographiae Biologicae. Springer Science+Business Media Dordrecht. Kluwer Academic Publishers

  • Betancourt WQ, Duarte DC, Vásquez RC, Gurian PL (2014) Cryptosporidium and Giardia in tropical recreational marine waters contaminated with domestic sewage: estimation of bathing-associated disease risks. Mar Pollut Bull 85(1):268–273

    Article  CAS  Google Scholar 

  • Bichai F, Payment P, Barbeau B (2008) Protection of waterborne pathogens by higher organisms in drinking water: a review. Can J Microbiol 54:509–524

    Article  CAS  Google Scholar 

  • Bichai F, Barbeau B, Dullemont, Y, Hijnen W (2010). Role of predation by zooplankton in transport and fate of protozoan (oo)cysts in granular activated carbon filtration. Water Quality Technology Conference and Exposition, 197–209

  • Bonatti T R, Branco N, Felisardo G, Siqueira-Castro ICV, Franco RMB (2014) Monitoring of Giadia spp. and Cryptosporidium spp. and biodiversity of ciliated protozoa in surface water and sediment samples of the Atibaia River, Campinas, São Paulo, Brazil. In: International Congress of Parasitology, ICOPA XIII, Mexico

  • Boscaro V, Vannini C, Fokin SI, Verni F, Petroni G (2012) Characterization of “Candidatus Nebulobacter yamunensis” from the cytoplasm of Euplotes aediculatus (Ciliophora, Spirotrichea) and emended description of the family Francisellaceae. Syst Appl Microbiol 35:432–440

    Article  CAS  Google Scholar 

  • Brookes JD, Antenucci J, Hipsey M, Burch MD, Ashbolt NJ, Ferguson C (2004) Fate and transport of pathogens in lakes and reservoirs. Environ Int 30(5):741–759

    Article  Google Scholar 

  • Cantusio Neto R, Santos LU, Franco RM (2006) Evaluation of activated sludge treatment and the efficiency of the disinfection of Giardia species cysts and Cryptosporidium oocysts by UV at a sludge treatment plant in Campinas, south-east Brazil. Water Sci Technol 54:89–94

    Article  CAS  Google Scholar 

  • Cantusio Neto R, Santos LU, Sato MIZ, Franco RMB (2010) Cryptosporidium spp. and Giardia spp. in surface water supply of Campinas, Southeast Brazil. Water Sci Technol 62:217–222

    Article  Google Scholar 

  • Díez B, Pedrós-Alió C, Massana R (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Environ Microbiol 67:2932–2941

    Article  Google Scholar 

  • Dopheide A, Lear G, Stott R, Lewis G (2009) Relative diversity and community structure of ciliates in stream biofilms according to molecular and microscopy methods. Appl Environ Microbiol 75:5261–5272

    Article  CAS  Google Scholar 

  • Dopheide A, Lear G, Stott R, Lewis G (2011) Preferential feeding by the Ciliates Chilodonella and Tetrahymena spp. and effects of these protozoa on bacterial biofilm structure and composition. Appl Environ Microbiol 4564–4572

  • Fayer R, Trout JM, Walsh E, Cole R (2000) Rotifers ingest oocysts of Cryptosporidium parvum. J Eukaryot Microbiol 47(2):161–163

    Article  CAS  Google Scholar 

  • Fenchel T (1980) Suspension feeding ciliated protozoa: feeding rates and their ecological significance. Microb Ecol 6:13–25

    Article  CAS  Google Scholar 

  • Finlay BJ, Fenchel T (1996) Ecology: role of ciliates in the natural environment. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer Verlag, Stuttgart, pp 417–440

    Google Scholar 

  • Foissner W (1992) Estimating the species richness of soil protozoa using the “non-flooded petri dish method”. In: Lee JJ, Soldo AT (eds) Protocols in protozoology. Allen Press, Lawrence, pp B10.1–B10.2

    Google Scholar 

  • Foissner W, Berger H (1996) A user friendly guide to ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes and waste water, with notes in their ecology. Freshw Biol 35:375–482

    Google Scholar 

  • Foissner W, Blatterer H, Berger H and Kohmann F (1991) Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems – Band I: Cyrtophorida, Oligotrichida, Hypotrichia, Colpodea. Informationsberichte des Bayer. Landesamtes für Wasserwirtschaft, 1/91, 478p

  • Foissner W, Berger H and Kohmann F (1992) Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems – Band II: Peritrichia, Heterotrichida, Odontostomatida. Informationsberichte des Bayer. Landesamtes für Wasserwirtschaft, 5/92, 502p

  • Franco RMB, Rocha-Eberhardt R, Cantusio Neto R (2001) Occurrence of Cryptosporidium oocysts and Giardia cysts in raw water from the Atibaia River, Campinas, Brazil. Rev Inst Med Trop Sao Paulo 43:109–111

    Article  CAS  Google Scholar 

  • Greinert-Goulart JA (2013) Estudo da remoção de cistos de Giardia spp. e oocistos de Cryptosporidium spp. e caracterização da microfauna em estações de tratamento de esgoto: instrumentos de avaliação e controle do processo. Thesis of Doctorate, University of Campinas

  • Hausmann K (2002) Food acquisition, food ingestion and food digestion by protists. Jpn J Protozool 35:85–95

    Google Scholar 

  • Huamanchay O, Genzlinger L, Iglesias M, Ortega YR (2004) Ingestion of Cryptosporidium oocysts by Caenorhabditis elegans. J Parasitol 90(5):1176–1178

    Article  Google Scholar 

  • Hunter PR, Thompson RCA (2005) The zoonotic transmission of Giardia and Cryptosporidium. Int J Parasitol 35:1181–1190

    Article  Google Scholar 

  • King BJ, Monis PT, Keegan AR, Harvey K, Saint C (2007) Investigation of the survival of Cryptosporidium in environmental waters. Cooperative Research Centre for Water Quality and Treatment, Salisbury

    Google Scholar 

  • Kotloff KL, Blackwelde WC, Nasrin D, Nataro JP et al (2012) The Global Enteric Multicenter Study (GEMS) of diarrheal disease in infants and young children in developing countries: epidemiologic and clinical methods of the case/control study. Clin Infect Dis 55:S232–S245

    Article  Google Scholar 

  • Lynn D (2008) The ciliate protozoa. Characterization, classification and guide to the literature, 3rd edn. Pergamon Press, New York

    Google Scholar 

  • Lynn DH, Small EB (2002) Phylum Ciliophora. In: LEE JJ, Bradbury PC, Leedale GF (eds) An illustrated guide to the protozoa. Society of Protozoologists, Lawrence, pp 371–656

    Google Scholar 

  • Méndez-Hermida F, Gómez-Couso H, Ares-Mazás E (2007) Possible involvement of Artemia as live diet in the transmission of cryptosporidiosis in cultured fish. Parasitol Res 101(3):823–827

    Article  Google Scholar 

  • Monis P, King B, Keegan A (2014) Removal and inactivation of Cryptosporidium from water. In: Cacciò SM, Widmer G (eds) Cryptosporidium: parasite and disease. Springer-Verlag, Wien

    Google Scholar 

  • Montagnes DJS, Barbosa AB, Boenigk J, Davidson K, Jürgens K, Macek MF, Parry JD, Roberts EC, Šimek K (2008) Selective feeding behaviour of key free-living protists: avenues for continued study. Aquat Microb Ecol 53:83–98

    Article  Google Scholar 

  • Nawrot D, Mieczan T (2012) Co-occurrence of psammonic ciliates and rotifers in poor eutrophic lake (Łęczna-Włodawa Lakeland). Teka Kom Ochr Kszt Środ Przyr – OL PAN 9:125–133

    Google Scholar 

  • Nawrot D, Mieczan T (2014) Ciliates vs. another components of microbial loop in the psammolittoral zone: horizontal distribution. Turk J Zool 38:168–178

    Article  CAS  Google Scholar 

  • Radek R, Hausmann K (1996) Phagotrophy of ciliates. In: Hausmann K, Bradbury PC (eds) Ciliates: cells as organisms. Gustav Fischer, Stuttgart, pp 197–219

    Google Scholar 

  • SANASA (Sociedade de Abastecimento de Água e Saneamento). Available in <http://www.sanasa.com.br/noticias/not_con3.asp?par_nrod=567&flag=TA> Access in October 2015

  • Sato MIZ, Galvani AT, Padula JA, Nardocci AC, Lauretto MS, Razzolini MTP, Hachich EM (2013) Assessing the infection risk of Giardia and Cryptosporidium in public drinking water delivered by surface water systems in Sao Paulo State. Braz Sci Total Environ 442:389–396

    Article  CAS  Google Scholar 

  • Sherr E, Sherr BF (2002) Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek 81:293–308

    Article  CAS  Google Scholar 

  • Sigee DC (2005) Grazing activities in the freshwater environment: the role protozoa and invertebrates. Chapter 9. In: Freshwater microbiology: biodiversity and dynamic interactions of microorganisms in the aquatic environment, pp 401–441

  • Stott R, May E, Matsushita E, Warren A (2001) Protozoan predation as a mechanism for the removal of Cryptosporidium oocysts from wastewaters in constructed wetlands. Water Sci Technol 44:191–198

    CAS  Google Scholar 

  • Stott R, May E, Ramirez E, Warren A (2003) Predation of Cryptosporidium oocysts by protozoa and rotifers: implications for water quality and public health. Water Sci Technol 47:77–83

    CAS  Google Scholar 

  • Strom SL, Loukos H (1998) Selective feeding by protozoa: model and experimental behaviors and their consequences for population stability. J Plankton Res 20:831–846

    Article  Google Scholar 

  • Swaffer BA, Vial HM, King BJ, Daly R, Frizenschaf J, Monis PT (2014) Investigating source water Cryptosporidium concentration, species and infectivity rates during rainfall-runoff in a multi-use catchment. Water Res 67:310–320

    Article  CAS  Google Scholar 

  • Vaerewijck MJM, Sabbe K, Baré J et al (2011) Occurrence and diversity of free-living protozoa on butterhead lettuce. Int J Food Microbiol 147(2):105–111

    Article  Google Scholar 

  • Verity PG (1991) Feeding in planktonic protozoans: evidence for non-random acquisition of prey. J Eukaryot Microbiol 38(1):69–76

    Google Scholar 

  • Wilks SA, Sleigh MA (1998) Grazing rates in Euplotes mutabilis: relationship between particle size and concentration. Microb Ecol 36:165–174

    Article  Google Scholar 

  • Yamashiro S, Foco M, Silva G A, Bonatti TR, Nour EAA, Siqueira-Castro ICV, Franco RMB (2014) Removal of Giardia spp. cysts and Cryptosporidium spp. oocysts and characterization of microfauna from a treatment system employing anaerobic filter followed by Biofilter Submerged Aerated applied to sanitary sewage receiving hospital effluent. In: Congresso da Sociedade Paulista de Parasitologia, São Carlos

  • Zhou K, Xu M, Liu B, Cao H (2008) Characteristics of microfauna and their relationships with the performance of an activated sludge plant in China. J Environ Sci 20:482–486

    Article  CAS  Google Scholar 

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Acknowledgments

We would like to thank the São Paulo Research Foundation (process numbers 2010/16222-4 and 2011/50244­8) and the National Council for the Improvement of Higher Education (CAPES) for supporting this work.

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Authors and Affiliations

  1. Protozoology Laboratory, Biology Institute, University of Campinas (UNICAMP), Campinas, São Paulo, Brazil

    Isabel Cristina Vidal Siqueira-Castro, Juliane Araújo Greinert-Goulart, Tais Rondello Bonatti, Sandra Yamashiro & Regina Maura Bueno Franco

  2. Cidade Universitária Zeferino Vaz, Rua Monteiro Lobato 255, CEP 13.083-862, Campinas, SP, Brazil

    Isabel Cristina Vidal Siqueira-Castro

  3. Parasitology Laboratory, Regional University of Blumenau (FURB), Blumenau, SC, Brazil

    Juliane Araújo Greinert-Goulart

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  1. Isabel Cristina Vidal Siqueira-Castro
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  5. Regina Maura Bueno Franco
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Correspondence to Isabel Cristina Vidal Siqueira-Castro.

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Responsible editor: Philippe Garrigues

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Siqueira-Castro, I.C.V., Greinert-Goulart, J.A., Bonatti, T.R. et al. First report of predation of Giardia sp. cysts by ciliated protozoa and confirmation of predation of Cryptosporidium spp. oocysts by ciliate species. Environ Sci Pollut Res 23, 11357–11362 (2016). https://doi.org/10.1007/s11356-016-6689-y

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