Abstract
Introduction
Saline groundwater desalination has recently emerged as an alternative source of irrigation water in arid and semiarid regions due to the gradual reduction in the quantity and quality of conventional water resources for agricultural use. In Fuerteventura Island (Spain), an extremely arid territory in the European Union, brackish water desalination is one of the few available water sources for agricultural production. Very little research has been conducted on the microbiological quality of this water mainly used for irrigation of vegetable crops. Free-living amoebae (FLA) are widely distributed protozoa in the environment and have been isolated from many environmental sources such as dust, soil and water. Among the pathogenic genera included in this group, Acanthamoeba spp., Naegleria fowleri and Balamuthia mandrillaris have been reported to be causative agents of lethal encephalitis, disseminated infections and keratitis. Particularly, Naegleria fowleri is a pathogenic FLA species which causes primary amoebic meningoencephalitis (PAM).
Materials and Methods
In the present study, the presence of pathogenic FLA strains on desalinated brackish water samples for irrigation has been evaluated during 7 months.
Results
From the analysed samples, only one was positive for Naegleria australiensis. This is the first report of Naegleria spp. in desalinated brackish water for irrigation in Spain.
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References
Abedkhojasteh H, Niyyati M, Rahimi F, Heidari M, Farnia S, Rezaeian M (2013) First report of Hartmannella keratitis in a cosmetic soft contact lens wearer in Iran. Iran J Parasitol 8(3):481–485
Avni Y, Porat N, Plakht J, Avni G (2006) Geomorphic changes leading to natural desertification versus anthropogenic land conservation in an arid environment, the Negev Highlands, Israel. Geomorphology 82:177–200. https://doi.org/10.1016/j.geomorph.2006.05.002
Booton GC, Visvesvara GS, Byers TJ, Kelly DJ, Fuerst PA (2005) Identification and distribution of Acanthamoeba species genotypes associated with non-keratitis infections. J Clin Microbiol 43(4):1689–1693. https://doi.org/10.1128/JCM.43.4.1689-1693.2005
Centeno M, Rivera F, Cerva L, Tsutsumi V, Gallegos E, Calderón A, Ortiz R, Bonilla P, Ramírez E, Suárez G (1996) Hartmannella vermiformis isolated from the cerebrospinal fluid of a young male patient with meningoencephalitis and bronchopneumonia. Arch Med Res 27(4):579–586 PMID: 8987199
De Jonckheere JF (2002) A century of research on amoeboflagellate genus Naegleria. Acta Protozool 41(4):309–342
De Jonckheere JF (2011) Origin and evolution of the worldwide distributed pathogenic amoeboflagellate Naegleria fowleri. Infect Genet Evol 11(7):1520–1528
De Jonckheere JF (2014) What do we know by now about the genus Naegleria? Exp Parasitol 145(Suppl):S2–S9. https://doi.org/10.1016/j.exppara.2014.07.011
Díaz FJ, Tejedor M, Jiménez C, Dahlgren RA (2011) Soil fertility dynamics in runoff-capture agriculture, Canary Islands, Spain. Agric Ecosyst Environ 144(1):253–261. https://doi.org/10.1016/j.agee.2011.08.021
Díaz FJ, Tejedor M, Jiménez C, Grattan SR, Dorta M, Hernándeza JM (2013) The imprint of desalinated seawater on recycled wastewater: consequences for irrigation in Lanzarote Island, Spain. Agric Water Manag 116:62–72. https://doi.org/10.1016/j.agwat.2012.10.011
Díaz FJ, Grattan SR, Reyes JA, de la Roza-Delgado B, Benes SE, Jiménez C, Dorta M, Tejedor M (2018) Using saline soil and marginal quality water to produce alfalfa in aridclimates. Agric Water Manag 199:11–21. https://doi.org/10.1016/j.agwat.2017.12.003
Dorta-Santos M, Tejedor M, Jiménez C, Hernández-Moreno JM, Díaz FJ (2016) Using marginal quality water for an energy crop in arid regions: effect of salinity and boron distribution patterns. Agric Water Manag 171:142–152. https://doi.org/10.1016/j.agwat.2016.04.005
Dyková I, Kyselova I, Peckova H, Obornik M, Lukes J (2001) Identity of Naegleria strains isolated from organs of freshwater fishes. Dis Aquat Org 46:115–121. https://doi.org/10.3354/dao046115
González-Robles A, Castañón G, Cristóbal-Ramos AR, Hernández-Ramírez VI, Omaña-Molina M, Martínez-Palomo A (2007) Cell surface differences of Naegleria fowleri and Naegleria lovaniensis exposed with surface markers. Exp Parasitol 117(4):399–404. https://doi.org/10.1016/j.exppara.2007.05.007
Helmreich B, Horn H (2009) Opportunities in rainwater harvesting. Desalination 248:118–124. https://doi.org/10.1016/j.desal.2008.05.046
Lorenzo-Morales J, Ortega-Rivas A, Foronda P, Martínez E, Valladares B (2005) Isolation and identification of pathogenic Acanthamoeba strains in Tenerife, Canary Islands, Spain from water sources. Parasitol Res 95:273–277. https://doi.org/10.1007/s00436-005-1301-2
Lorenzo-Morales J, Monteverde-Miranda CA, Jiménez C, Tejedor ML, Valladares B, Ortega-Rivas A (2005) Evaluation of Acanthamoeba isolates from environmental sources in Tenerife, Canary Islands, Spain. Ann Agric Environ Med 12:233–236
Lorenzo-Morales J, Martínez-Carretero E, Batista N, Álvarez-Marín J, Bahaya Y, Walochnik J, Valladares B (2007) Early diagnosis of amoebic keratitis due to a mixed infection with Acanthamoeba and Hartmannella. Parasitol Res 102(1):167–169 PMID: 17899193
Marciano-Cabral FM, Fulford DE (1986) Cytopathology of pathogenic and nonpathogenic Naegleria species for cultured rat neuroblastoma cells. Appl Environ Microbiol 51:1133–1137 (PMCID: PMC239024)
Marciano-Cabral F, Jamerson M, Kaneshiro ES (2010) Free-living amoebae, Legionella and Mycobacterium in tap water supplied by a municipal drinking water utility in the USA. J Water Health 8(1):71–82. https://doi.org/10.2166/wh.2009.129
Martínez-Beltrán J., Koo-Oshima S. 2006. Water desalination for agricultural applications, Water Resources, Development and Management Service Land and Water Development Division. Food and Agriculture Organization of the United NationsRome, Italy. In: proceedings of the FAO Expert Consultation on Water Desalination for Agricultural Applications 26–27 April 2004, Rome
Niyyati M, Lorenzo-Morales J, Rezaeian M, Martin-Navarro CM, Haghi AM, Maciver SK, Valladares B (2009) Isolation of Balamuthia mandrillaris from urban dust, free of known infectious involvement. Parasitol Res 106(1):279–281. https://doi.org/10.1007/s00436-009-1592-9
Prasad R, Mertia RS, Narain P (2004) Khadin cultivation: a traditional runoff farming system in Indian Desert needs sustainable management. J Arid Environ 58:87–96. https://doi.org/10.1016/S0140-1963(03)00105-8
Oweis T, Hachum A (2006) Water harvesting and supplemental irrigation for improved water productivity of dry farming systems in West Asia and North Africa. Agric Water Manag 80:57–73. https://doi.org/10.1016/j.agwat.2005.07.004
Page FC (1967) Re-definition of the genus Acanthamoeba with descriptions of three species. J Protozool 14(4):709–724
Qvarnstrom Y, da Silva AJ, Schuster FL, Gelman BB, Visvesvara GS (2009) Molecular confirmation of Sappinia pedata as a causative agent of amoebic encephalitis. J Infect Dis 199(8):1139–1142. https://doi.org/10.1086/597473
Reyes-Batlle M, Niyyati M, Martín-Navarro CM, López-Arencibia A, Valladares B, Martínez-Carretero E et al (2015) Unusual Vermamoeba vermiformis strain isolated from Snow in Mount Teide, Tenerife, Canary. Islands, Spain. Nov Biomed 3:189–192
Reyes-Batlle M, Wagner C, López-Arencibia A, Sifaoui I, Martínez-Carretero E, Valladares B et al (2017) Isolation and molecular characterization of a Naegleria strain from a recreational water fountain in Tenerife, Canary Islands, Spain. Acta Parasitol 62:265–268. https://doi.org/10.1515/ap-2017-0033
Rivera F, Roy-Ocotla G, Rosas I, Ramirez E, Bonilla P, Lares F (1987) Amoebae isolated from the atmosphere of Mexico City and environs. Environ Res 42(1):149–154 PMID: 3803333
Sandor JA, Norton JB, Homburg JA, Muenchrath DA, White CS, Williams SE et al (2007) Biogeochemical studies of a native American runoff agroecosystem. Geoarchaeol Int J 22:359–386. https://doi.org/10.1002/gea.20157
Sadhwani Alonso J, Álvarez Álvarez L, Melián-Martel N, Sadhwani Díaz J (2015) The Canary Islands and its passion for water desalination. Desalin Water Treat 55(9):2340–2350. https://doi.org/10.1080/19443994.2014.939862
Schallenberg-Rodríguez JC, Veza JM, Blanco-Marigorta A (2014) Energy efficiency and desalination in the Canary Islands. Renew Sustain Energy Rev 40:741–748. https://doi.org/10.1016/j.rser.2014.07.213
Segura C (2018) Pocos quieren beber el agua que salvó a Canarias. Publishing El País web. https://elpais.com/politica/2018/01/20/actualidad/1516475753_444638.html. Accessed 29 Sep 2018
Siddiqui R, Ali IKM, Cope JR, Khan NA (2016) Biology and pathogenesis of Naegleria fowleri. Acta Trop 164:375–394. https://doi.org/10.1016/j.actatropica.2016.09.009
Smirnov A, Chao E, Nassonova E, Cavalier-Smith T (2011) Revised classification of nonmycetozoan naked lobose amoebae (Amoebozoa). Protist 162(4):545–570
Stremolet S (2001) Water means business in the Canaries. In: Financial times global water report, Issue 122
Visvesvara GS, Moura H, Schuster FL (2007) Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol Med Microbiol 50(1):1–26 (PMID: 17428307)
Zarzo D, Campos E, Terrero P (2012) Spanish experience in desalination for agriculture. Desalin Water Treat 51:1–14. https://doi.org/10.1080/19443994.2012.708155
Acknowledgements
This work was funded by the proyect FIS PI18/01380 “Protozoosis emergentes por amebas de vida libre: Mejora de estrategias de diagnóstico, nuevas terapias y mecanismo de acción y traslación clínicas de los resultados” and Project AGL2013-46054-R. Spanish Ministry of Economic and Competitiveness. MRB was supported by the grants RICET [project no. RD16/0027/0001 of the programme of Redes Temáticas de Investigación Cooperativa, FIS], Spanish Ministry of Health, Madrid, Spain Spanish Ministry of Health, Madrid, Spain. ALA and IS were funded by the Agustín de Betancourt Programme. OC was supported by a grant from Tunisian Ministry of Higher Education and the International Relationships Vicechancellor at the Universidad de La Laguna. JEPB was funded by Proyectos puente al Plan Estatal de I + D+I. Plan Propio 2018 Universidad de La Laguna.
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Reyes-Batlle, M., Rizo-Liendo, A., Viera-Santana, R.A. et al. Isolation and Molecular Identification of Naegleria australiensis in Irrigation Water of Fuerteventura Island, Spain. Acta Parasit. 64, 331–335 (2019). https://doi.org/10.2478/s11686-019-00046-8
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DOI: https://doi.org/10.2478/s11686-019-00046-8