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Morphological and molecular characterization of Plasmodium cathemerium (lineage PADOM02) from the sparrow Passer domesticus with complete sporogony in Culex pipiens complex

Published online by Cambridge University Press:  27 April 2020

Mohamed Z. Y. Aly ,
Ibrahem I. I. Mohamed ,
Salwa I. Sebak ,
Ralph E. T. Vanstreels Open the ORCID record for Ralph E. T. Vanstreels [Opens in a new window]  and
Azza M. El gendy Open the ORCID record for Azza M. El gendy [Opens in a new window]
Mohamed Z. Y. Aly
Affiliation:
Faculty of Science, Department of Zoology, South Valley University, Qena, Egypt
Ibrahem I. I. Mohamed
Affiliation:
Faculty of Science, Department of Zoology, South Valley University, Qena, Egypt
Salwa I. Sebak
Affiliation:
Faculty of Science, Department of Zoology, South Valley University, Qena, Egypt
Ralph E. T. Vanstreels
Affiliation:
Marine Apex Predator Research Units (MAPRU), Institute for Coastal and Marine Research, Nelson Mandela University, South Africa Department of Zoology, DST-NRF Centre of Excellence at the Fitz Patrick Institute for African Ornithology, Nelson Mandela University, South Africa
Azza M. El gendy*
Affiliation:
Faculty of Science, Department of Entomology, Cairo University, Giza, PO Box 12613, Egypt
*
Author for correspondence: Azza M. El gendy, E-mail: aelgendy@sci.cu.edu.eg
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Abstract

Avian malaria is a mosquito-borne disease caused by Plasmodium spp. protozoa. Although these parasites have been extensively studied in North America and Eurasia, knowledge on the diversity of Plasmodium, its vectors and avian hosts in Africa is scarce. In this study, we report on natural malarial infections in free-ranging sparrows (Passer domesticus) sampled at Giza Governorate, Egypt. Parasites were morphologically characterized as Plasmodium cathemerium based on the examination of thin blood smears from the avian host. Sequencing a fragment of the mitochondrial cytochrome b gene showed that the parasite corresponded to lineage PADOM02. Phylogenetic analysis showed that this parasite is closely related to the lineages SERAU01 and PADOM09, both of which are attributed to P. cathemerium. Experimental infection of Culex pipiens complex was successful, with ookinetes first detected at 1-day post infection (dpi), oocysts at 4 dpi and sporozoites at 6 dpi. The massive infection of the salivary glands by sporozoites corroborates that Cx. pipiens complex is a competent vector of PADOM02. Our findings confirm that Plasmodium lineage PADOM02 infects sparrows in urban areas along the Nile River, Egypt, and corroborate that Cx. pipiens complex is a highly competent vector for these parasites. Furthermore, our results demonstrate that this lineage corresponds to the morphospecies P. cathemerium and not P. relictum as previously believed.

Keywords

Avian malariaCulicidaecytochrome bHaemosporidalight microscopyPCRsporogonyvector-borne pathogen
Type
Research Article
Information
Parasitology , Volume 147 , Issue 9 , August 2020 , pp. 985 - 993
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Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Abdelwhab, EM and Hafez, HM (2011) An overview of the epidemic of highly pathogenic H5N1 avian influenza virus in Egypt: epidemiology and control challenges. Epidemiology & Infection 139, 647–657.10.1017/S0950268810003122CrossRefGoogle ScholarPubMed
Adham, FK, Gabre, RM, Ayaad, TH and Galal, FH (2003) The effects of laboratory Hepatozoon gracilis infection on the fecundity, mortality and longevity of Culex pipiens Linnaeus (Diptera: Culicidae). Egyptian Journal Egyptian Society Parasitology 33, 353–360.Google Scholar
Beadell, JS, Ishtiaq, F, Covas, R, Melo, M, Warren, BH, Atkinson, CT, Bensch, S, Graves, GR, Jhala, YV, Peirce, MA, Rahmani, AR, Fonseca, DM and Fleischer, RC (2006) Global phylogeographic limits of Hawaii's avian malaria. Proceedings of the Royal Society of London B: Biological Sciences 273, 2935–2944.10.1098/rspb.2006.3671CrossRefGoogle ScholarPubMed
Bensch, S (2019) MalAvi: A database for avian haemosporidiian parasites. http://130.235.244.92/Malavi/index.html (access on 07 November 2019).Google Scholar
Bensch, S, Hellgren, O and Pérez-Tris, J (2009) Malavi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 1353–1358.10.1111/j.1755-0998.2009.02692.xCrossRefGoogle ScholarPubMed
Bonneaud, C, Pérez-Tris, J, Federici, P, Chastel, O and Sorci, G (2006) Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60, 383–389.10.1111/j.0014-3820.2006.tb01114.xCrossRefGoogle Scholar
Carbo-Ramirez, P, Zuria, I, Schaefer, HM and Santiago-Alarcon, D (2017) Avian haemosporidians at three environmentally contrasting urban greenspaces. Journal of Urban Ecology 3, 1–11.10.1093/jue/juw011CrossRefGoogle Scholar
Carvalho, BM, Rangel, EF and Vale, MM (2017) Evaluation of the impacts of climate change on disease vectors through ecological niche modelling. Bulletin Entomological Research 107, 419–430.10.1017/S0007485316001097CrossRefGoogle ScholarPubMed
Clark, JN, Clegg, MS and Lima, RM (2014) A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. International Journal of Parasitology 44, 329–338.10.1016/j.ijpara.2014.01.004CrossRefGoogle ScholarPubMed
D'Amico, VL and Baker, AJ (2010) A rare case of Plasmodium (Haemamoeba) relictum Infection in a free-living Red Knot (Calidris Canutus rufa, Scolopacidae). Journal of Ornithology 151, 951–954.10.1007/s10336-010-0566-0CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.10.1038/nmeth.2109CrossRefGoogle ScholarPubMed
Davidson, NC and Stroud, DA (2006) African–Western Eurasian Flyways: current knowledge, population status and future challenges. In Boere, GC, Galbraith, CA and Stroud, DA (eds), Waterbirds Around the World. Edinburgh, UK: The Stationery Office, pp. 63–73.Google Scholar
Drovetski, SV, Aghayan, SA, Mata, VA, Lopes, RJ, Mode, NA, Harvey, JA and Voelker, G (2014) Does the niche breadth or trade-off hypothesis explain the abundance–occupancy relationship in avian Haemosporidia? Molecular Ecology 23, 3322–3329.10.1111/mec.12744CrossRefGoogle ScholarPubMed
Duncan, RP (1997) The role of competition and introduction effort in the success of passeriform birds introduced to New Zealand. The American Naturalist 149, 903–915.10.1086/286029CrossRefGoogle ScholarPubMed
Ejiri, H, Sato, Y, Sawai, R, Sasaki, E, Matsumoto, R, Ueda, M, Higa, Y, Tsuda, Y, Omori, S, Murata, K and Yukawa, M (2009) Prevalence of avian malaria parasite in mosquitoes collected at a zoological garden in Japan. Parasitology Research 105, 629–633.10.1007/s00436-009-1434-9CrossRefGoogle Scholar
Ejiri, H, Sato, Y, Kim, KS, Hara, T, Tsuda, Y, Imura, T, Murata, K and Yukawa, M (2011) Entomological study on transmission of avian malaria parasites in a zoological garden in Japan: bloodmeal identification and detection of avian malaria parasite DNA from blood-fed mosquitoes. Journal of Medical Entomology 48, 600–607.10.1603/ME10197CrossRefGoogle Scholar
Ewen, JG, Bensch, S, Blackburn, TM, Bonneaud, C, Brown, R, Cassey, P, Clarke, RH and Pérez-Tris, J (2012) Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecology Letters 15, 1112–1119.10.1111/j.1461-0248.2012.01833.xCrossRefGoogle Scholar
Farajollahi, A, Fonseca, DM, Kramer, LD and Marm Kilpatrick, A (2011) “Bird biting” mosquitoes and human disease: a review of the role of Culex Pipiens complex mosquitoes in epidemiology. Infection. Genetics and Evolution 11, 1577–1585.10.1016/j.meegid.2011.08.013CrossRefGoogle Scholar
Ferraguti, M, Martínez-de la Puente, J, Bensch, S, Roiz, D, Ruiz, S, Viana, DS, Soriguer, RC and Figuerola, J (2018) Ecological determinants of avian malaria infections: an integrative analysis at landscape, mosquito and vertebrate community levels. Journal of Animal Ecology 87, 727–740.10.1111/1365-2656.12805CrossRefGoogle ScholarPubMed
Garcia-Longoria, L, Marzal, A, De Lope, F and Garamszegi, L (2019) Host-parasite interaction explains variation in the prevalence of avian haemosporidians at the community level. PloS One 14, 1–17.10.1371/journal.pone.0205624CrossRefGoogle ScholarPubMed
Glaizot, O, Fumagalli, L, Iritano, K, Lalubin, F, Van Rooyen, J and Christe, P (2012) High prevalence and lineage diversity of avian malaria in wild populations of great tits (Parus major) and mosquitoes (Culex Pipiens). PLoS One 7, e34964.10.1371/journal.pone.0034964CrossRefGoogle Scholar
Godfrey, RD Jr., Fedynich, AM and Pence, DB (1987) Quantification of hematozoa in blood smears. Journal of Wildlife Diseases 23, 558–565.10.7589/0090-3558-23.4.558CrossRefGoogle ScholarPubMed
Guindy, E, Hoogstraal, H and Mohammed, AHH (1965) Plasmodium garnhami sp. nov. from the Egyptian hoopoe (Upupa epops major brehm). Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 280–282.10.1016/0035-9203(65)90007-6CrossRefGoogle Scholar
Haiba, MH (1948) Plasmodia of common Egyptian birds. Journal of Comparative Pathology and Therapeutics 58, 81–93.10.1016/S0368-1742(48)80007-XCrossRefGoogle ScholarPubMed
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acid Symposium Series No. 41, 95–98.Google Scholar
Harbach, RE (1985) Pictorial keys to the genera of mosquitoes, subgenera of Culex and the species of Culex (Culex) occurring in southwestern Asia and Egypt, with a note on the subgeneric placement of Culex deserticola (Diptera: Culicidae). Mosquito Systematics 17, 83–107.Google Scholar
Hellgren, O, Waldenström, J, Peréz-Tris, J, Ösi, ES, Hasselquist, D, Krizanauskiene, A, Ottosson, U and Bensch, S (2007) Detecting shifts of transmission areas in avian blood parasites-a phylogenetic approach. Molecular Ecology 16, 1281–1290.CrossRefGoogle Scholar
Hongoh, V, Berrang-Ford, L, Scott, ME and Lindsay, R (2012) Expanding geographical distribution of the mosquito, Culex pipiens, in Canada under climate change. Applied Geography 33, 53–62.10.1016/j.apgeog.2011.05.015CrossRefGoogle Scholar
Huff, CG (1927) Studies on the infectivity of Plasmodia of birds for mosquitoes, with special reference to the problem of immunity in the mosquito. American Journal of Hygiene 7, 706–734.Google Scholar
Huff, CG (1932) Further infectivity experiments with mosquitoes and bird malaria. American Journal of Hygiene 15, 751–754.Google Scholar
Ibrahim, WAL (2011) An overview of bird migration studies in Egypt. The Ring 33, 1–2Google Scholar
Inumaru, M, Murata, K and Sato, Y (2017) Prevalence of avian haemosporidia among injured wild birds in Tokyo and environs, Japan. International Journal for Parasitology: Parasites and Wildlife 6, 299–309.Google ScholarPubMed
Ishtiaq, F, Gering, E, Rappole, JH, Rahmani, AR, Jhala, YV, Dove, CJ, Milensky, C, Olson, SL, Peirce, MA and Fleischer, RC (2007) Prevalence and diversity of avian hematozoan parasites in Asia: a regional survey. Journal of Wildlife Diseases 43, 382–398.10.7589/0090-3558-43.3.382CrossRefGoogle ScholarPubMed
Kazlauskienė, R, Bernotienė, R, Palinauskas, V, Iezhova, TA and Valkiūnas, G (2013) Plasmodium relictum (lineages pSGS1 and pGRW11): complete synchronous sporogony in mosquitoes Culex pipiens pipiens. Experimental Parasitology 133, 454–461.10.1016/j.exppara.2013.01.008CrossRefGoogle ScholarPubMed
Kim, KS and Tsuda, Y (2010) Seasonal changes in the feeding pattern of Culex Pipiens pallens govern the transmission dynamics of multiple lineages of avian malaria parasites in Japanese wild bird community. Molecular Ecology 19, 5545–5554.10.1111/j.1365-294X.2010.04897.xCrossRefGoogle ScholarPubMed
Kim, KS, Tsuda, Y, Yamada, A and Yamada, A (2009) Bloodmeal identification and detection of avian malaria parasite from mosquitoes (Diptera: Culicidae) inhabiting coastal areas of Tokyo Bay, Japan. Journal of Medical Entomology 46, 1230–1234.CrossRefGoogle ScholarPubMed
LaPointe, DA, Goff, ML and Atkinson, CT (2010) Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai'i. Journal of Parasitology 96, 318–324.10.1645/GE-2290.1CrossRefGoogle ScholarPubMed
LaPointe, DA, Atkinson, CT and Samuel, MD (2012) Ecology and conservation biology of avian malaria. Annals of the New York Academy of Sciences 1249, 211–226.10.1111/j.1749-6632.2011.06431.xCrossRefGoogle ScholarPubMed
Liu, B, Deng, Z, Huang, W, Dong, L and Zhang, Y (2019) High prevalence and narrow host range of haemosporidian parasites in Godlewski's bunting (Emberiza godlewskii) in northern China. Parasitology International 69, 121–125.10.1016/j.parint.2018.09.004CrossRefGoogle Scholar
Loiseau, C, Zoorob, R, Robert, A, Chastel, O, Julliard, R and Sorci, G (2010) Plasmodium relictum infection and MHC diversity in the house sparrow (Passer domesticus). Proceedings of the Royal Society B: Biological Sciences 278, 1264–1272.10.1098/rspb.2010.1968CrossRefGoogle Scholar
Martínez-De la Puente, J, Ferraguti, M, Ruiz, S, Roiz, D, Soriguer, R and Figuerola, J (2016) Culex Pipiens forms and urbanization: effects on blood feeding sources and transmission of avian Plasmodium. Malaria Journal 15, 589–597.CrossRefGoogle ScholarPubMed
Marzal, A, Ricklefs, RE, Valkiūnas, G, Albayrak, T, Arriero, E, Bonneaud, C, Czirják, GA, Ewen, J, Hellgren, O, Hořáková, D, Iezhova, TA, Jensen, H, Križanauskienė, A, Lima, MR, de Lope, F, Magnussen, E, Martin, LB, Møller, AP, Palinauskas, V, Pap, PL, Pérez-Tris, J, Sehgal, RNM, Soler, M, Szöllősi, E, Westerdahl, H, Zetindjiev, P and Bensch, S (2011) Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS One 6, e21905.10.1371/journal.pone.0021905CrossRefGoogle Scholar
Mohammed, AHH (1958a) Protozoal Blood Parasites of Egyptian Birds, (Thesis), London School of Hygiene and Tropical Medicine.Google Scholar
Mohammed, AHH (1958b) Systematic and Experimental Studies on Protozoal Blood Parasites of Egyptian Birds. Volume I& II. Cairo: Cairo University Press.Google Scholar
Palinauskas, V, Iezhova, TA, Križanauskienė, A, Markovets, MY, Bensch, S and Valkiūnas, G (2013) Molecular characterization and distribution of Haemoproteus minutus (Haemosporida, Haemoproteidae): a pathogenic avian parasite. Parasitology International 62, 358–363.CrossRefGoogle ScholarPubMed
Patz, JA, Epstein, PR, Burke, TA and Balbus, JM (1996) Global climate change and emerging infectious diseases. Journal of the American Medical Association 275, 217–223.10.1001/jama.1996.03530270057032CrossRefGoogle ScholarPubMed
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 1572–1574.10.1093/bioinformatics/btg180CrossRefGoogle ScholarPubMed
Sambrook, J, Fritsch, EF and Maniatis, T (1989) Molecular cloning: a laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.Google Scholar
Santiago-Alarcon, D, Palinauskas, V and Schaefer, HH (2012) Diptera vectors of avian Haemospoidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87, 928–964.CrossRefGoogle ScholarPubMed
Schoener, ER, Harl, J, Himmel, T, Fragner, K, Weissenböck, H and Fuehrer, HP (2019) Protozoan parasites in Culex Pipiens mosquitoes in Vienna. Parasitology Research 118, 1261–1269.CrossRefGoogle ScholarPubMed
Synek, P, Munclinger, P, Albrecht, T and Votýpka, J (2013) Avian haemosporidians in haematophagous insects in the Czech Republic. Parasitology Research 112, 839–845.CrossRefGoogle ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Tandina, F, Doumbo, O, Yaro, AS, Traoré, SF, Parola, P and Robert, V (2018) Mosquitoes (Diptera: Culicidae) and mosquito-borne diseases in Mali, West Africa. Parasite and Vectors 11, 1–12.CrossRefGoogle ScholarPubMed
Thompson, JD, Gibson, TJ and Higgins, DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Current Protocols Bioinformatics 00, 2.3.1–2.3.22.CrossRefGoogle Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and other Haemosporidia. Boca Raton, Florida, USA: CRC Press, 932 pp.Google Scholar
Valkiūnas, G (2011) Haemosporidian vector research: marriage of molecular and microscopical approaches is essential. Molecular Ecology 20, 3084–3086.10.1111/j.1365-294X.2011.05187.xCrossRefGoogle ScholarPubMed
Valkiūnas, G and Iezhova, TA (2018) Keys to the avian malaria parasites. Malaria Journal 17, 1–24.10.1186/s12936-018-2359-5CrossRefGoogle ScholarPubMed
Valkiūnas, G, Zehtindjiev, P, Dimitrov, D, Križanauskienė, A, Iezhova, TA and Bensch, S (2008) Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitology Research 102, 1185–1193.10.1007/s00436-008-0892-9CrossRefGoogle ScholarPubMed
Valkiūnas, G, Kazlauskiene, R, Bernotiene, R, Palinauskas, V and Iezhova, TA (2013) Abortive long-lasting sporogony of two Haemoproteus species (Haemosporida. Haemoprodteidae) in the mosquito Ochlerotatus Cantans, with perspective on haemosporidian vector research. Parasitology Research 112, 2159–2169.CrossRefGoogle Scholar
Valkiūnas, G, Žiegytė, R, Palinauskas, V, Bernotienė, R, Bukauskaitė, D, Ilgūnas, M, Dimitrov, D and Iezhova, TA (2015) Complete sporogony of Plasmodium relictum (lineage pGRW4) in mosquitoes Culex Pipiens pipiens, with implications on avian malaria epidemiology. Parasitology Research 114, 3075–3085.10.1007/s00436-015-4510-3CrossRefGoogle ScholarPubMed
Valkiūnas, G, Ilgūnas, M, Bukauskaite, D, Palinauskas, V, Bernotiene, R and Iezhova, TA (2017) Molecular characterization and distribution of Plasmodium matutinum, a common avian malaria parasite. Parasitology 144, 1726–1735.10.1017/S0031182017000737CrossRefGoogle ScholarPubMed
Vanstreels, RET, Kolesnikovas, CKM, Sandri, S, Silveira, P, Belo, NO, Junior, FCF, Epiphanio, S, Steindel, M, Braga, ÉM and Catão-Dias, JL (2014) Outbreak of avian malaria associated to multiple species of Plasmodium in Magellanic penguins undergoing rehabilitation in southern Brazil. Plos One 9, e94994.CrossRefGoogle ScholarPubMed
Waldenström, J, Bensch, S, Hasselquist, D and Östman, Ö (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191–194.10.1645/GE-3221RNCrossRefGoogle ScholarPubMed
Weaver, SC and Reisen, WK (2010) Present and future arboviral threats. Antiviral Research 85, 328–345.CrossRefGoogle ScholarPubMed
Wiersch, SC, Maier, WA and Kampen, H (2005) Plasmodium (Haemamoeba) cathemerium gene sequences for phylogenetic analysis of malaria parasites. Parasitology Research 96, 90–94.CrossRefGoogle ScholarPubMed
Žiegytė, R, Bernotienė, R, Bukauskaitė, D, Palinauskas, V, Iezhova, TA and Valkiūnas, G (2014) Complete sporogony of Plasmodium relictum (lineage pSGS1 and pGRW11) in mosquitoes Culex Pipiens form molestus, with implications to avian epidemiology. Journal of Parasitology 100, 878–882.CrossRefGoogle ScholarPubMed
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