Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-10T06:36:10.276Z Has data issue: false hasContentIssue false
  • English
  • Français

Plasmodium ouropretensis, n. sp., a new case of non-erythrocytic species within lizard malaria parasites

Published online by Cambridge University Press:  08 June 2021

Oscar Hernandes Córdoba Open the ORCID record for Oscar Hernandes Córdoba [Opens in a new window] ,
Francisco C. Ferreira Open the ORCID record for Francisco C. Ferreira [Opens in a new window] ,
M. Andreína Pacheco ,
Ananias A. Escalante  and
Érika Martins Braga
Oscar Hernandes Córdoba*
Affiliation:
Red de Biología y Conservación de Vertebrados, Instituto de Ecología, A.C. Xalapa, Veracruz, México Malaria Laboratory, Department of Parasitology, Universidade Federal de Minas Gerais, Belo Horizonte – MG, Brazil
Francisco C. Ferreira
Affiliation:
Center for Conservation Genomics, Smithsonian Conservation Biology Institute, Washington, DC, USA Center for Vector Biology, Rutgers University, New Brunswick, NJ, USA
M. Andreína Pacheco
Affiliation:
Biology Department/Institute of Genomics and Evolutionary Medicine (iGEM), Temple University, Philadelphia, PA, USA
Ananias A. Escalante
Affiliation:
Biology Department/Institute of Genomics and Evolutionary Medicine (iGEM), Temple University, Philadelphia, PA, USA
Érika Martins Braga
Affiliation:
Malaria Laboratory, Department of Parasitology, Universidade Federal de Minas Gerais, Belo Horizonte – MG, Brazil
*
Author for correspondence: Oscar Hernandes Córdoba, E-mail: oscarhernandezcordoba@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Delimiting and describing Plasmodium species in reptiles remains a pressing problem in Haemosporida taxonomy. The few morphological characters used can overlap, and the significance of some life-history traits is not fully understood. Morphologically identical lizard Plasmodium forms have been reported infecting different cell types (red and white blood cells) in the same host and have been considered the same species. An example is Plasmodium tropiduri tropiduri, a species known to infect erythrocytes, thrombocytes and lymphocyte-like cells. Here, both forms of P. t. tropiduri were analysed using light microscope-based morphological characteristics and phylogenetic inferences based on almost complete mitochondrial genomes of parasites naturally infecting lizards in southeastern Brazil. Although morphologically similar, two distinct phylogenetic lineages infecting erythrocytes and non-erythrocytic cells were found. The lineage found in the erythrocytes forms a monophyletic group with species from Colombia. However, the non-erythrocytic lineage shares a recent common ancestor with Plasmodium leucocytica, which infects leucocytes in lizards from the Caribbean islands. Here, Plasmodium ouropretensis n. sp. is described as a species that infects thrombocytes and lymphocyte-like cells.

Keywords

Cryptic speciescytb geneHaemosporidamtDNA sequencing
Type
Research Article
Information
Parasitology , Volume 148 , Issue 12 , October 2021 , pp. 1467 - 1474
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altschul, SF, Gish, W, Miller, W, Myers, EW and Lipman, DJ (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.CrossRefGoogle ScholarPubMed
Carini, A (1941) Sobre um Plasmodium endoglobular de um largarto. Arquivos do Instituto Biológico 25, 46–47.Google Scholar
Dallas, TA, Laine, AL and Ovaskainen, O (2019) Detecting parasite associations within multi-species host and parasite communities. Proceedings of the Royal Society B: Biological Sciences 286, 2019–1109.Google ScholarPubMed
Falk, B, Mahler, DL and Perkins, SL (2011) Tree-based delimitation of morphologically ambiguous taxa: a study of the lizard malaria parasites on the Caribbean island of Hispaniola. International Journal for Parasitology 41, 967–980.CrossRefGoogle ScholarPubMed
Ferreira, FC, Alves, LGM, Jager, GB, Franzini, LD, Mesquita, DO, Díaz-Delgado, J, Catão-Dias, JL and Martins-Braga, ÉM (2020) Molecular and pathological investigations of Plasmodium parasites infecting striped forest whiptail lizards (Kentropyx calcarata) in Brazil. Parasitology Research 119, 2631–2640.CrossRefGoogle ScholarPubMed
Gouy, M, Guindon, S and Gascuel, O (2010) SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27(2), 221–224. http://dx.doi.org/10.1093/molbev/msp259CrossRefGoogle ScholarPubMed
Harris, DJ, Santos, JL, Borges-Nojosa, DM and de Castro, DP (2019) Molecular screening of Plasmodium (Haemosporidia: Plasmodiidae) Parasites from Reptiles in Brazil. Journal of Parasitology 105, 913.CrossRefGoogle ScholarPubMed
Hellgren, O, Waldenström, J and Bensch, S (2004) A new pcr assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood a new PCR assay for simultaneous studies of Leucocytozoon. Journal of Parasitology 90, 797–802.CrossRefGoogle Scholar
Hernandes-Cordoba, O and Braga, E (2019) Plasmodium tropiduri tropiduri in co-occurrence with Chigger Mites and Microfilaria in the Ground Lizard Tropidurus torquatus. Herpetological Conservation and Biology 14, 402–410.Google Scholar
Kimura, M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Lainson, R and Shaw, JJ (1969) New host records for Plasmodium diploglossi, P. tropiduri Aragao and Neiva, 1909, and P. cnemidophori Garini, 1941. Parasitology 59, 163–170.CrossRefGoogle Scholar
Lainson, R, Landau, I and Shaw, JJ (1971) On a new family of non-pigmented parasites in the blood of reptiles: Garniidae fam. nov. (Coccidiida: Haemosporidiidea). Some species of the new genus Garnia. International Journal for Parasitology 1, 241–250.CrossRefGoogle Scholar
Lainson, R, Landau, I and Shaw, J (1974) Further parasites of the family Garniidae (Coccidiida: Haemosporidiidea) in Brazilian lizards. Fallisia effusa gen.nov., sp.nov. and Fallisia modesta gen.nov., sp.nov. Parasitology 68, 117–125.CrossRefGoogle ScholarPubMed
Matta, NE, González, LP, Pacheco, MA, Escalante, AA, Moreno, AM, González, AD and Calderón-Espinosa, ML (2018) Plasmodium parasites in reptiles from the Colombia Orinoco-Amazon basin: a re-description of Plasmodium kentropyxi Lainson R, Landau I, Paperna I, 2001 and Plasmodium carmelinoi Lainson R, Franco CM, da Matta R, 2010. Parasitology Research 117, 1357–1370.CrossRefGoogle Scholar
Pacheco, MA and Escalante, AA (2020) Cophylogenetic patterns and speciation in Avian Haemosporidians. In Santiago-Alarcon, D and Marzal, A (eds), Avian Malaria and Related Parasites in the Tropics. Gewerbestrasse, SW: Springer Nature, pp. 401–427.CrossRefGoogle Scholar
Pacheco, MA, Cepeda, AS and Bernotiene, R (2018) Primers targeting mitochondrial genes of avian haemosporidians: PCR detection and differential DNA amplification of parasites belonging to different genera. International Journal for Parasitology 45, 657–670.CrossRefGoogle Scholar
Palinauskas, V, Žiegyte, R, Ilgunas, M, Iezhova, TA, Bernotiene, R, Bolshakov, C and Valkiunas, G (2015) Description of the first cryptic avian malaria parasite, Plasmodium homocircumflexum n. sp., with experimental data on its virulence and development in avian hosts and mosquitoes. International Journal for Parasitology 45, 51–62.CrossRefGoogle Scholar
Perkins, SL (2000) Species concepts and malaria parasites: detecting a cryptic species of Plasmodium. Proceedings of the Royal Society B: Biological Sciences 267, 2345–2350.CrossRefGoogle ScholarPubMed
Perkins, SL and Schall, JJ (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology 88, 972–978.CrossRefGoogle ScholarPubMed
Perkins, SL, Osgood, SM and Schall, JJ (1998) Use of PCR for detection of subpatent infections of lizard malaria: implications for epizootiology. Molecular Ecology 7, 1587–1590.CrossRefGoogle Scholar
Perkins, SL, Martinsen, ES and Falk, BG (2011) Do molecules matter more than morphology? Promises and pitfalls in parasites. Parasitology 138, 1664–1674.CrossRefGoogle ScholarPubMed
Pessôa, SB and Lopes, J (1963) Nota sôbre alguns hematozoarios de lagartixas de Jacobina (Bahia, Brasil). Revista do instituto de medicina tropical de São Paulo 5, 133–139.Google Scholar
Picelli, AM, Ramires, AC, Masseli, GS, Pessoa, FAC, Viana, LA and Kaefer, IL (2020) Under the light: high prevalence of haemoparasites in lizards (reptilia: Squamata) from central amazonia revealed by microscopy. Anais da Academia Brasileira de Ciencias 92, 1–19.CrossRefGoogle ScholarPubMed
Poulin, R (2011) The many roads to parasitism: a tale of convergence. Advances in Parasitology 74, 1–40.CrossRefGoogle ScholarPubMed
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Rocha e Silva, E and Rodrigues, D (1974) Encontro do Plasmodium (s) tropiduri no estado de São Paulo, Brasil. Revista de Saude Publica de Sao Paulo 8, 163–170.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, D, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, M and Huelsenbeck, J (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 6, 539–542.CrossRefGoogle Scholar
Sambrook, J and Russell, DW (2001) Molecular Cloning. New York, USA: CSHL Press.Google Scholar
Schall, J (2002) Parasite virulence. In Lewis, EE, Campell, JF and Sukhdeo, MVK (eds), The Behavioural Ecology of Parasites. Boston, USA: CAB International, pp. 283–313.CrossRefGoogle Scholar
Schall, JJ and Bromwich, CR (1994) Interspecific interactions tested: two species of malarial parasite in a West African lizard. Oecologia 97, 326–332.CrossRefGoogle Scholar
Scorza, J (1970) Unpigmented gametocytes of Plasmodium (Sauramoeba) tropiduri in thrombocytes of Tropidurus torquatus (Iguanidae). Journal of Parasitology 56, 470–471.Google Scholar
Scorza, J (1971) Asexual and sexual stages of a malaria parasite in the thrombocytes of Tropidurus torquatus (Iguanidae) infected with Plasmodium tropiduri. Eukaryotic Microbiology 18, 403–410.Google ScholarPubMed
Telford, R (1973) Saurian malarial parasites from Guyana: their effect upon the validity of the family Garniidae and the genus Garnia, with descriptions of two new species. International Journal for Parasitology 3, 829–842.CrossRefGoogle Scholar
Telford, SR (1979) A taxonomic reconsideration of some Plasmodium species from Iguanid lizards. Annales de Parasitologie Humaine et Comparée 54, 129–144.CrossRefGoogle ScholarPubMed
Telford, SR (1980) The saurian malarias of Venezuela: species from iguanid and teiid hosts. International Journal for Parasitology 10, 365–374.CrossRefGoogle ScholarPubMed
Telford, SR (1988) A contribution to the systematics of the reptilian malaria parasites, family Plasmodiidae (Apicomplexa: Haemospororina). Bulletin of the Florida State Museum. Biological Science 34, 65–97.Google Scholar
Telford, SR (2009) Hemoparasites of the Reptilia Color Atlas and Text. Boca Raton, USA: CRC Press; Taylor & Francis Group.Google Scholar