The 18S rRNA genes of Haemoproteus (Haemosporida, Apicomplexa) parasites from European songbirds with remarks on improved parasite diagnostics.

Publisher: BioMed Central Country of Publication: England NLM ID: 101139802 Publication Model: Electronic Cited Medium: Internet ISSN: 1475-2875 (Electronic) Linking ISSN: 14752875 NLM ISO Abbreviation: Malar J Subsets: MEDLINE

Original Publication: London : BioMed Central, [2002-

Haemosporida* ; Songbirds* ; Parasites* ; Bird Diseases*/parasitology ; Apicomplexa*/genetics ; Plasmodium*/genetics ; Protozoan Infections, Animal*/parasitology; Animals ; Phylogeny ; RNA, Ribosomal, 18S/genetics ; Genes, rRNA ; Mammals/genetics

Background: The nuclear ribosomal RNA genes of Plasmodium parasites are assumed to evolve according to a birth-and-death model with new variants originating by duplication and others becoming deleted. For some Plasmodium species, it has been shown that distinct variants of the 18S rRNA genes are expressed differentially in vertebrate hosts and mosquito vectors. The central aim was to evaluate whether avian haemosporidian parasites of the genus Haemoproteus also have substantially distinct 18S variants, focusing on lineages belonging to the Haemoproteus majoris and Haemoproteus belopolskyi species groups.
Methods: The almost complete 18S rRNA genes of 19 Haemoproteus lineages of the subgenus Parahaemoproteus, which are common in passeriform birds from the Palaearctic, were sequenced. The PCR products of 20 blood and tissue samples containing 19 parasite lineages were subjected to molecular cloning, and ten clones in mean were sequenced each. The sequence features were analysed and phylogenetic trees were calculated, including sequence data published previously from eight additional Parahaemoproteus lineages. The geographic and host distribution of all 27 lineages was visualised as CytB haplotype networks and pie charts. Based on the 18S sequence data, species-specific oligonucleotide probes were designed to target the parasites in host tissue by in situ hybridization assays.
Results: Most Haemoproteus lineages had two or more variants of the 18S gene like many Plasmodium species, but the maximum distances between variants were generally lower. Moreover, unlike in most mammalian and avian Plasmodium species, the 18S sequences of all but one parasite lineage clustered into reciprocally monophyletic clades. Considerably distinct 18S clusters were only found in Haemoproteus tartakovskyi hSISKIN1 and Haemoproteus sp. hROFI1. The presence of chimeric 18S variants in some Haemoproteus lineages indicates that their ribosomal units rather evolve in a semi-concerted fashion than according to a strict model of birth-and-death evolution.
Conclusions: Parasites of the subgenus Parahaemoproteus contain distinct 18S variants, but the intraspecific variability is lower than in most mammalian and avian Plasmodium species. The new 18S data provides a basis for more thorough investigations on the development of Haemoproteus parasites in host tissue using in situ hybridization techniques targeting specific parasite lineages.
(© 2023. BioMed Central Ltd., part of Springer Nature.)

Elder JF Jr, Turner BJ. Concerted evolution of repetitive DNA sequences in eukaryotes. Q Rev Biol. 1995;70:297–320. (PMID: 756867310.1086/419073)
Schlötterer C, Tautz D. Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution. Curr Biol. 1994;4:777–83. (PMID: 782054710.1016/S0960-9822(00)00175-5)
Liao D. Concerted evolution: molecular mechanism and biological implications. Am J Hum Genet. 1999;64:24–30. (PMID: 9915939137769810.1086/302221)
Rooney AP. Mechanisms underlying the evolution and maintenance of functionally heterogeneous 18S rRNA genes in apicomplexans. Mol Biol Evol. 2004;21:1704–11. (PMID: 1517541110.1093/molbev/msh178)
Waters AP, Syin C, McCutchan TF. Developmental regulation of stage-specific ribosome populations in Plasmodium. Nature. 1989;342:438–40. (PMID: 258661310.1038/342438a0)
McCutchan TF, Li J, McConkey GA, Rogers MJ, Waters AP. The cytoplasmic ribosomal RNAs of Plasmodium spp. Parasitol Today. 1995;11:134–8. (PMID: 1527535610.1016/0169-4758(95)80132-4)
Dame JB, Sullivan M, McCutchan TF. Two major sequence classes of ribosomal RNA genes in Plasmodium berghei. Nucleic Acids Res. 1984;12:5943–52. (PMID: 637960632004210.1093/nar/12.14.5943)
Harl J, Himmel T, Valkiūnas G, Weissenböck H. The nuclear 18S ribosomal DNAs of avian haemosporidian parasites. Malar J. 2019;18:305. (PMID: 31481072672429510.1186/s12936-019-2940-6)
Valkiūnas G, Iezhova TA. Keys to the avian Haemoproteus parasites (Haemosporida, Haemoproteidae). Malar J. 2022;21:269. (PMID: 36123731948709710.1186/s12936-022-04235-1)
Valkiūnas G, Atkinson CT. Introduction to life cycles, taxonomy, distribution, and basic research techniques. In: Avian malaria and related parasites in the tropics. Cham: Springer; 2020. p. 45–80. (PMID: 10.1007/978-3-030-51633-8_2)
Himmel T, Harl J, Matt J, Weissenböck H. A citizen science-based survey of avian mortality focusing on haemosporidian infections in wild passerine birds. Malar J. 2021;20:1–13. (PMID: 10.1186/s12936-021-03949-y)
Hellgren O, Waldenström J, Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol. 2004;90:797–802. (PMID: 1535707210.1645/GE-184R1)
Hall TA. BioEdit: a user-friendly biological sequences alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8.
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80. (PMID: 23329690360331810.1093/molbev/mst010)
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating Maximum-Likelihood phylogenies. Mol Biol Evol. 2015;32:268–74. (PMID: 2537143010.1093/molbev/msu300)
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–42. (PMID: 22357727332976510.1093/sysbio/sys029)
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3. (PMID: 19505945271234410.1093/bioinformatics/btp348)
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–9. (PMID: 29722887596755310.1093/molbev/msy096)
Martin DP, Varsani A, Roumagnac P, Botha G, Maslamoney S, Schwab T, et al. RDP5: a computer program for analyzing recombination in, and removing signals of recombination from, nucleotide sequence datasets. Virus Evol. 2021;7: veaa087. (PMID: 3393677410.1093/ve/veaa087)
Martin D, Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics. 2000;16:562–3. (PMID: 1098015510.1093/bioinformatics/16.6.562)
Salminen MO, Carr JK, Burke DS, McCutchan FE. Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retrovir. 1995;11:1423–5. (PMID: 857340310.1089/aid.1995.11.1423)
Padidam M, Sawyer S, Fauquet CM. Possible emergence of new geminiviruses by frequent recombination. Virology. 1999;265:218–25. (PMID: 1060059410.1006/viro.1999.0056)
Smith JM. Analyzing the mosaic structure of genes. J Mol Evol. 1992;34:126–9. (PMID: 155674810.1007/BF00182389)
Posada D, Crandall KA. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA. 2001;98:13757–62. (PMID: 117174356111410.1073/pnas.241370698)
Gibbs MJ, Armstrong JS, Gibbs AJ. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics. 2000;16:573–82. (PMID: 1103832810.1093/bioinformatics/16.7.573)
Boni MF, Posada D, Feldman MW. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics. 2007;176:1035–47. (PMID: 17409078189457310.1534/genetics.106.068874)
Križanauskienė A, Hellgren O, Kosarev V, Sokolov L, Bensch S, Valkiūnas G. Variation in host specificity between species of avian hemosporidian parasites: evidence from parasite morphology and cytochrome B gene sequences. J Parasitol. 2006;92:1319–24. (PMID: 1730481410.1645/GE-873R.1)
Ilgūnas M, Chagas CRF, Bukauskaitė D, Bernotienė R, Iezhova T, Valkiūnas G. The life-cycle of the avian haemosporidian parasite Haemoproteus majoris, with emphasis on the exoerythrocytic and sporogonic development. Parasit Vectors. 2019;12:516. (PMID: 31685020682999210.1186/s13071-019-3773-4)
Scordato ESC, Kardish MR. Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography. J Anim Ecol. 2014;83:1387–97. (PMID: 2481087810.1111/1365-2656.12246)
Valkiūnas G, Križanauskienė A, Iezhova TA, Hellgren O, Bensch S. Molecular phylogenetic analysis of circumnuclear hemoproteids (Haemosporida: Haemoproteidae) of sylviid birds, with a description of Haemoproteus parabelopolskyi sp. nov. J Parasitol. 2007;93:680–7. (PMID: 1762636410.1645/GE-1102R.1)
Križanauskienė A, Iezhova TA, Palinauskas V, Chernetsov N, Valkiūnas G. Haemoproteus nucleocondensus n. sp. (Haemosporida, Haemoproteidae) from a Eurasian songbird, the Great Reed Warbler Acrocephalus arundinaceus. Zootaxa. 2012;3441:36–46. (PMID: 10.11646/zootaxa.3441.1.3)
Fang J, McCutchan TF. Malaria: thermoregulation in a parasite’s life cycle. Nature. 2002;418:742. (PMID: 1218155710.1038/418742a)
Li J, Gutell RR, Damberger SH, Wirtz RA, Kissinger JC, Rogers MJ, et al. Regulation and trafficking of three distinct 18S ribosomal RNAs during development of the malaria parasite. J Mol Biol. 1997;269:203–13. (PMID: 919106510.1006/jmbi.1997.1038)
Gunderson JH, Sogin ML, Wollett G, Hollingdale M, De La Cruz VF, Waters AP, et al. Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science. 1987;238:933–7. (PMID: 367213510.1126/science.3672135)
Corredor V, Enea V. The small ribosomal subunit RNA isoforms in Plasmodium cynomolgi. Genetics. 1994;136:857–65. (PMID: 8005440120589110.1093/genetics/136.3.857)
Bensch S, Canbäck B, DeBarry JD, Johansson T, Hellgren O, Kissinger JC, et al. The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. Genome Biol Evol. 2016;8:1361–73. (PMID: 27190205489879810.1093/gbe/evw081)
Arnheim N, Krystal M, Schmickel R, Wilson G, Ryder O, Zimmer E. Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc Natl Acad Sci USA. 1980;77:7323–7. (PMID: 626125135049510.1073/pnas.77.12.7323)
Nei M, Gu X, Sitnikova T. Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci USA. 1997;94:7799–806. (PMID: 92232663370910.1073/pnas.94.15.7799)
Nei M, Hughes AL. Balanced polymorphism and evolution by the birth-and-death process in the MHC loci. In: Tsuji K, Aizawa M; Sasazuki T, editors. 11th histocompatibility workshop and conference Oxford Univ Press, Oxford, UK; 1992.
Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;61:315–20. (PMID: 826473410.1016/0166-6851(93)90077-B)
Rougemont M, Van Saanen M, Sahli R, Hinrikson HP, Bille J, Jaton K. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol. 2004;42:5636–43. (PMID: 1558329353522610.1128/JCM.42.12.5636-5643.2004)
Seilie AM, Chang M, Hanron AE, Billman ZP, Stone BC, Zhou K, et al. Beyond blood smears: qualification of Plasmodium 18S rRNA as a biomarker for controlled human malaria infections. Am J Trop Med Hyg. 2019;100:1466. (PMID: 31017084655391310.4269/ajtmh.19-0094)
Matsubara J, Chang M, Seilie AM, Murphy SC. Flow cytometric sorting of infected erythrocytes demonstrates reliable detection of individual ring-stage Plasmodium falciparum parasites by Plasmodium 18S rRNA reverse transcription polymerase chain reaction. Am J Trop Med Hyg. 2022;106:1653. (PMID: 35405648920991010.4269/ajtmh.21-1226)
Groff TC, Lorenz TJ, Crespo R, Iezhova T, Valkiūnas G, Sehgal RNM. Haemoproteosis lethality in a woodpecker, with molecular and morphological characterization of Haemoproteus velans (Haemosporida, Haemoproteidae). Int J Parasitol Parasites Wildl. 2019;10:93–100. (PMID: 31417845669063710.1016/j.ijppaw.2019.07.007)
Ortiz-Catedral L, Brunton D, Stidworthy MF, Elsheikha HM, Pennycott T, Schulze C, et al. Haemoproteus minutus is highly virulent for Australasian and South American parrots. Parasit Vectors. 2019;12:40. (PMID: 30654841633780210.1186/s13071-018-3255-0)
Fordyce SL, Kampmann M-L, van Doorn NL, Gilbert MTP. Long-term RNA persistence in postmortem contexts. Investig Genet. 2013;4:1–7. (PMID: 10.1186/2041-2223-4-7)
Dinhopl N, Mostegl MM, Richter B, Nedorost N, Maderner A, Fragner K, et al. Application of in-situ hybridization for the detection and identification of avian malaria parasites in paraffin wax-embedded tissues from captive penguins. Avian Pathol. 2011;40:315–20. (PMID: 21711191314510110.1080/03079457.2011.569533)
Himmel T, Harl J, Kübber-Heiss A, Konicek C, Fernández N, Juan-Sallés C, et al. Molecular probes for the identification of avian Haemoproteus and Leucocytozoon parasites in tissue sections by chromogenic in situ hybridization. Parasit Vectors. 2019;12:282. (PMID: 31159851654760910.1186/s13071-019-3536-2)
Dinhopl N, Nedorost N, Mostegl MM, Weissenbacher-Lang C, Weissenböck H. In situ hybridization and sequence analysis reveal an association of Plasmodium spp. with mortalities in wild passerine birds in Austria. Parasitol Res. 2015;114:1455–62. (PMID: 2563624610.1007/s00436-015-4328-z)
Harl J, Himmel T, Valkiūnas G, Ilgūnas M, Nedorost N, Matt J, et al. Avian haemosporidian parasites of accipitriform raptors. Malar J. 2022;21:14. (PMID: 34986864872915510.1186/s12936-021-04019-z)
Ilgūnas M, Himmel T, Harl J, Dagys M, Valkiūnas G, Weissenböck H. Exo-erythrocytic development of avian haemosporidian parasites in European owls. Animals. 2022;12:2212. (PMID: 36077935945441610.3390/ani12172212)
Himmel T, Harl J, Pfanner S, Nedorost N, Nowotny N, Weissenböck H. Haemosporidioses in wild Eurasian blackbirds (Turdus merula) and song thrushes (T. philomelos): an in situ hybridization study with emphasis on exo-erythrocytic parasite burden. Malar J. 2020;19:69. (PMID: 32050970701745910.1186/s12936-020-3147-6)

P 33480 Austrian Science Fund

Keywords: Birth-and-death evolution; Parahaemoproteus; Ribosomal genes; Semi-concerted evolution

0 (RNA, Ribosomal, 18S)

Date Created: 20230810 Date Completed: 20230814 Latest Revision: 20231120

20231215

PMC10416517

10.1186/s12936-023-04661-9

37563610