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Journal of Molecular Evolution

, Volume 86, Issue 9, pp 646–654 | Cite as

Delineation of the Genera Haemoproteus and Plasmodium Using RNA-Seq and Multi-gene Phylogenetics

  • Jasper Toscani FieldEmail author
  • Josh Weinberg
  • Staffan Bensch
  • Nubia E. Matta
  • Gediminas Valkiūnas
  • Ravinder N. M. Sehgal
Original Article

Abstract

Members of the order Haemosporida are protist parasites that infect mammals, reptiles and birds. This group includes the causal agents of malaria, Plasmodium parasites, the genera Leucocytozoon and Fallisia, as well as the species rich genus Haemoproteus with its two subgenera Haemoproteus and Parahaemoproteus. Some species of Haemoproteus cause severe disease in avian hosts, and these parasites display high levels of diversity worldwide. This diversity emphasizes the need for accurate evolutionary information. Most molecular studies of wildlife haemosporidians use a bar coding approach by sequencing a fragment of the mitochondrial cytochrome b gene. This method is efficient at differentiating parasite lineages but insufficient for accurate phylogenetic inferences in highly diverse taxa such as haemosporidians. Recent studies have utilized multiple mitochondrial genes (cyt b, cox1 and cox3), sometimes combined with a few apicoplast and nuclear genes. These studies have been highly successful with one notable exception: the evolutionary relationships of the genus Haemoproteus remain unresolved. Here we describe the transcriptome of Haemoproteus columbae and investigate its phylogenetic position recovered from a multi-gene dataset (600 genes). This genomic approach restricts the taxon sampling to 18 species of apicomplexan parasites. We employed Bayesian inference and maximum likelihood methods of phylogenetic analyses and found H. columbae and a representative from the subgenus Parahaemoproteus to be sister taxa. This result strengthens the hypothesis of genus Haemoproteus being monophyletic; however, resolving this question will require sequences of orthologs from, in particular, representatives of Leucocytozoon species.

Keywords

Haemoproteus Phylogenetics Transcriptome Avian parasitology 

Notes

Acknowledgements

This work was supported by Research Council of Lithuania (Grant MIP-045/2015). This study was also supported by the grant to RNMS, NIH 1SC3GM118210-01A1. The authors would like to thank Elvin J. Lauron, Bradley Bowser and Dr. Frank Cipriano for helping in planning rna-seq and project logistics. We are grateful to Dr. Greg Spicer, Andrew Ontano, Dr. Emily Jane McTavish and Trent Liu for assistance on phylogenetic and scripting advisement.

Supplementary material

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Supplementary material 1 (XLSX 28 KB)
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Supplementary material 2 (TXT 182 KB)
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Supplementary material 3 (PHY 1153 KB)
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Supplementary material 4 (PHY 3483 KB)

References

  1. Adriano EA, Cordeiro NS (2001) Prevalence and intensity of Haemoproteus columbae in three species of wild doves from Brazil. Mem Inst Oswaldo Cruz 96(2):175–178CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410CrossRefGoogle Scholar
  3. Auburn S, Campino S, Clark TG, Djimde AA, Zongo I, Manske M, Mangano V, Alcock D, Anastasi E, Maslen G, MacInnis B, Rockett K, Modiano D, Newbold CI, Doumbo OK, Ouédrago JB, Kwiatkowski DP (2011) An effective method to purify Plasmodium falciparum DNA directly from clinical blood samples for whole genome high-throughput sequencing. PLoS ONE 6(7):4–11CrossRefGoogle Scholar
  4. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Miller JA, Nayak V, Pennington C, Pinney DF, Roos DS, Ross C, Stoekert CJ Jr, Treatman C, Wang H (2008) PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 37(Suppl_1):D539–D543PubMedPubMedCentralGoogle Scholar
  5. Babraham Bioinformatics (2017) http://www.bioinformatics.babraham.ac.uk/
  6. Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9(5):1353–1358CrossRefGoogle Scholar
  7. Bensch S, Canbäck B, DeBarry JD, Johansson T, Hellgren O, Kissinger JC, Palinauskas V, Videvall E, Valkiūnas G (2016) The Genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. Genome Biol Evol 8(5):1361–1373CrossRefGoogle Scholar
  8. Böehme U, Otto TD, Cotton J, Steinbiss S, Sanders M, Oyola SO, Nicot A, Gandon S, Patra KP, Herd C, Bushell E, Modrzynska KK, Billker O, Vinetz JM, Rivero A, Newbold CI, Berriman M (2018) Complete avian malaria parasite genomes reveal host-specific parasite evolution in birds and mammals. Genome Res 28:547–560CrossRefGoogle Scholar
  9. Borner J, Pick C, Thiede J, Kolawole OM, Kingsley MT, Schulze J, Cottontail VM, Wellinghausen N, Schmidt-Chanasit J, Burmester T (2016) Phylogeny of haemosporidian blood parasites revealed by a multi-gene approach. Mol Phylogenet Evol 94:221–231CrossRefGoogle Scholar
  10. Bozdech Z, Llinás M, Pulliam BL, Wong ED, Zhu J, DeRisi JL (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1(1):e5CrossRefGoogle Scholar
  11. Carlson JS, Martínez-Gómez JE, Valkiūnas G, Loiseau C, Bell DA, Sehgal RN (2013) Diversity and phylogenetic relationships of hemosporidian parasites in birds of Socorro Island, México, and their role in the re-introduction of the Socorro Dove (Zenaida graysoni). J Parasitol 99(2):270–276CrossRefGoogle Scholar
  12. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17(4):540–552CrossRefGoogle Scholar
  13. Dimitrov D, Palinauskas V, Iezhova TA, Bernotienė R, Ilgūnas M, Bukauskaitė D, Zehtindjiev P, Ilieva M, Shapoval AP, Bolshakov CV, Markovets MY, Bensch B, Valkiūnas G (2015) Plasmodium spp.: an experimental study on vertebrate host susceptibility to avian malaria. Exp Parasitol 148:1–16CrossRefGoogle Scholar
  14. Earlé RA, Bastianello SS, Bennett GF, Krecek RC (1993) Histopathology and morphology of the tissue stages of Haemoproteus columbae causing mortality in Columbiformes. Avian Pathol 22(1):67–80CrossRefGoogle Scholar
  15. Gajria B, Bahl A, Brestelli J, Dommer J, Fischer S, Gao X, Heiges M, Iodice J, Kissinger JC, Mackey AJ, Pinney DF, Roos DS, Stoeckert CJ, Jr, Wang H, Brunk BP (2007) ToxoDB: an integrated Toxoplasma gondii database resource. Nucl Acids Res 36(suppl_1):D553–D556CrossRefGoogle Scholar
  16. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan M, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DMA, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498CrossRefGoogle Scholar
  17. Garnham PCC (1966) Malaria parasites and other haemosporidia. In: Malaria parasites and other haemosporidia. Wiley, HobokenGoogle Scholar
  18. Grech K, Watt K, Read AF (2006) Host–parasite interactions for virulence and resistance in a malaria model system. J Evol Biol 19(5):1620–1630CrossRefGoogle Scholar
  19. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity. Nat Protoc 8(8):1494CrossRefGoogle Scholar
  20. Hellgren O, Waldenström J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90(4):797–802CrossRefGoogle Scholar
  21. Hellgren O, Križanauskiene A, Valkiūnas G, Bensch S (2007) Diversity and phylogeny of mitochondrial cytochrome B lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). J Parasitol 93(4):889–896CrossRefGoogle Scholar
  22. Hellgren O, Kutzer M, Bensch S, Valkiūnas G, Palinauskas V (2013) Identification and characterization of the merozoite surface protein 1 (msp1) gene in a host-generalist avian malaria parasite, Plasmodium relictum (lineages SGS1 and GRW4) with the use of blood transcriptome. Malaria J 12(1):381CrossRefGoogle Scholar
  23. Jasper MA, Hull JM, Hull AC, Sehgal RNM (2014) Widespread lineage diversity of Leucocytozoon blood parasites in distinct populations of western Red-tailed Hawks. J Ornithol 155(3):767–775CrossRefGoogle Scholar
  24. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, Mclnerney JO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6(1):29CrossRefGoogle Scholar
  25. Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360CrossRefGoogle Scholar
  26. Lauron EJ, Oakgrove KS, Tell LA, Biskar K, Roy SW, Sehgal RN (2014) Transcriptome sequencing and analysis of Plasmodium gallinaceum reveals polymorphisms and selection on the apical membrane antigen-1. Malaria Journal 13(1):382CrossRefGoogle Scholar
  27. Lauron EJ, Loiseau C, Bowie RC, Spicer GS, Smith TB, Melo M, Sehgal RN (2015) Coevolutionary patterns and diversification of avian malaria parasites in African sunbirds (Family Nectariniidae). Parasitology 142(5):635–647CrossRefGoogle Scholar
  28. Lee SA, Chan CH, Tsai CH, Lai JM, Wang FS, Kao CY, Huang CYF (2008) Ortholog-based protein-protein interaction prediction and its application to inter-species interactions. BMC Bioinform 9(12):S11CrossRefGoogle Scholar
  29. Lefèvre T, Sanchez M, Ponton F, Hughes D, Thomas F (2007) Virulence and resistance in malaria: who drives the outcome of the infection? Trends Parasitol 23(7):299–302CrossRefGoogle Scholar
  30. Levin II, Valkiūnas G, Santiago-Alarcón D, Cruz LL, Iezhova TA, O’Brien SL, Hailer F, Dearborn D, Schreiber EA, Fleischer RC, Ricklefs RE, Parker PG (2012) Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: evidence from molecular and morphological studies, with a description of Haemoproteus iwa. Int J Parasitol 41(10):1019–1027CrossRefGoogle Scholar
  31. Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659CrossRefGoogle Scholar
  32. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Ndjango JN, Sanz CM, Morgan DB, Locatelli S, Gonder MK, Kranzusch PJ, Walsh PD, Delaporte E, Mpoudi-Ngole E, Georgiev AV, Muller MN, Shaw GM, Peeters M, Sharp PM, Rayner JC, Hahn BH (2010) Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467(7314):420CrossRefGoogle Scholar
  33. Lutz HL, Patterson BD, Peterhans JCK, Stanley WT, Webala PW, Gnoske TP, Hackett SJ, Stanhope MJ (2016) Diverse sampling of East African haemosporidians reveals chiropteran origin of malaria parasites in primates and rodents. Mol Phylogenet Evol 99:7–15CrossRefGoogle Scholar
  34. Martinez C, Marzec T, Smith CD, Tell LA, Sehgal RN (2013) Identification and expression of maebl, an erythrocyte-binding gene, in Plasmodium gallinaceum. Parasitol Res 112(3):945–954CrossRefGoogle Scholar
  35. Martinez-de la Puente, J, Martinez J, Aguilar RD, Herrero J, Merino S (2011) On the specificity of avian blood parasites: revealing specific and generalist relationships between haemosporidians and biting midges. Mol Ecol 20(15):3275–3287CrossRefGoogle Scholar
  36. Martinsen ES, Perkins SL, Schall JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Mol Phylogenet Evol 47(1):261–273CrossRefGoogle Scholar
  37. Mbengue A, Bhattacharjee S, Pandharkar T, Liu H, Estiu G, Stahelin RV, Rizk S, Njimoh DL, Ryan Y, Kesinee C, Nguon C, Ghorbal M, Lopez-Rubio J, Pfrender M, Emrich S, Mohandas N, Dondorp AM, Wiest O, Haldar K (2015) A molecular mechanism of artemisinin resistance in Plasmodium falciparum malaria. Nature 520(7549):683CrossRefGoogle Scholar
  38. National Center for Biotechnology Information (NCBI)[Internet] (2017) Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information; Accessed Apr 12 2017Google Scholar
  39. Neher RA, Bedford T, Daniels RS, Russell CA, Shraiman BI (2016) Prediction, dynamics, and visualization of antigenic phenotypes of seasonal influenza viruses. Proc Natl Acad Sci USA 113(12):E1701–E1709CrossRefGoogle Scholar
  40. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302(1):205–217CrossRefGoogle Scholar
  41. Otto TD, Wilinski D, Assefa S, Keane TM, Sarry LR, Böhme U, Lemieux J, Barrell B, Pain A, Berriman M, Newbold C, Llinas M (2010) New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-SEq. Mol Microbiol 76(1):12–24CrossRefGoogle Scholar
  42. Outlaw DC, Ricklefs RE (2014) Species limits in avian malaria parasites (Haemosporida): how to move forward in the molecular era. Parasitology 141(10):1223–1232CrossRefGoogle Scholar
  43. Oyola SO, Gu Y, Manske M, Otto TD, Alcock D, Macinnis B, Berriman M, Newbold CI, Kwiatkowski DP, Swerdlow HP, Quail MA (2012) Efficient depletion of Host DNA contamination in malaria clinical sequencing. J Clin Microbiol 51(3):745–751CrossRefGoogle Scholar
  44. Pacheco MA, Matta NE, Valkiunas G, Parker PG, Mello B, Stanley CE Jr, Lenino M, Garcia-Amado MA, Cranfield M, Pond SLK, Escalante AA (2017) Mode and rate of evolution of haemosporidian mitochondrial genomes: timing the radiation of avian parasites. Mol Biol Evol 35(2):383–403CrossRefGoogle Scholar
  45. Pacheco MA, Cepeda AS, Bernotienė R, Lotta IA, Matta NE, Valkiūnas G, Escalante AA (2018) Primers targeting mitochondrial genes of avian haemosporidians: PCR detection and differential DNA amplification of parasites belonging to different genera. Int J Parasitol 48(8):657–670CrossRefGoogle Scholar
  46. Palinauskas V, Valkiūnas G, Bolshakov CV, Bensch S (2008) Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Exp Parasitol 120(4):372–380CrossRefGoogle Scholar
  47. Palinauskas V, Iezhova TA, Križanauskienė A, Markovets MY, Bensch S, Valkiūnas G (2013) Molecular characterization and distribution of Haemoproteus minutus (Haemosporida, Haemoproteidae): a pathogenic avian parasite. Parasitol Int 62(4):358–363CrossRefGoogle Scholar
  48. Palinauskas V, Žiegytė R, Ilgūnas M, Iezhova TA, Bernotienė R, Bolshakov C, Valkiūnas 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. Int J Parasitol 45(1):51–62CrossRefGoogle Scholar
  49. Parker IM, Saunders M, Bontrager M, Weitz AP, Hendricks R, Magarey R, Suiter K, Gilbert GS (2015) Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520(7548):542–544CrossRefGoogle Scholar
  50. Perkins SL (2008) Molecular systematics of the three mitochondrial protein-coding genes of malaria parasites: corroborative and new evidence for the origins of human malaria: full-length research article. DNA Seq 19(6):471–478CrossRefGoogle Scholar
  51. Perkins SL (2014) Malaria’s many mates: past, present, and future of the systematics of the order Haemosporida. J Parasitol 100(1):11–25CrossRefGoogle Scholar
  52. PiroplasmaDB (2014), http://piroplasmadb.org
  53. Puiu D, Enomoto S, Buck GA, Abrahamsen MS, Kissinger JC (2004) CryptoDB: the Cryptosporidium genome resource. Nucleic Acids Res 32:D329–D331CrossRefGoogle Scholar
  54. Rao VS, Srinivas K, Sujini GN, Kumar GN (2014) Protein-protein interaction detection: methods and analysis. Int J Proteomics 2014:147648CrossRefGoogle Scholar
  55. Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc Lond B 269(1494):885–892CrossRefGoogle Scholar
  56. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574CrossRefGoogle Scholar
  57. Santiago-Alarcón D, Outlaw DC, Ricklefs RE, Parker PG (2010) Phylogenetic relationships of haemosporidian parasites in New World Columbiformes, with emphasis on the endemic Galapagos dove. Int J Parasitol 40(4):463–470CrossRefGoogle Scholar
  58. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313CrossRefGoogle Scholar
  59. Sukumaran J, Holder MT (2010) DendroPy: a Python library for phylogenetic computing. Bioinformatics 26(12):1569–1571CrossRefGoogle Scholar
  60. Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca RatonGoogle Scholar
  61. Valkiūnas G, Iezhova TA (2017) Exo-erythrocytic development of avian malaria and related haemosporidian parasites. Malaria J 16(1):101CrossRefGoogle Scholar
  62. Valkiūnas G, Iezhova TA, Loiseau C, Chasar A, Smith TB, Sehgal RN (2008a) New species of haemosporidian parasites (Haemosporida) from African rainforest birds, with remarks on their classification. Parasitol Res 103(5):1213CrossRefGoogle Scholar
  63. Valkiūnas G, Zehtindjiev P, Dimitrov D, Križanauskienė A, Iezhova TA, Bensch S (2008b) Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitol Res 102(6):1185–1193CrossRefGoogle Scholar
  64. Valkiūnas G, Santiago-Alarcón D, Levin II, Iezhova TA, Parker PG (2010) A new Haemoproteus species (Haemosporida: Haemoproteidae) from the endemic Galapagos dove Zenaida galapagoensis, with remarks on the parasite distribution, vectors, and molecular diagnostics. J Parasitol 96(4):783–792CrossRefGoogle Scholar
  65. Valkiūnas G, Ilgūnas M, Bukauskaitė D, Žiegytė R, Bernotienė R, Jusys V, Eigirdas V, Fragner K, Weissenböck H, Iezhova TA (2016) Plasmodium delichoni n. sp.: description, molecular characterisation and remarks on the exoerythrocytic merogony, persistence, vectors and transmission. Parasitol Res 115(7):2625–2636CrossRefGoogle Scholar
  66. Videvall E (2018) Plasmodium parasites of birds have the most AT-rich genes of eukaryotes. Microb Genomics 4:1–9CrossRefGoogle Scholar
  67. Videvall E, Cornwallis CK, Palinauskas V, Valkiūnas G, Hellgren O (2015) The avian transcriptome response to malaria infection. Mol Biol Evol 32(5):1255–1267CrossRefGoogle Scholar
  68. Videvall E, Cornwallis CK, Ahrén D, Palinauskas V, Valkiūnas G, Hellgren O (2017) The transcriptome of the avian malaria parasite Plasmodium ashfordi displays host-specific gene expression. Mol Ecol 26(11):2939–2958CrossRefGoogle Scholar
  69. Waite JL, Henry AR, Adler FR, Clayton DH (2012) Sex-specific effects of an avian malaria parasite on an insect vector: support for the resource limitation hypothesis. Ecology 93(11):2448–2455CrossRefGoogle Scholar
  70. Waite JL, Henry AR, Owen JP, Clayton DH (2014) An experimental test of the effects of behavioral and immunological defenses against vectors: do they interact to protect birds from blood parasites? Parasites Vectors 7(1):104CrossRefGoogle Scholar
  71. Waldenström J, Bensch S, Kiboi S, Hasselquist D, Ottosson U (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol 11(8):1545–1554CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Jasper Toscani Field
    • 1
    Email author
  • Josh Weinberg
    • 1
  • Staffan Bensch
    • 2
  • Nubia E. Matta
    • 3
  • Gediminas Valkiūnas
    • 4
  • Ravinder N. M. Sehgal
    • 1
  1. 1.Department of BiologySan Francisco State UniversitySan FranciscoUSA
  2. 2.Department of BiologyLund UniversityLundSweden
  3. 3.Sede Bogotá, Facultad de Ciencias, Departamento de Biología, Grupo de Investigación Caracterización genética e inmunologíaUniversidad Nacional de ColombiaBogotáColombia
  4. 4.Nature Research CentreVilnius 21Lithuania

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