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Next-generation sequencing reveals cryptic mtDNA diversity of Plasmodium relictum in the Hawaiian Islands

Published online by Cambridge University Press:  19 August 2013

S. I. JARVI ,
M. E. FARIAS ,
D. A. LAPOINTE ,
M. BELCAID  and
C. T. ATKINSON
S. I. JARVI*
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, 34 Rainbow Drive, Hilo, HI 96720, USA
M. E. FARIAS
Affiliation:
Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, 34 Rainbow Drive, Hilo, HI 96720, USA
D. A. LAPOINTE
Affiliation:
U.S. Geological Survey, Pacific Island Ecosystems Research Center, Kilauea Field Station, P.O. Box 44, Building 343, Hawaii National Park, HI 96718, USA
M. BELCAID
Affiliation:
Information and Computer Sciences Department, University of Hawaii at Manoa, Pacific Ocean Science and Technology Building, Room 317, 1680 East-West Road, Honolulu, HI 96822, USA
C. T. ATKINSON
Affiliation:
U.S. Geological Survey, Pacific Island Ecosystems Research Center, Kilauea Field Station, P.O. Box 44, Building 343, Hawaii National Park, HI 96718, USA
*
*Corresponding author. Department of Pharmaceutical Sciences, Daniel K. Inouye College of Pharmacy, University of Hawaii at Hilo, 34 Rainbow Drive, Hilo, HI 96720, USA. E-mail: [email protected]
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Summary

Next-generation 454 sequencing techniques were used to re-examine diversity of mitochondrial cytochrome b lineages of avian malaria (Plasmodium relictum) in Hawaii. We document a minimum of 23 variant lineages of the parasite based on single nucleotide transitional changes, in addition to the previously reported single lineage (GRW4). A new, publicly available portal (Integroomer) was developed for initial parsing of 454 datasets. Mean variant prevalence and frequency was higher in low elevation Hawaii Amakihi (Hemignathus virens) with Avipoxvirus-like lesions (P = 0·001), suggesting that the variants may be biologically distinct. By contrast, variant prevalence and frequency did not differ significantly among mid-elevation Apapane (Himatione sanguinea) with or without lesions (P = 0·691). The low frequency and the lack of detection of variants independent of GRW4 suggest that multiple independent introductions of P. relictum to Hawaii are unlikely. Multiple variants may have been introduced in heteroplasmy with GRW4 or exist within the tandem repeat structure of the mitochondrial genome. The discovery of multiple mitochondrial lineages of P. relictum in Hawaii provides a measure of genetic diversity within a geographically isolated population of this parasite and suggests the origins and evolution of parasite diversity may be more complicated than previously recognized.

Keywords

mtDNAavian malariaHawaiiPlasmodium relictumnext generation sequencingIntegroomer
Type
Research Article
Information
Parasitology , Volume 140 , Issue 14 , December 2013 , pp. 1741 - 1750
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Atkinson, C. T. and Lapointe, D. A. (2009). Ecology and pathogenicity of avian malaria and pox. In Conservation Biology of Hawaiian Forest Birds: Implications for Island Avifauna (ed. Pratt, T. K., Atkinson, C. T., Banko, P. C., Jacobi, J. D. and Woodworth, B. L.), pp. 234–252. Yale University Press, New Haven, CT, USA.Google Scholar
Atkinson, C. T., Dusek, R. J. and Lease, J. K. (2001). Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawai'i Amakihi. Journal of Wildlife Diseases 37, 20–27.CrossRefGoogle Scholar
Beadell, J. S., Ishtiaq, F., Covas, R., Melo, M., Warren, B. H., Atkinson, C. T., Bensch, S., Graves, G. R., Jhala, Y. V., Peirce, M. A., Rahmani, A. R., Fonseca, D. M. and Fleischer, R. C. (2006). Global phylogeographic limits of Hawai'i's avian malaria. Proceedings of the Royal Society of London Series B 273, 2935–2944.Google Scholar
Bensch, S., Stjernman, M., Hasselquist, D., Ostman, O., Hansson, B., Westerdahl, H. and Torres-Pinheiro, R. (2000). Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London Series B 267, 1583–1589.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Blankenberg, D., Von Kuster, G., Coraor, N., Ananda, G., Lazarus, R., Mangan, M., Nekrutenko, A. and Taylor, J. (2010). Galaxy: a web-based genome analysis tool for experimentalists. Current Protocols in Molecular Biology 19.10, 1–21.Google Scholar
Conway, D. J. (2007). Molecular epidemiology of malaria. Clinical Microbiology Reviews 20, 188–204.CrossRefGoogle ScholarPubMed
Divo, A. A., Geary, T. G., Jenson, J. B. and Ginsburg, H. (1985). The mitochondrion of Plasmodium falciparum visualized by rhodamine 123 fluorescence. Journal of Protozoology 32, 442–446.CrossRefGoogle ScholarPubMed
Ekala, M., Khim, N., Legrand, E., Randrianarivelojosia, M., Jambou, R., Fandeur, T., Menard, D., Assi, A., Henry, M., Rogier, C., Bouchier, C. and Mercereau-Puijalon, O. (2007). Sequence analysis of Plasmodium falciparum cytochrome b in multiple geographic sites. Malaria Journal 6, 164. doi:10.1186/1475-2875-6-164.CrossRefGoogle ScholarPubMed
Ewing, B. and Green, P. (1998). Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Research 8, 186–194. PMID 9521922.CrossRefGoogle ScholarPubMed
Farias, M. E. M., Atkinson, C. T., LaPointe, D. A. and Jarvi, S. I. (2012). Analysis of the trap gene provides evidence for the role of elevation and vector abundance in the genetic diversity of Plasmodium relictum in Hawai'i. Malaria Journal 11, 305.CrossRefGoogle Scholar
Feagin, J. E. (1992). The 6 kb element of Plasmodium falciparum encodes mitochondrial genes. Molecular and Biochemical Parasitology 52, 145–148.CrossRefGoogle Scholar
Hartl, D. L. and Clark, A. G. (1997). Principles of Population Genetics, 3rd Edn. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Hellgren, O., Krizanauskiene, A., Valkiūnas, G. and Bensch, S. (2007). Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoprotidae). Journal of Parasitology 93, 889–896.CrossRefGoogle Scholar
Hopkins, J., Fowler, R., Krischna, S., Wison, I., Mitchell, G. and Bannister, L. (1999). The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist 150, 283–295.CrossRefGoogle ScholarPubMed
Hunt, P., Fawcett, R., Carter, R. and Walliker, D. (2005). Estimating SNP proportions in populations of malaria parasites by sequencing: validation and applications. Molecular and Biochemical Parasitology 143, 173–182.CrossRefGoogle ScholarPubMed
Jarvi, S. I., Farias, M. E. M. and Atkinson, C. T. (2008). Genetic characterization of Hawaiian isolates of Plasmodium relictum reveals mixed-genotype infections. Biology Direct 3, 25.CrossRefGoogle ScholarPubMed
Kapoor, A., Jones, M., Shafer, R. W., Rhee, S. Y., Kazanjian, P. and Delwart, E. L. (2004). Sequencing-based detection of low-frequency human immunodeficiency virus type 1 drug-resistance mutants by an RNA/DNA heteroduplex generator-tracking assay. Journal of Virology 78, 7112–7123.CrossRefGoogle ScholarPubMed
Korsinczky, M., Chen, N., Kotecka, B., Saul, A., Rieckmann, K. and Cheng, Q. (2000). Mutations in Plasmodium falciparum cytochrome b that are associated with atovaquone resistance are located at a putative drug-binding site. Antimicrobial Agents and Chemotherapy 44, 2100–2108.CrossRefGoogle Scholar
Lindner, D. L. and Banik, M. T. (2009). Effects of cloning and root-tip size on observations of fungal ITS sequences from Picea glauca roots. Mycologia 101, 157–165.CrossRefGoogle ScholarPubMed
Omori, S., Sata, Y., Isobe, T., Yukawa, M. and Murata, K. (2007). Complete nucleotide sequences of the mitochondrial genomes of two avian malaria protozoa, Plasmodium gallinaceum and Plasmodium juxtanucleare. Parasitology Research 100, 661–664.CrossRefGoogle ScholarPubMed
Perez-Tris, J. and Bensch, S. (2005). Diagnosing genetically diverse avian malaria infections using mixed-sequence analysis and TA-cloning. Parasitology 131, 15–23.CrossRefGoogle ScholarPubMed
Richly, E. and Leister, D. (2004). NUMTs in sequenced eukaryotic genomes. Molecular Biology and Evolution 21, 1081–1084.CrossRefGoogle ScholarPubMed
Ricklefs, R. E. and Outlaw, D. C. (2010). A molecular clock for malaria parasites. Science 329, 226.CrossRefGoogle ScholarPubMed
Robson, K. J. H., Hall, J. R. S., Davies, L. C., Crisanti, A., Hill, A. V. S. and Wellems, T. E. (1990). Polymorphism of the TRAP gene of Plasmodium falciparum. Proceedings of the Royal Society B: Biological Science 242, 205–216.Google ScholarPubMed
Roche Diagnostics GmbH (2009). Amplicon fusion primer design guidelines for GS FLX Titanium. Series Lib-A Chemistry TCB No. 013-2009.Google Scholar
Schmieder, R. and Edwards, R. (2011). Quality control and preprocessing of metagenomic datasets. Bioinformatics 27, 863–864.CrossRefGoogle ScholarPubMed
Schwobel, B., Alifrangis, M., Salanti, A. and Jelinek, T. (2003). Different mutation patterns of atovaquone resistance to Plasmodium falciparum in vitro and in vivo: rapid detection of codon 268 polymorphisms in the cytochrome b as potential in vivo resistance marker. Malaria Journal 2, 5.CrossRefGoogle ScholarPubMed
Sharma, I., Pasha, P. T. and Sharma, Y. D. (1998). Complete nucleotide sequence of the Plasmodium vivax 6 kb element. Molecular and Biochemical Parasitology 97, 259–263.CrossRefGoogle ScholarPubMed
Smith, S. A. and Kotwal, G. J. (2002). Immune response to poxvirus infections in various animals. Critical Reviews in Microbiology 28, 149–185.CrossRefGoogle ScholarPubMed
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Vaidya, A. B. and Arasu, P. (1987). Tandemly arranged gene clusters of malarial parasites that are highly conserved and transcribed. Molecular and Biochemical Parasitology 22, 249–257.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Iezhova, T. A., Loiseau, C., Smith, T. B. and Sehgal, R. N. M. (2009). New malaria parasites of the subgenus Novyella in African rainforest birds, with remarks on their high prevalence, classification and diagnostics. Parasitology Research 104, 1061–1077.CrossRefGoogle ScholarPubMed
van Riper, C. III, van Riper, S. G., Goff, M. L. and Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327–344.CrossRefGoogle Scholar
van Riper, C. III, van Riper, S. G. and Hansen, W. R. (2002). Epizootiology and effect of avian pox on Hawaiian forest birds. Auk 119, 929–942.CrossRefGoogle Scholar
Woodworth, B., Atkinson, C. T., LaPointe, D. A., Hart, P. J., Spiegel, C. S., Tweed, E. J., Henneman, C., LeBrun, J., Denette, T., DeMots, R., Kozar, K. L., Triglia, D., Lease, D., Gregor, A., Smith, T. and Duffy, D. (2005). Host population persistence in the face of introduced vector-borne diseases: Hawai'i Amakihi and avian malaria. Proceedings of the National Academy of Sciences USA 102, 1531–1536.CrossRefGoogle Scholar