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Trypanosomatid biodiversity in Costa Rica: genotyping of parasites from Heteroptera using the spliced leader RNA gene

Published online by Cambridge University Press:  05 October 2004

S. J. WESTENBERGER ,
N. R. STURM ,
D. YANEGA ,
S. A. PODLIPAEV ,
R. ZELEDÓN ,
D. A. CAMPBELL  and
D. A. MASLOV
S. J. WESTENBERGER
Affiliation:
Department of Microbiology, Immunology and Molecular Genetics, David Geffen School of Medicine, University of California – Los Angeles, Los Angeles, CA 90095-1487, USA
N. R. STURM
Affiliation:
Department of Microbiology, Immunology and Molecular Genetics, David Geffen School of Medicine, University of California – Los Angeles, Los Angeles, CA 90095-1487, USA
D. YANEGA
Affiliation:
Department of Entomology and Entomology Research Museum, University of California – Riverside, Riverside, CA 92521, USA Zoological Institute, Russian Academy of Sciences, 199034 St. Petersburg, Russia
S. A. PODLIPAEV
Affiliation:
Zoological Institute, Russian Academy of Sciences, 199034 St. Petersburg, Russia
R. ZELEDÓN
Affiliation:
School of Veterinary Medicine, National University, Heredia, Costa Rica
D. A. CAMPBELL
Affiliation:
Department of Microbiology, Immunology and Molecular Genetics, David Geffen School of Medicine, University of California – Los Angeles, Los Angeles, CA 90095-1487, USA
D. A. MASLOV
Affiliation:
Department of Biology, University of California – Riverside, Riverside, CA 92521, USA
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Abstract

The biodiversity of insect trypanosomes is largely unknown, resulting in significant gaps in the understanding of pathogen evolution. A culture-independent preliminary survey of trypanosomatid fauna was conducted for the parasites of Heteroptera (Hemiptera) from several localities in Costa Rica. Trypanosomatid infections were detected by light microscopy of smeared gut contents. Out of 257 insects representing 6 families, infections were found in 62 cases; cultures were obtained for 29 new isolates. Gut material from infected hosts was preserved in the field using an SDS–EDTA buffer solution for subsequent DNA extraction in the laboratory. PCR amplification of the trypanosomatid-specific spliced leader (SL) RNA gene repeats was successful for 60 field samples. Eighteen distinct SL RNA typing units were identified in a set of 28 samples analysed in detail. Cluster analysis indicated that these typing units were unique and thus could represent new species and, in some cases, new genera. This study reveals only a minor fraction of the trypanosomatid biodiversity, which is anticipated to be high.

Keywords

Trypanosomatidaebiodiversitymini-exonSL RNAgenotyping
Type
Research Article
Information
Parasitology , Volume 129 , Issue 5 , November 2004 , pp. 537 - 547
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

BALDAUF, S. L. ( 2003). The deep roots of eukaryotes. Science 300, 1703–1706.CrossRefGoogle Scholar
BATISTOTI, M., CAVAZZANA, M. Jr., SERRANO, M. G., OGATTA, S. F., BACCAN, G. C., JANKEVICIUS, J. V., TEIXEIRA, M. M. G. & JANKEVICIUS, S. T. ( 2001). Genetic variability of trypanosomatids isolated from phytophagous Hemiptera defined by morphological, biochemical, and molecular taxonomic markers. Journal of Parasitology 87, 1335–1341.CrossRefGoogle Scholar
BRISSE, S., VERHOEF, J. & TIBAYRENC, M. ( 2001). Characterization of large and small subunit rRNA and mini-exon genes further supports the distinction of six Trypanosoma cruzi lineages. International Journal for Parasitology 31, 1218–1226.CrossRefGoogle Scholar
CAMPBELL, D. A., STURM, N. R. & YU, M. C. ( 2000). Transcription of the kinetoplastid spliced leader RNA gene. Parasitology Today 16, 78–82.CrossRefGoogle Scholar
CATARINO, L. M., SERRANO, M. G., CAVAZZANA, M. Jr., ALMEIDA, M. L., KANESHINA, E. K., CAMPANER, M., JANKEVICIUS, J. V., TEIXEIRA, M. M. G. & ITOW-JANKEVICIUS, S. ( 2001). Classification of trypanosomatids from fruits and seeds using morphological, biochemical and molecular markers revealed several genera among fruit isolates. FEMS Microbiology Letters 201, 65–72.CrossRefGoogle Scholar
CROAN, D. G., MORRISON, D. A. & ELLIS, J. T. ( 1997). Evolution of the genus Leishmania revealed by comparison of DNA and RNA polymerase gene sequences. Molecular and Biochemical Parasitology 89, 149–159.CrossRefGoogle Scholar
DOLLET, M. ( 1994). Identification and characterization of pest organisms: a plant trypanosomes case study. In Identification and Characterization of Pest Organisms ( ed. Hawksworth, D. L.), pp. 415–426. CAB International, Wallingford, UK.
DOLLET, M., STURM, N. R. & CAMPBELL, D. A. ( 2001). The spliced leader RNA gene array in phloem-restricted plant trypanosomatids (Phytomonas) partitions into two major groupings: epidemiological implications. Parasitology 122, 289–297.CrossRefGoogle Scholar
DOLLET, M., STURM, N. R., SÁNCHEZ-MORENO, M. & CAMPBELL, D. A. ( 2000). 5S ribosomal RNA gene repeat sequences define at least eight groups of plant trypanosomatids (Phytomonas spp.): phloem-restricted pathogens form a distinct section. Journal of Eukaryotic Microbiology 47, 569–574.Google Scholar
FERNANDES, O., DEGRAVE, W. & CAMPBELL, D. A. ( 1993). The mini-exon gene: a molecular marker for Endotrypanum schaudinni. Parasitology 107, 219–224.CrossRefGoogle Scholar
FERNANDES, O., MURTHY, V. K., KURATH, U., DEGRAVE, W. M. & CAMPBELL, D. A. ( 1994). Mini-exon gene variation in human pathogenic Leishmania species. Molecular and Biochemical Parasitology 66, 261–271.CrossRefGoogle Scholar
FERNANDES, O., SANTOS, S. S., CUPOLILLO, E., MENDONÇA, B., DERRE, R., JUNQUEIRA, A. C. V., SANTOS, L. C., STURM, N. R., NAIFF, R. D., BARRET, T. V. & CAMPBELL, D. A. ( 2001). A mini-exon multiplex polymerase chain reaction to distinguish the major groups of Trypanosoma cruzi and T. rangeli in the Brazilian Amazon. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 97–99.CrossRefGoogle Scholar
FERNANDES, O., SOUTO, R. P., CASTRO, J. A., PEREIRA, J. B., FERNANDES, N. C., JUNQUEIRA, A. C. V., NAIFF, R. D., BARRETT, T. V., DEGRAVE, W., ZINGALES, B., CAMPBELL, D. A. & COURA, J. R. ( 1998). Brazilian isolates of Trypanosoma cruzi from humans and triatomines classified into two lineages using mini-exon and ribosomal RNA sequences. American Journal of Tropical Medicine and Hygiene 58, 807–811.CrossRefGoogle Scholar
FERNANDES, O., TEIXEIRA, M. M., STURM, N. R., SOUSA, M. A., CAMARGO, E. P., DEGRAVE, W. M. & CAMPBELL, D. A. ( 1997). Mini-exon gene sequences define six groups within the genus Crithidia. Journal of Eukaryotic Microbiology 44, 535–539.CrossRefGoogle Scholar
GODOI, M. M. I., SERRANO, M. G., TEIXEIRA, M. M. G. & CAMARGO, E. P. ( 2002). A PCR-based survey on Phytomonas (Euglenozoa: Trypanosomatidae) in phytophagous hemipterans of the Amazon region. Journal of Eukaryotic Microbiology 49, 275–279.CrossRefGoogle Scholar
GRISARD, E. C., CAMPBELL, D. A. & ROMANHA, A. J. ( 1999). Mini-exon gene sequence polymorphism among Trypanosoma rangeli strains isolated from distinct geographical regions. Parasitology 118, 375–382.CrossRefGoogle Scholar
GRISARD, E. C., STURM, N. R. & CAMPBELL, D. A. ( 2003). A new species of trypanosomes isolated from South American bats, Trypanosoma desterrensis sp. n. Parasitology 127, 265–271.CrossRefGoogle Scholar
HAAG, J., O'HUIGIN, C. & OVERATH, P. ( 1998). The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology 91, 37–49.CrossRefGoogle Scholar
HARRIS, E., KROPP, G., BELLI, A., RODRIGUEZ, B. & AGABIAN, N. ( 1998). Single-step multiplex PCR assay for characterization of New World Leishmania complexes. Journal of Clinical Microbiology 36, 1989–1995.Google Scholar
HOLLAR, L., LUKEš, J. & MASLOV, D. A. ( 1998). Monophyly of endosymbiont containing trypanosomatids: phylogeny versus taxonomy. Journal of Eukaryotic Microbiology 45, 293–297.CrossRefGoogle Scholar
HOLLAR, L., MASLOV, D. A. ( 1997). A phylogenetic view on the genus Phytomonas. Molecular and Biochemical Parasitology 89, 295–299.CrossRefGoogle Scholar
JANKEVICIUS, S. I., DE ALMEIDA, M. L., JANKEVICIUS, J. V., CAVAZZANA, M. Jr., ATTIAS, M. & DE SOUZA, W. ( 1993). Axenic cultivation of trypanosomatids found in corn (Zea mays) and in phytophagous hemipterans (Leptoglossus zonatus Coreidae) and their experimental transmission. Journal of Eukaryotic Microbiology 40, 576–581.CrossRefGoogle Scholar
KUNZ, W. ( 2002). When is a parasite species a species? Trends in Parasitology 18, 121–124.Google Scholar
LOPEZ-GARCIA, P., PHILIPPE, H., GAILL, F. & MOREIRA, D. ( 2003). Autochthonous eukaryotic diversity in hydrothermal sediment and experimental micro-colonizers at the Mid-Atlantic Ridge. Proceedings of the National Academy of Sciences, USA 100, 697–702.CrossRefGoogle Scholar
LUKEš, J., JIRKŮ, M., DOLEŽEL, D., KRAL'OVÁ, I., HOLLAR, L. & MASLOV, D. A. ( 1997). Analysis of ribosomal RNA genes suggests that trypanosomes are monophyletic. Journal of Molecular Evolution 44, 521–527.CrossRefGoogle Scholar
MARCHE, S., ROTH, CH., PHILIPPE, H., DOLLET, M. & BALTZ, T. ( 1995). Characterization and detection of plant trypanosomatids by sequence analysis of the small subunit ribosomal RNA gene. Molecular and Biochemical Parasitology 71, 15–26.CrossRefGoogle Scholar
MARFURT, J., NASEREDDIN, A., NIEDERWIESER, I., JAFFE, C. L., BECK, H. P. & FELGER, I. ( 2003). Identification and differentiation of Leishmania species in clinical samples by PCR amplification of the miniexon sequence and subsequent restriction fragment length polymorphism analysis. Journal of Clinical Microbiology 41, 3147–3153.CrossRefGoogle Scholar
MASLOV, D. A., ELGORT, M. G., WONG, S., PECKOVÁ, H., LOM, J., SIMPSON, L. & CAMPBELL, D. A. ( 1993). Organization of mini-exon and 5S rRNA genes in the kinetoplastid Trypanoplasma borreli. Molecular and Biochemical Parasitology 61, 127–136.CrossRefGoogle Scholar
MERZLYAK, E., YURCHENKO, V., KOLESNIKOV, A. A., ALEXANDROV, K., PODLIPAEV, S. A. & MASLOV, D. A. ( 2001). Diversity and phylogeny of insect trypanosomatids based on small subunit rRNA genes: Polyphyly of Leptomonas and Blastocrithidia. Journal of Eukaryotic Microbiology 48, 161–169.CrossRefGoogle Scholar
MULLER, E., AHOMADEGBE, J., COULAUD, D., GARGANI, D., FERNANDEZ-BECERRA, C. & DOLLET, M. ( 1995). Variability of kinetoplast DNA from plant trypanosomatids responsible for Hartrot and Marchitez diseases. Phytopathology 85, 942–947.CrossRefGoogle Scholar
MULLER, E., GARGANI, D., SCHAEFFER, V., STEVENS, J., FERNANDEZ-BECERRA, C., SANCHEZ-MORENO, M. & DOLLET, M. ( 1994). Variability in the phloem restricted plant trypanosomes (Phytomonas spp) associated with wilts of cultivated crops. European Journal of Plant Pathology 100, 425–434.CrossRefGoogle Scholar
MURTHY, V. K., DIBBERN, K. M. & CAMPBELL, D. A. ( 1992). PCR amplification of mini-exon genes differentiates Trypanosoma cruzi and Trypanosoma rangeli. Molecular and Cellular Probes 6, 237–243.CrossRefGoogle Scholar
NOYES, H. A., ARANA, B. A., CHANCE, M. L. & MAINGON, R. ( 1997). The Leishmania hertigi (Kinetoplastida; Trypanosomatidae) complex and the lizard Leishmania: Their classification and evidence for a Neotropical origin of the Leishmania-Endotrypanum clade. Journal of Eukaryotic Microbiology 44, 511–517.CrossRefGoogle Scholar
NUNES, L. R., TEIXEIRA, M. M. G., CAMARGO, E. P. & BUCK, G. A. ( 1995). Sequence and structural characterization of the spliced leader genes and transcripts in Phytomonas. Molecular and Biochemical Parasitology 74, 233–237.CrossRefGoogle Scholar
PODLIPAEV, S. A. ( 1990). Catalogue of World Fauna of Trypanosomatidae (Protozoa). Leningrad, USSR.
PODLIPAEV, S. A., STURM, N. R., FIALA, I., FERNANDES, O., WESTENBERGER, S. J., DOLLET, M., CAMPBELL, D. A. & LUKEš, J. ( 2004). Diversity of insect trypanosomatids assessed from the spliced leader RNA ans 5S rRNA genes and intergenic regions. Journal of Eukaryotic Microbiology 51, 283–290.CrossRefGoogle Scholar
RAMOS, A., MASLOV, D. A., FERNANDES, O., CAMPBELL, D. A. & SIMPSON, L. ( 1996). Detection and identification of human pathogenic Leishmania and Trypanosoma species by hybridization of PCR-amplified mini-exon repeats. Experimental Parasitology 82, 242–250.CrossRefGoogle Scholar
SAITO, R. M., ELGORT, M. G. & CAMPBELL, D. A. ( 1994). A conserved upstream element is essential for transcription of the Leishmania tarentolae mini-exon gene. EMBO Journal 13, 5460–5469.Google Scholar
SAMBROOK, J., FRITSCH, E. F. & MANIATIS, T. ( 1989). Molecular Cloning – a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
SANTANA, D. M., LUKEš, J., STURM, N. R. & CAMPBELL, D. A. ( 2001). Two sequence classes of kinetoplastid 5S ribosomal RNA gene revealed among bodonid spliced leader RNA gene arrays. FEMS Microbiology Letters 204, 233–237.CrossRefGoogle Scholar
SBRAVATE, C., CAMPANER, M., CAMARGO, L. E. A., CONCHON, I., TEIXEIRA, M. & CAMARGO, E. P. ( 1989). Culture and generic identification of trypanosomatids of phytophagous Hemiptera in Brazil. Journal of Protozoology 36, 543–547.CrossRefGoogle Scholar
SERRANO, M. G., NUNES, L. R., CAMPANER, M., BUCK, G. A., CAMARGO, E. P. & TEIXEIRA, M. M. G. ( 1999). Trypanosomatidae: Phytomonas detection in plants and phytophagous insects by PCR amplification of a genus-specific sequence of the spliced leader gene. Experimental Parasitology 91, 268–279.CrossRefGoogle Scholar
SOUTO, R. P., FERNANDES, O., MACEDO, A. M., CAMPBELL, D. A. & ZINGALES, B. ( 1996). DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Molecular and Biochemical Parasitology 83, 141–152.CrossRefGoogle Scholar
STEVENS, J. R. ( 2001). One million insects – a lot of parasites? Trends in Parasitology 17, 119–120.Google Scholar
STEVENS, J. R., NOYES, H. A., DOVER, G. A. & GIBSON, W. C. ( 1999). The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118, 107–116.CrossRefGoogle Scholar
STURM, N. R., FERNANDES, O. & CAMPBELL, D. A. ( 1995). The mini-exon genes of three Phytomonas isolates that differ in plant tissue tropism. FEMS Microbiology Letters 130, 177–182.CrossRefGoogle Scholar
STURM, N. R., MASLOV, D. A., GRISARD, E. C. & CAMPBELL, D. A. ( 2001). Diplonema spp. possess spliced leader RNA genes similar to the Kinetoplastida. Journal of Eukaryotic Microbiology 48, 325–331.Google Scholar
SWOFFORD, D. L. ( 1998). PAUP* 4.0: Phylogenetic Analysis Using Parsimony (and Other Methods), beta version, 1998. Sinauer Associates, Inc., Sunderland, MA.
TEIXEIRA, M. M. G., SERRANO, M. G., NUNES, L. R., CAMPANER, M., BUCK, G. A. & CAMARGO, E. P. ( 1996). Trypanosomatidae: a spliced-leader-derived probe specific for genus Phytomonas. Experimental Parasitology 84, 311–319.CrossRefGoogle Scholar
THOMPSON, J. D., GIBSON, T. J., PLEWNIAK, F., JEANMOUGIN, F. & HIGGINS, D. G. ( 1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.CrossRefGoogle Scholar
TIBAYRENC, M. ( 1998). Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. International Journal for Parasitology 28, 85–104.CrossRefGoogle Scholar
TIBAYRENC, M., KJELLBERG, F. & AYALA, F. J. ( 1990). A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomical consequences. Proceedings of the National Academy of Sciences, USA 87, 2414–2418.CrossRefGoogle Scholar
WALLACE, F. G. ( 1966). The trypanosomatid parasites of insects and arachnids. Experimental Parasitology 18, 124–193.CrossRefGoogle Scholar
YU, M. C., ORLANDO, T. C., STURM, N. R., ZHONG, L., SAITO, R. M., FLOETER-WINTER, L. M. & CAMPBELL, D. A. ( 2002). Two distinct functional spliced leader RNA gene arrays in Leishmania tarentolae are found in several lizard Leishmania species. International Journal for Parasitology 32, 1411–1422.CrossRefGoogle Scholar