Advertisement

Parasitology Research

, Volume 109, Issue 1, pp 163–173 | Cite as

Species delimitation and phylogenetic relationships of Chinese Leishmania isolates reexamined using kinetoplast cytochrome oxidase II gene sequences

  • De-Ping Cao
  • Xian-Guang Guo
  • Da-Li ChenEmail author
  • Jian-Ping ChenEmail author
Original Paper

Abstract

Leishmaniasis is a geographically widespread disease caused by protozoan parasites belonging to the genus Leishmania and transmitted by certain species of sand fly. This disease still remains endemic in China, especially in the west and northwest frontier regions. A recent ITS1 phylogeny of Chinese Leishmania isolates has challenged some aspects for their traditional taxonomy and cladistic hypotheses of their phylogeny. However, disagreement with respect to relationships within Chinese Leishmania isolates highlights the need for additional data and analyses. Here, we test the phylogenetic relationships among Chinese isolates and their relatives by analyzing kinetoplast cytochrome oxidase II (COII) gene sequences, including 14 Chinese isolates and three isolates from other countries plus 17 sequences retrieved from GenBank. The COII gene might have experienced little substitution saturation, and its evolutionary process was likely to have been stationary, reversible, and homogeneous. Both neighbor-joining and Bayesian analyses reveal a moderately supported group comprising ten newly determined isolates, which is closely related to Leishmania tarentolae and Endotrypanum monterogeii. In combination with genetic distance analysis as well as Bayesian hypothesis testing, this further corroborates the occurrence of an undescribed species of Leishmania. Our results also suggest that (1) isolate MHOM/CN/93/GS7 and isolate IPHL/CN/77/XJ771 are Leishmania donovani; (2) isolate MHOM/CN/84/JS1 is Leishmania tropica; (3) the status referring to an isolate MRHO/CN/62/GS-GER20 from a great gerbil in Gansu, China, as Leishmania gerbilli, formerly based on multilocus enzyme electrophoresis, is recognized; and (4) E. monterogeii is nested within the genus Leishmania, resulting in a paraphyletic Leishmania. In addition, the results of this study enrich our understanding of the heterogeneity and relationships of Chinese Leishmania isolates.

Keywords

Visceral Leishmaniasis Leishmaniasis Leishmania Species COII Gene Bayesian Inference Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by the National Natural Science Foundations of China (30771883, 30800094), the National Project of Important Infectious Diseases (2008-ZX10004-011), and the Foundation for Young Teachers in Sichuan University (grant no. 07056). X-G Guo was supported by the National Natural Science Foundation of China (30700062).

References

  1. Ababneh F, Jermiin LS, Ma C, Robinson J (2006) Matched-pairs tests of homogeneity with applications to homologous nucleotide sequences. Bioinformatics 22:1225–1231PubMedCrossRefGoogle Scholar
  2. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723CrossRefGoogle Scholar
  3. Asato Y, Oshiro M, Myint CK, Yamamoto Y, Kato H, Marco JD, Mimori T, Gomez EA, HashiguchiY UH (2009) Phylogenic analysis of the genus Leishmania by cytochrome b gene sequencing. Exp Parasitol 121:352–361PubMedCrossRefGoogle Scholar
  4. Bañuls A-L, Hide M, Tibayrenc M (2002) Evolutionary genetics and molecular diagnosis of Leishmania species. Trans R Soc Trop Med Hyg 96(Suppl 1):S9–S13PubMedCrossRefGoogle Scholar
  5. Bañuls A-L, Hide M, Prugnolle F (2007) Leishmania and the leishmaniases: a parasite genetic update and advances in taxonomy, epidemiology and pathogenicity in humans. Adv Parasitol 64:1–109PubMedCrossRefGoogle Scholar
  6. Blom D, de Haan A, van den Berg M, Sloof P, Jirku M, Lukeš J, Benne R (1998) RNA editing in the free-living bodonid Bodo saltans. Nucleic Acids Res 26:1205–1213PubMedCrossRefGoogle Scholar
  7. Botilde Y, Laurent T, Quispe W, Chicharro C, Canavate C, Cruz I, Kuhls K, Schönian G, Dujardin JC (2006) Comparison of molecular markers of strain typing of Leishmania infantum. Infect Genet Evol 6:440–446PubMedCrossRefGoogle Scholar
  8. Bu L-Y, Hu X-S, Jing B-Q, Yi T-L (2000) Sequence analysis of SSU rDNA variable regions of Leishmania isolates from hilly foci and plain foci of China. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 18:321–324 (in Chinese with English abstract)PubMedGoogle Scholar
  9. Carstens BC, Knowles LL (2007) Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Syst Biol 56:400–411PubMedCrossRefGoogle Scholar
  10. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  11. de la Cruz VF, Neckelmann N, Simpson L (1984) Sequences of six genes and several open reading frames in the kinetoplast maxicircle DNA of Leishmania tarentolae. J Bio Chem 259:15136–15147Google Scholar
  12. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886PubMedCrossRefGoogle Scholar
  13. Desjeux P (2004) Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27:305–318PubMedCrossRefGoogle Scholar
  14. El Tai NO, El Fari M, Mauricio I, Miles MA, Oskam L, El Safi SH, Presber WH, Schönian G (2001) Leishmania donovani: intraspecific polymorphisms of Sudanese isolates revealed by PCR-based analyses and DNA sequencing. Exp Parasitol 97:35–44PubMedCrossRefGoogle Scholar
  15. Felsensten JP (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  16. Fraga J, Montalvo AM, de Doncker S, Dujardin J-C, der Auwera GV (2010) Phylogeny of Leishmania species based on the heat-shock protein 70 gene. Infect Genet Evol 10:238–245PubMedCrossRefGoogle Scholar
  17. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–511CrossRefGoogle Scholar
  18. Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224PubMedCrossRefGoogle Scholar
  19. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321CrossRefGoogle Scholar
  20. Ho JWK, Adams CE, Lew JB, Matthews TJ, Ng CC, Shahabi-Sirjan A, Tan LH, Zhao Y, Easteal S, Wilson SR, Jermin LS (2006) SeqVis: visualization of compositional heterogeneity in large alignments of nucleotides. Bioinformatics 22:2162–2163PubMedCrossRefGoogle Scholar
  21. Hu X-S, Bu L, Ma Y, Wang Y, Jing B, Yi T (2002) Difference in DNA sequences in SSU rDNA variable regions among pathogens isolated from different epidemic foci of visceral leishmaniasis in China. Chin Med J (Engl) 115:1457–1459Google Scholar
  22. Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51:673–688PubMedCrossRefGoogle Scholar
  23. Hughes L, Piontkivska H (2003) Phylogeny of Trypanosomatidae and Bodonidae (Kinetoplastida) based on 18S rRNA: evidence for paraphyly of Trpanosoma and six other genera. Mol Biol Evol 20:644–652PubMedCrossRefGoogle Scholar
  24. Ibrahim ME, Barker DC (2001) The origin and evolution of the Leishmania donovani complex as inferred from a mitochondrial cytochrome oxidase II gene sequence. Infect Genet Evol 1:61–68PubMedCrossRefGoogle Scholar
  25. Ibrahim ME, Mahdi MA, Bereir RE, Giha RS, Wasunna C (2008) Evolutionary conservation of RNA editing in the genus Leishmania. Infect Genet Evol 8:378–380PubMedCrossRefGoogle Scholar
  26. Jermiin LS, Jayaswal V, Ababneh F, Robinson J (2008) Phylogenetic model evaluation. In: Keith J (ed) Methods in molecular biology: bioinformatics. Humana, TotowaGoogle Scholar
  27. Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795CrossRefGoogle Scholar
  28. Kim KS, Teixeira SM, Kirchhoff LV, Donelson JE (1994) Transcription and editing of cytochrome oxidase II RNAs in Trypanosoma cruzi. J Biol Chem 269:1206–1211PubMedGoogle Scholar
  29. Knowles LL, Carstens BC (2007) Delimiting species without monophyletic gene trees. Syst Biol 56:887–895PubMedCrossRefGoogle Scholar
  30. Lin Y-C, Hsu J-Y, Hsu S-J, Chi Y, Chiang S-C, Lee S-T (2008) Two distinct arsenite-resistant variants of Leishmania amazonensis take different routes to achieve resistance as revealed by comparative transcriptomics. Mol Biochem Parasitol 162:16–31PubMedCrossRefGoogle Scholar
  31. Lu H-G, Hu X-S (1988) Identification of Leishmania by dot blot hybridization with photobiotin labelled kDNA. J West China Univ Med Sci 19:222–225 (in Chinese with English abstract)Google Scholar
  32. Lu H-G, Hu X-S (1990) Identification of Leishmania by kinetoplast DNA minicircle and cloning of minicircle. Chin Med J (Engl) 103:418–423Google Scholar
  33. Lu H-G, Zhong L, Guan L-R, Qu J-Q, Hu X-S, Chai J-C, Xu Z-B, Wang C-T, Chang K-P (1994) Separation of Chinese Leishmania isolates into five genotypes by kinetoplast and chromosomal DNA heterogeneity. Am J Trop Med Hyg 50:763–770PubMedGoogle Scholar
  34. Lu F-L, Hu X-S, Jing B-Q, Luo P, Lin F-Q (1997) Analysis of kDNA of Leishmania isolates from hill and plain foci of China. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 5:101–103 (in Chinese with English abstract)Google Scholar
  35. Lu F-L, Hu X-S, Jing B-Q, Ma Y (1998) Analysis of nuclear DNA gene types of Leishmania isolates from hilly and plain foci of China. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 16:432–435 (in Chinese with English abstract)PubMedGoogle Scholar
  36. Lu D-M, Hu X-S, Qiao Z-D (2001) Analysis of Leishmania species and strains from China by RAPD technique. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 19:290–293 (in Chinese with English abstract)PubMedGoogle Scholar
  37. Lu D-M, Hu X-S, Qiao Z-D, Ma Y (2002) Analysis of kDNA and nDNA of Leishmania by RAPD. Acta Parasitol Med Entomol Sin 9:1–6 (in Chinese with English abstract)Google Scholar
  38. Lukeš J, Mauricio IL, Schönian G, Dujardin J-C, Soteriadou K, Dedet J-P, Kuhls K, Tintaya KWQ, Jirků M, Chocholová E, Haralambous C, Pratlong F, Oborník M, Horák A, Ayala FJ, Miles MA (2007) Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy. Proc Natl Acad Sci USA 104:9375–9380PubMedCrossRefGoogle Scholar
  39. Maddison WP (1997) Gene trees in species trees. Syst Biol 46:523–536CrossRefGoogle Scholar
  40. Nebohacova M, KimCE SL, Maslov DA (2009) RNA editing and mitochondrial activity in promastigotes and amastigotes of Leishmania donovani. Int J Parasitol 39:635–644PubMedCrossRefGoogle Scholar
  41. Newton MA, Raftery AE (1994) Approximate Bayesian inference by the weighted likelihood bootstrap (with discussion). J R Stat Soc Series B 56:3–48Google Scholar
  42. Noyes HA, Arana BA, Chance ML, Maingon R (1997) The Leishmania hertigi (Kinetoplastida; Trypanosomatidae) complex and the lizard Leishmania: their classification and evidence for a neotropical origin of the LeishmaniaEndotrypanum clade. J Eukaryot Microbiol 44:511–517PubMedCrossRefGoogle Scholar
  43. Piarroux R, Fontes M, Perasso R, Gambarelli F, Joblet C, Dumon H, Auilici M (1995) Phylogenetic relationships between Old World Leishmania strains revealed by analysis of a repetitive DNA sequence. Mol Biochem Parasitol 73:249–252PubMedCrossRefGoogle Scholar
  44. Pollock DD, Zwickl DJ, Mccguire JA, Hillis DM (2002) Increased taxon sampling is advantageous for phylogenetic inference. Syst Biol 51:664–671PubMedCrossRefGoogle Scholar
  45. Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609PubMedCrossRefGoogle Scholar
  46. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approach. Syst Biol 53:793–808PubMedCrossRefGoogle Scholar
  47. Posada D, Crandal KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45PubMedCrossRefGoogle Scholar
  48. Posda D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  49. Raftery AE (1996) Hypothesis testing and model selection. In: Gilks WR, Spiegelhalter DJ, Richardson S (eds) Markov chain Monte Carlo in practice. Chapman and Hall, London, pp 163–188Google Scholar
  50. Rambaut A, Drummond AJ (2009) Tracer v1.5. Available from http://beast.bio.ed.ac.uk/Tracer
  51. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  52. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  53. Schönian G, Mauricio I, Cupolillo E (2010) Is it time to revise the nomenclature of Leishmania? Trends Parasitol 26:466–469PubMedCrossRefGoogle Scholar
  54. Slowinski JB, Page RDM (1999) How should species phylogenies be inferred from sequence data? Syst Biol 48:814–825PubMedCrossRefGoogle Scholar
  55. Suchard MA, Weiss RE, Sinsheimer JS (2001) Bayesian selection of continuous time Markov chain evolutionary models. Mol Biol Evol 18:1001–1013PubMedGoogle Scholar
  56. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods), version 4. Sinauer, SunderlandGoogle Scholar
  57. Swofford DL, Olsen GJ, Waddell PJ, Hillis DM (1996) Phylogenetic inference. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer, SunderlandGoogle Scholar
  58. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  59. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Bio Evol 24:1596–1599CrossRefGoogle Scholar
  60. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  61. Tibayrenc M (1998) Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. Int J Parasitol 28:85–104PubMedCrossRefGoogle Scholar
  62. Tibayrenc M (2006) The species concept in parasites and other pathogens: a pragmatic approach? Trends Parasitol 22:66–70PubMedCrossRefGoogle Scholar
  63. van der Spek H, Arts GJ, van den Burg J, Sloof P, Benne R (1989) The nucleotide sequence of mitochondrial maxicircle genes of Crithidia fasciculate. Nucleic Acids Res 17:4876PubMedCrossRefGoogle Scholar
  64. WHO (1990) Control of leishmaniases. World Health Organization, GenevaGoogle Scholar
  65. Wiens JJ (2003) Missing data, incomplete taxa, and phylogenetic accuracy. Syst Biol 52:528–538PubMedCrossRefGoogle Scholar
  66. Xia X, Lemey P (2009) Assessing substitution saturation with DAMBE. In: Lemey P (ed) The phylogenetic handbook. Cambridge University Press, CambridgeGoogle Scholar
  67. Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373PubMedCrossRefGoogle Scholar
  68. Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7PubMedCrossRefGoogle Scholar
  69. Xu Z-B, Le Blancq S, Evans DA, Peters W (1984) The characterization by isoenzyme electrophoresis of Leishmania isolated in the People's Republic of China. Trans R Soc Trop Med Hyg 78:689–693PubMedCrossRefGoogle Scholar
  70. Yang B-B, Guo X-G, Hu X-S, Zhang J-G, Liao L, Chen D-L, Chen J-P (2010) Species discrimination and phylogenetic inference of 17 Chinese Leishmania isolates based on internal transcribed spacer 1 (ITS1) sequences. Parasitol Res 107:1049–1065PubMedCrossRefGoogle Scholar
  71. Yatawara L, Le TH, Wickramasinghe S, Agatsuma T (2008) Maxicircle (mitochondrial) genome sequence (partial) of Leishmania major: gene content, arrangement and composition compared with Leishmania tarentolae. Gene 424:80–86PubMedCrossRefGoogle Scholar
  72. Zwickl DJ, Hillis DM (2002) Increased taxon sampling greatly reduces phylogenetic error. Syst Biol 51:588–598PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Parasitology, West China School of Preclinical and Forensic MedicineSichuan UniversityChengduChina
  2. 2.Chengdu Institute of BiologyChinese Academy of SciencesChengduChina
  3. 3.Animal Disease Prevention and Food Safety Key Laboratory of Sichuan ProvinceSichuan UniversityChengduChina

Personalised recommendations