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

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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.

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References

  • Ababneh F, Jermiin LS, Ma C, Robinson J (2006) Matched-pairs tests of homogeneity with applications to homologous nucleotide sequences. Bioinformatics 22:1225–1231

    Article  PubMed  CAS  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723

    Article  Google Scholar 

  • 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 121:352–361

    Article  PubMed  CAS  Google Scholar 

  • 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–S13

    Article  PubMed  Google Scholar 

  • 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 64:1–109

    Article  PubMed  Google Scholar 

  • 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 26:1205–1213

    Article  PubMed  CAS  Google Scholar 

  • 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 6:440–446

    Article  PubMed  CAS  Google Scholar 

  • 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)

    PubMed  CAS  Google Scholar 

  • Carstens BC, Knowles LL (2007) Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Syst Biol 56:400–411

    Article  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  PubMed  CAS  Google Scholar 

  • 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 259:15136–15147

    Google Scholar 

  • de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886

    Article  PubMed  Google Scholar 

  • Desjeux P (2004) Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27:305–318

    Article  PubMed  CAS  Google Scholar 

  • 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 97:35–44

    Article  PubMed  CAS  Google Scholar 

  • Felsensten JP (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • 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 10:238–245

    Article  PubMed  CAS  Google Scholar 

  • Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–511

    Article  Google Scholar 

  • 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 27:221–224

    Article  PubMed  CAS  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    Article  CAS  Google Scholar 

  • 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 22:2162–2163

    Article  PubMed  CAS  Google Scholar 

  • 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) 115:1457–1459

    CAS  Google Scholar 

  • Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol 51:673–688

    Article  PubMed  Google Scholar 

  • 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 20:644–652

    Article  PubMed  CAS  Google Scholar 

  • 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 1:61–68

    Article  PubMed  CAS  Google Scholar 

  • Ibrahim ME, Mahdi MA, Bereir RE, Giha RS, Wasunna C (2008) Evolutionary conservation of RNA editing in the genus Leishmania. Infect Genet Evol 8:378–380

    Article  PubMed  CAS  Google Scholar 

  • Jermiin LS, Jayaswal V, Ababneh F, Robinson J (2008) Phylogenetic model evaluation. In: Keith J (ed) Methods in molecular biology: bioinformatics. Humana, Totowa

    Google Scholar 

  • Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795

    Article  Google Scholar 

  • Kim KS, Teixeira SM, Kirchhoff LV, Donelson JE (1994) Transcription and editing of cytochrome oxidase II RNAs in Trypanosoma cruzi. J Biol Chem 269:1206–1211

    PubMed  CAS  Google Scholar 

  • Knowles LL, Carstens BC (2007) Delimiting species without monophyletic gene trees. Syst Biol 56:887–895

    Article  PubMed  Google Scholar 

  • 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 162:16–31

    Article  PubMed  CAS  Google Scholar 

  • 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)

    CAS  Google Scholar 

  • Lu H-G, Hu X-S (1990) Identification of Leishmania by kinetoplast DNA minicircle and cloning of minicircle. Chin Med J (Engl) 103:418–423

    CAS  Google Scholar 

  • 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 50:763–770

    PubMed  CAS  Google Scholar 

  • 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)

    CAS  Google Scholar 

  • 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)

    PubMed  CAS  Google Scholar 

  • 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)

    PubMed  CAS  Google Scholar 

  • 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)

    CAS  Google Scholar 

  • 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 104:9375–9380

    Article  PubMed  Google Scholar 

  • Maddison WP (1997) Gene trees in species trees. Syst Biol 46:523–536

    Article  Google Scholar 

  • Nebohacova M, KimCE SL, Maslov DA (2009) RNA editing and mitochondrial activity in promastigotes and amastigotes of Leishmania donovani. Int J Parasitol 39:635–644

    Article  PubMed  CAS  Google Scholar 

  • Newton MA, Raftery AE (1994) Approximate Bayesian inference by the weighted likelihood bootstrap (with discussion). J R Stat Soc Series B 56:3–48

    Google Scholar 

  • 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 Leishmania–Endotrypanum clade. J Eukaryot Microbiol 44:511–517

    Article  PubMed  CAS  Google Scholar 

  • 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 73:249–252

    Article  PubMed  CAS  Google Scholar 

  • Pollock DD, Zwickl DJ, Mccguire JA, Hillis DM (2002) Increased taxon sampling is advantageous for phylogenetic inference. Syst Biol 51:664–671

    Article  PubMed  Google Scholar 

  • 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 55:595–609

    Article  PubMed  Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approach. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

  • Posada D, Crandal KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45

    Article  PubMed  Google Scholar 

  • Posda D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  Google Scholar 

  • 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 163–188

    Google Scholar 

  • Rambaut A, Drummond AJ (2009) Tracer v1.5. Available from http://beast.bio.ed.ac.uk/Tracer

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schönian G, Mauricio I, Cupolillo E (2010) Is it time to revise the nomenclature of Leishmania? Trends Parasitol 26:466–469

    Article  PubMed  Google Scholar 

  • Slowinski JB, Page RDM (1999) How should species phylogenies be inferred from sequence data? Syst Biol 48:814–825

    Article  PubMed  CAS  Google Scholar 

  • Suchard MA, Weiss RE, Sinsheimer JS (2001) Bayesian selection of continuous time Markov chain evolutionary models. Mol Biol Evol 18:1001–1013

    PubMed  CAS  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (* and other methods), version 4. Sinauer, Sunderland

    Google Scholar 

  • Swofford DL, Olsen GJ, Waddell PJ, Hillis DM (1996) Phylogenetic inference. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer, Sunderland

    Google Scholar 

  • 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 10:512–526

    PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Bio Evol 24:1596–1599

    Article  CAS  Google Scholar 

  • 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 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tibayrenc M (1998) Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. Int J Parasitol 28:85–104

    Article  PubMed  CAS  Google Scholar 

  • Tibayrenc M (2006) The species concept in parasites and other pathogens: a pragmatic approach? Trends Parasitol 22:66–70

    Article  PubMed  Google Scholar 

  • 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 17:4876

    Article  PubMed  Google Scholar 

  • WHO (1990) Control of leishmaniases. World Health Organization, Geneva

    Google Scholar 

  • Wiens JJ (2003) Missing data, incomplete taxa, and phylogenetic accuracy. Syst Biol 52:528–538

    Article  PubMed  Google Scholar 

  • Xia X, Lemey P (2009) Assessing substitution saturation with DAMBE. In: Lemey P (ed) The phylogenetic handbook. Cambridge University Press, Cambridge

    Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  PubMed  CAS  Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7

    Article  PubMed  CAS  Google Scholar 

  • 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 78:689–693

    Article  PubMed  CAS  Google Scholar 

  • 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 107:1049–1065

    Article  PubMed  Google Scholar 

  • 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 424:80–86

    Article  PubMed  CAS  Google Scholar 

  • Zwickl DJ, Hillis DM (2002) Increased taxon sampling greatly reduces phylogenetic error. Syst Biol 51:588–598

    Article  PubMed  Google Scholar 

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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).

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  1. Department of Parasitology, West China School of Preclinical and Forensic Medicine, Sichuan University, Chengdu, 610041, Sichuan, China

    De-Ping Cao, Da-Li Chen & Jian-Ping Chen

  2. Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, 610041, Sichuan, China

    Xian-Guang Guo

  3. Animal Disease Prevention and Food Safety Key Laboratory of Sichuan Province, Sichuan University, Chengdu, 610064, Sichuan, China

    Jian-Ping Chen

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  1. De-Ping Cao
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Correspondence to Da-Li Chen or Jian-Ping Chen.

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The authors wish it to be known that, in their opinion, the first two authors, De-Ping Cao and Xian-Guang Guo, should be regarded as joint first authors.

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Cao, DP., Guo, XG., Chen, DL. et al. Species delimitation and phylogenetic relationships of Chinese Leishmania isolates reexamined using kinetoplast cytochrome oxidase II gene sequences. Parasitol Res 109, 163–173 (2011). https://doi.org/10.1007/s00436-010-2239-6

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