An Appraisal of the Taxonomy and Nomenclature of Trypanosomatids Presently Classified As Leishmania and Endotrypanum

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An Appraisal of the Taxonomy and Nomenclature of Trypanosomatids Presently Classified As Leishmania and Endotrypanum SPECIAL ISSUE ARTICLE 430 An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum O. A. ESPINOSA1,M.G.SERRANO2,E.P.CAMARGO1,M.M.G.TEIXEIRA1* and J. J. SHAW1* 1 Departamento de Parasitologia, Universidade de São Paulo, São Paulo, SP, Brazil 2 Virginia Commonwealth University, Center for the Study of Biological Complexity, Richmond, Virginia, USA (Received 31 August 2016; revised 14 October 2016; accepted 15 October 2016; first published online 15 December 2016) SUMMARY We propose a taxonomic revision of the dixenous trypanosomatids currently classified as Endotrypanum and Leishmania, including parasites that do not fall within the subgenera L. (Leishmania) and L. (Viannia) related to human leishmaniasis or L. (Sauroleishmania) formed by leishmanias of lizards: L. colombiensis, L. equatorensis, L. herreri, L. hertigi, L. deanei, L. enriettii and L. martiniquensis. The comparison of these species with newly characterized isolates from sloths, porcu- pines and phlebotomines from central and South America unveiled new genera and subgenera supported by past (RNA PolII gene) and present (V7V8 SSU rRNA, Hsp70 and gGAPDH) phylogenetic analyses of the organisms. The genus Endotrypanum is restricted to Central and South America, comprising isolates from sloths and transmitted by phleboto- mines that sporadically infect humans. This genus is the closest to the new genus Porcisia proposed to accommodate the Neotropical porcupine parasites originally described as L. hertigi and L. deanei. A new subgenus Leishmania (Mundinia)is created for the L. enriettii complex that includes L. martiniquensis. The new genus Zelonia harbours trypanosomatids from Neotropical hemipterans placed at the edge of the Leishmania–Endotrypanum-Porcisia clade. Finally, attention is drawn to the status of L. siamensis and L. australiensis as nomem nudums. Key words: Leishmaniinae, Leishmania, Endotrypanum, new genera, new subgenera, SSU rRNA, HSP70, gGAPDH, phylogeny, molecular taxonomy. INTRODUCTION Lainson and Shaw (1979, 1987) concluded that there were three very different groups of parasites The classification of Leishmania was initially based that warranted sub-generic status: L. (Leishmania), on the clinical symptoms of the disease that they L. (Viannia) and L. (Sauroleishmania). However, generated. Parasites causing cutaneous leishmaniasis the taxonomic position of some Leishmania-like throughout the world were considered as being parasites remained uncertain such as L. colombiensis L. tropica and those causing visceral leishmaniasis and L. martiniquensis isolated from patients and L. as being L. donovani.Thefirst move away from enriettii, L. equatorensis, L. herreri and L. hertigi iso- this position was by Nicolle (1908) who considered lated from wild animals. Another dixenous parasite that Mediterranean visceral leishmaniasis was clinic- that like the Leishmania also produces promastigotes ally and epidemiologically different from that of in its vector and in culture is Endotrypanum. This India, naming it L. infantum. Three years later genus was created to accommodate endoerythrocytic Vianna (1911) gave the name L. braziliensis to the sloth trypanosomatids described in French Guyana parasite responsible for a case of disseminated leish- (Mesnil and Brimont, 1908). maniasis from Brazil. Following this, Yakimoff and Molecular phylogeny has helped to clarify the Schokhor (1914) considered that the parasites taxonomy of the trypanosomatids, including many causing urban and rural cutaneous leishmaniasis in pathogens. In 2012, a group formed by dixenous Asia were different varieties of L. tropica, denomin- and monoxenous trypanosomatids originally called ating the urban form as var. minor and the rural form ‘slow evolving’, due to the high conservation of as var. major. SSU rRNA sequences, was given subfamily status Over the years more parasites from different parts under the name Leishmaniinae (Jirkú et al. 2012). of the world were examined and in the 1980s The dixenous members of this subfamily included parasites of wild animals that may accidentally * Corresponding authors. Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São infect man, causing diseases generically known as Paulo, São Paulo, SP 05508-900 Brazil. E-mail: jeffreyj@ leishmaniasis. The depth of the taxonomic com- usp.br, [email protected] plexity of the parasites originally described as Parasitology (2018), 145, 430–442. © Cambridge University Press 2016 doi:10.1017/S0031182016002092 Downloaded from https://www.cambridge.org/core. University of Athens, on 27 Sep 2021 at 12:45:39, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0031182016002092 Appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum 431 Leishmania is presently being disclosed by molecu- from GenBank and genome data banks of all lar studies. The question is: should they all be clas- Leishmania-like and Endotrypanum species, and refer- sified as belonging to the same genus? The mere ence-species of all subgenera of Leishmania. suggestion that organisms other than Leishmania species cause leishmaniasis is immediately boy- PCR amplification, sequencing and phylogenetic cotted or met with scepticism. But is this view analysis acceptable in the light of our present day knowledge of their genetic diversity and phylogenetic Total DNA was extracted from cultured flagellates relationships? using the traditional phenol–chloroform method. Renewed interests on trypanosomatids from wild The V7V8 SSU rRNA and gGAPDH gene were animals have unveiled a diversified genetic repertoire PCR-amplified as previously described (Hamilton within the genera Trypanosoma and Leishmania. et al. 2004; Teixeira et al. 2011). The amplification Recent studies have provided relevant insights into of HSP70 gene was done under the same reaction the broader genetic diversity and new reservoirs of conditions adopted for gGAPDH and using the fol- human- and non-human infective species of lowing primers: Hspf 5′-TGC GCA TCA TCA Leishmania (Cupolillo et al. 1998; Asato et al. ACG AGC C-3′ and Hspr 5′-ATC TTG GTC 2009; Cassia-Pires et al. 2014; Pothirat et al. 2014). ATGA TCG GGT TGC-3′. Consequently, there is an increasing number of PCR-amplified sequences were cloned using the ‘leishmanias’ from non-human hosts that cannot TA Cloning Kit (Carlsbad, CA, USA), and from be classified in any of the existing subgenera of one to five clones were sequenced for each gene of Leishmania, and are herein refereed as enigmatic or each trypanosomatid isolate. Sequences were aligned Leishmania-like trypanosomatids. The focus of this using CLUSTALX (Thompson et al. 1997), and paper is to molecularly characterize a large number manually refinedtoobtainthefollowingalignments: of new isolates from Amazonian wild mammals 1, V7V8 SSU rRNA sequences (∼850 bp = bar- (sloth and porcupine) and sand flies from Central codes); 2, gGAPDH sequences (768 bp); 3, HSP70 and South America, and to compare the data obtained sequences (611 bp); 4, consisting of concatenated with data available from other enigmatic leishmanias gGAPDH and HSP70 sequences (1·378 characters). and reference species of all accepted subgenera of Sequences determined in this study were all Leishmania, and their closest related monoxenous deposited in GenBank (Table S1). Sequences from species. For this, we inferred taxon-rich phylogenetic Leptomonas costaricensis (Costa Rica), the isolate trees based on gGAPDH and HSP70 genes, and used TCC169 (L. costaricensis-like from Brazil), the data to critically discuss the generic status and Leptomonas seymouri, Leptomonas pyrrhocoris and nomenclature of the dixenous parasites that produce Crithidia fasciculata were included in all analyses promastigotes in their vectors and cultures, some of (Supplementary Table S1). Sequences from which are the aetiological agents of the cohort of dis- Angomonas deanei, Angomonas desouzai and species eases known as leishmaniasis. of other genera of trypanosomatids were used as out- groups of Leishmaniinae (Jirkú et al. 2012). The den- drogram inferred using V7V8 SSU rRNA sequences MATERIAL AND METHODS of the Leishmaniinae subfamily and closely related trypanosomatids was done using the method of Organisms and cultures Maximum Parsimony (MP). The alignments of The organisms characterized in this study are rou- gGAPDH and HSP70 sequences were employed for tinely grown at 23–25 °C in TC100 medium phylogenetic inferences based on MP, Maximum (=Grace medium) supplemented with 10% FBS, and Likelihood (ML) and Bayesian inference (BI) ana- deposited in the Trypanosomatid Culture Collection lyses. The MP and bootstrap analyses used the of the University of São Paulo (TCC-USP). PAUP* version 4.0b10 software (Swofford, 2002), Routinely, upon inclusion in the TCC-USP, the pre- with 500 random sequence addition replicates fol- dominant morphotype of each new isolate is recorded, lowed by branch swapping (RAS-TBR), and the while the isolate itself is barcoded by V7V8 SSU ML analyses used RAxML v.2.2.3 (Stamatakis, rRNA sequencing (Teixeira et al. 2011). This proced- 2006). The general time reversible (GTR) model of ure serves only as preliminary information for future nucleotide substitution with proportion of invariable phylogenetic analyses of selected samples based on sites and gamma distribution was selected for the gGAPDH sequences. The samples selected for this
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