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Kinetoplastid Biology and Disease Biomed Central Kinetoplastid Biology and Disease BioMed Central Review Open Access Genetic subdivisions within Trypanosoma cruzi (Discrete Typing Units) and their relevance for molecular epidemiology and experimental evolution Michel Tibayrenc* Address: UR62 "Genetics of Infectious Diseases", UMR CNRS/IRD 9926, IRD Centre, BP 64501, 34394 Montpellier Cedex 5, France Email: Michel Tibayrenc* - [email protected] * Corresponding author Published: 28 October 2003 Received: 18 July 2003 Accepted: 28 October 2003 Kinetoplastid Biology and Disease 2003, 2:12 This article is available from: http://www.kinetoplastids.com/content/2/1/12 © 2003 Tibayrenc; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL. Abstract Background: This paper summarizes the main results obtained on Trypanosoma cruzi genetic diversity and population structure since this parasite became the theme of many genetic and molecular studies in the early seventies. Results: T. cruzi exibits a paradigmatic pattern of long-term, clonal evolution, which has structured its natural populations into several discrete genetic subdivisions or "Discrete Typing Units" (DTU). Rare hybridization events are nevertheless detectable in natural populations and have been recently obtained in the laboratory. Conclusions: The DTUs and natural clones of T. cruzi constitute relevant units for molecular epidemiology and experimental evolution. Experimental mating opens the way to an in-depth knowledge of this parasite's formal genetics. Introduction analysis for epidemiological surveys [3] and hypotheses It is probable that Trypanosoma cruzi, the agent of Chagas on T. cruzi pathogenicity [4]. Numerical taxonomy disease, is the pathogenic microorganism for which showed their overall clustering [5]. However the biologi- intraspecific genetic diversity is the best known. Long- cal nature and evolutionary origin of the zymodemes* standing interest in this diversity has led many teams cur- remained entirely unknown. The specific contribution of rently working on this parasite to follow and even to our group has been to apply the concepts of population generate the recent technological progress in biochemical genetics to the study of T. cruzi biochemical and genetic typing, molecular epidemiology* (Terms quoted * are polymorphism. The present paper describes the main explained in the glossary) and population genetics*. In results reached in this field by our group and other teams. the early seventies, obtaining knowledge of the popula- tion structure of pathogenic microorganisms was a major Methodology challenge, since their formal genetics was entirely specula- The key-point in understanding the population structure tive. The isoenzyme* era gave us the first insights to the of a pathogenic microorganism is its mating system. The genetic diversity of T. cruzi and other parasites. Pioneering classical view, that microbes reproduce clonally, has been studies by Miles et al. [1,2] showed clearly the existence of upset by the population genetic era. Genetic exchange is three main isoenzyme types, which were called "principal very frequent in many microbial species. Whatever its pre- zymodemes*". Such zymodemes were taken as units of cise cytological mechanism, horizontal gene transfer Page 1 of 6 (page number not for citation purposes) Kinetoplastid Biology and Disease 2003, 2 http://www.kinetoplastids.com/content/2/1/12 Table 1: Criteria and tests of clonality (after 10) our group to detect linkage disequilibrium are communi- cated in table 1 and will be made available on the internet Criterion Description in a near future. Other tests relying on the same basic prin- Segregation ciples are available [12]. Linkage disequilibrium* tests are (within locus) extremely powerful, since the probability of occurrence of a Fixed heterozygosity * a given mutlilocus combination under the panmictic* b Absence of segregation genotypes * assumptions is very low if the number of loci is sufficient. c Deviation from Hardy-Weinberg expectation Observing repeated multilocus combinations is therefore Recombination in itself a strong indication for linkage disequilibrium*, (beween loci) d Overrepresented, identical genotypes widespread * which statistical level of significance is evaluated by the (statistical tests d1 ** # and d2 ** § tests (table 1). Apart from predominant clonal* evolu- e Absence of recombinant genotypes ** §/P> tion, linkage disequilibrium* can be generated by either f Linkage disequilibrium ** §/P> cryptic speciation or epidemic clonality (propagation of g Correlation between two independent sets of ephemeral clones in a basically sexual species; [12]). genetic markers ** §P Means to distinguish between these two cases from "true" * = used qualitatively, without statistical calculations; ** = used with clonal* evolution have been communicated [13]. statistical calculations. # Combinatorial analysis §Monte Carlo simulation with 104 iterations ¶Mantel nonparametric test of The "clones*" observed by a given set of genetic markers correlation between genetic distances obtained from different will prove to be genetically heterogeneous if a more dis- markers criminative marker is used. We have forged the term "clonet" to designate a set of stocks that appear genetically identical with a given set of markers in a clonal* species [11]. affects pathogen population structure: it clouds phyloge- netic individualization of lineages and renders individual In complement with population genetics, classical phylo- genotypes ephemeral [6]. There is a practical consequence genetic analysis is useful to look for possible discrete of this for molecular epidemiology: if pathogen multilo- genetic subdivisions in the species under study. In the case cus genotypes have a short lifetime, they cannot be con- of microbial pathogens, many times, such subdivisions veniently used as epidemiological tracers. The "clonality/ are observed, however they do not fulfill the rigorous cri- sexuality debate" has been, therefore, the target of many teria of phylogenetic analysis, since some level of horizon- research groups in the last twenty years, and is still contro- tal gene transfer renders these subdivisions incompletely versial. The approach proposed by us for T. cruzi [7] and isolated from each other. The descriptive concept of "Dis- by others for bacteria [8] has been to look for the expected crete Typing Unit" (DTU) designates a set of stocks that consequences of random allelic segregation and unilocus are genetically more similar to each other than to any genotype recombination in the natural populations sur- other stock, and are identifiable by common genetic, veyed. If these consequences are not observed, this is molecular, or immunological markers named "tags" [14]. taken as circumstantial evidence that gene flow is inhib- ited. Allelic segregation is surveyed by the classical Hardy- Main results in Trypanosoma cruzi Weinberg equilibrium* statistics. It is a demanding T. cruzi still is a paradigmatic case of predominantly approach when microbial pathogens are considered. First clonal evolution. Evidence for lack of Mendelian segrega- it requires that the ploidy of the organism is known. This tion, an argument taken long ago on the basis of the is sometimes difficult. As an example, T. cruzi, which was diploidy hypothesis [7], has been challenged by recent supposed to be diploid [7], is now considered an aneu- mating experiments showing that T. cruzi is aneuploid [9]. ploid organism according to experimental recombination However such results do not falsify the line of evidence data [9]. Second, Hardy-Weinberg tests are not applicable based on the analysis of linkage disequilibrium*, which to haploid organisms, which is the case for bacteria and remains valid. As a matter of fact, an impressive congru- human forms of Plasmodium parasites. For these reasons, ence of results corroborates the existence of strong linkage recombination tests are considered more reliable [10]. disequilibrium* in the agent of Chagas disease [15], even They are based on the null hypothesis of free genetic in sylvatic cycles and when each genetic subdivision is exchange (panmixia) and rely on the analysis of linkage analyzed separately. A striking illustration of this linkage disequilibrium*. The same basic principles are still used disequilibrium* is the existence of a highly significant cor- in recent contributions to this field of research [6]. Physi- relation between independent genetic markers, including cal obstacles to gene flow (isolation by either time or isoenzymes [16], Random Primed Amplified Polymor- space or both) can generate linkage disequilibrium* too phic DNA* or RAPD [17] and microsatellites [18]. It (Wahlund effect). Means to avoid such biases have been seems that long-term clonal evolution in T. cruzi has been detailed previously [11]. The statistical tests elaborated by Page 2 of 6 (page number not for citation purposes) Kinetoplastid Biology and Disease 2003, 2 http://www.kinetoplastids.com/content/2/1/12 RAPDDTU MLEE (F5-d) (Idh 5),(Nhi 1/1) M1117 M1117 SC13 A10-a, F1-a, F13-e, N9-c SC13 Davis2 Davis2 STP3.1 (Nhi 1/1) Idh 3,Nhi 2/2* (F5-d) SP1 OPS4 133-79 cl7 (Got 3) STP3.1 X39501 X39501 P209 FIRST B17-a, LGN Gpi 5/5 B19-b 133-79 cl7 MAJOR Nazca Cuica cl1 P209 cl1 1 S034 LINEAGE Nazca OPS21 cl11 Sod 5-6-9 SP1 Teh cl2 OPS4 LGN OPS21 cl11 Mdh 2/2 Cuica
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