Phylogenetic and syntenic data support a single horizontal transference to aTrypanosoma ancestor of a prokaryotic proline racemase implicated in parasite evasion from host defences

Authors

Zuleima C. Caballero, Universidade de São Paulo, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología-AIP
Andre G. Costa-Martins, Universidade de São Paulo
Robson C. Ferreira, Universidade de São Paulo
João M P Alves, Universidade de São Paulo
Myrna G. Serrano, Virginia Commonwealth UniversityFollow
Erney P. Camargo, Universidade de São Paulo
Gregory A. Buck, Virginia Commonwealth UniversityFollow
Paola Minoprio, Institut Pasteur
Marata M G Teixeira, Universidade de São Paulo

Document Type

Article

Original Publication Date

2015

Journal/Book/Conference Title

Parasites & Vectors

Volume

8

DOI

10.1186/s13071-015-0829-y

Comments

Originally published at http://dx.doi.org/10.1186/s13071-015-0829-y

Date of Submission

December 2015

Abstract

Background

Proline racemase (PRAC) enzymes of Trypanosoma cruzi (TcPRAC), the agent of Chagas disease, and Trypanosoma vivax (TvPRAC), the agent of livestock trypanosomosis, have been implicated in the B-cells polyclonal activation contributing to immunosuppression and the evasion of host defences. The similarity to prokaryotic PRAC and the absence in Trypanosoma brucei andTrypanosoma congolense have raised many questions about the origin, evolution, and functions of trypanosome PRAC (TryPRAC) enzymes.

Findings

We identified TryPRAC homologs as single copy genes per haploid genome in 12 of 15Trypanosoma species, including T. cruzi and T. cruzi marinkellei, T. dionisii, T. erneyi, T. rangeli, T. conorhini and T. lewisi, all parasites of mammals. Polymorphisms in TcPRAC genes matched T. cruzi genotypes: TcI-TcIV and Tcbat have unique genes, while the hybrids TcV and TcVI containTcPRACA and TcPRACB from parental TcII and TcIII, respectively. PRAC homologs were identified in trypanosomes from anurans, snakes, crocodiles, lizards, and birds. Most trypanosomes have intact PRAC genes. T. rangeli possesses only pseudogenes, maybe in the process of being lost. T. brucei, T. congolense and their allied species, except the more distantly related T. vivax, have completely lost PRAC genes.

Conclusions

The genealogy of TryPRAC homologs supports an evolutionary history congruent with theTrypanosoma phylogeny. This finding, together with the synteny of PRAC loci, the relationships with prokaryotic PRAC inferred by taxon-rich phylogenetic analysis, and the absence in trypanosomatids of any other genera or in bodonids or euglenids suggest that a common ancestor of Trypanosoma gained PRAC gene by a single and ancient horizontal gene transfer (HGT) from a Firmicutes bacterium more closely related to Gemella and other species of Bacilli than toClostridium as previously suggested. Our broad phylogenetic study allowed investigation ofTryPRAC evolution over long and short timescales. TryPRAC genes diverged to become species-specific and genotype-specific for T. cruzi and T. rangeli, with resulting genealogies congruent with those obtained using vertically inherited genes. The inventory of TryPRAC genes described here is the first step toward the understanding of the roles of PRAC enzymes in trypanosomes differing in life cycles, virulence, and infection and immune evasion strategies.

Rights

Copyright © 2015 Caballero et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Is Part Of

VCU Microbiology and Immunology Publications