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Open Access Highly Accessed Research article

Endosymbiosis in trypanosomatids: the genomic cooperation between bacterium and host in the synthesis of essential amino acids is heavily influenced by multiple horizontal gene transfers

João MP Alves15*, Cecilia C Klein234, Flávia Maia da Silva5, André G Costa-Martins5, Myrna G Serrano1, Gregory A Buck1, Ana Tereza R Vasconcelos4, Marie-France Sagot23, Marta MG Teixeira5, Maria Cristina M Motta6 and Erney P Camargo5

Author affiliations

1 Virginia Commonwealth University, Richmond, VA, USA

2 BAMBOO Team, INRIA Grenoble-Rhône-Alpes, Villeurbanne, France

3 Laboratoire Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR5558, Villeurbanne, France

4 Laboratório Nacional de Computação Científica, Petrópolis, Rio de Janeiro, Brazil

5 Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil

6 Laboratório de Ultraestrutura Celular Hertha Meyer. Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

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Citation and License

BMC Evolutionary Biology 2013, 13:190  doi:10.1186/1471-2148-13-190

Published: 9 September 2013

Abstract

Background

Trypanosomatids of the genera Angomonas and Strigomonas live in a mutualistic association characterized by extensive metabolic cooperation with obligate endosymbiotic Betaproteobacteria. However, the role played by the symbiont has been more guessed by indirect means than evidenced. Symbiont-harboring trypanosomatids, in contrast to their counterparts lacking symbionts, exhibit lower nutritional requirements and are autotrophic for essential amino acids. To evidence the symbiont’s contributions to this autotrophy, entire genomes of symbionts and trypanosomatids with and without symbionts were sequenced here.

Results

Analyses of the essential amino acid pathways revealed that most biosynthetic routes are in the symbiont genome. By contrast, the host trypanosomatid genome contains fewer genes, about half of which originated from different bacterial groups, perhaps only one of which (ornithine cyclodeaminase, EC:4.3.1.12) derived from the symbiont. Nutritional, enzymatic, and genomic data were jointly analyzed to construct an integrated view of essential amino acid metabolism in symbiont-harboring trypanosomatids. This comprehensive analysis showed perfect concordance among all these data, and revealed that the symbiont contains genes for enzymes that complete essential biosynthetic routes for the host amino acid production, thus explaining the low requirement for these elements in symbiont-harboring trypanosomatids. Phylogenetic analyses show that the cooperation between symbionts and their hosts is complemented by multiple horizontal gene transfers, from bacterial lineages to trypanosomatids, that occurred several times in the course of their evolution. Transfers occur preferentially in parts of the pathways that are missing from other eukaryotes.

Conclusion

We have herein uncovered the genetic and evolutionary bases of essential amino acid biosynthesis in several trypanosomatids with and without endosymbionts, explaining and complementing decades of experimental results. We uncovered the remarkable plasticity in essential amino acid biosynthesis pathway evolution in these protozoans, demonstrating heavy influence of horizontal gene transfer events, from Bacteria to trypanosomatid nuclei, in the evolution of these pathways.

Keywords:
Endosymbiosis; Trypanosomatids; Amino acid biosynthesis; Phylogeny; Genomic analyses; Metabolic pathway evolution; Proteobacteria