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

Abstract

BackgroundTrypanosomatids 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.ResultsAnalyses 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.ConclusionWe 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.

The Evolutionary Loss of RNAi Key Determinants in Kinetoplastids as a Multiple Sporadic Phenomenon

“… Abbreviations used in the Table: pp—genome sequences were generously provided pre-publication by the Euglenozoan Genome Consortium (see Acknowledgements) Genome sequences of strains with shown accession numbers were previously published (Alves et al 2013a, b). Other sequences used herein were obtained from TriTrypDB (Aslett et al 2010)…”

“… Genome sequences of strains with shown accession numbers were previously published (Alves et al 2013a, b). Other sequences used herein were obtained from TriTrypDB (Aslett et al 2010)…”

Symbiont modulates expression of specific gene categories in Angomonas deanei

“…An example is the wild type (WT) Angomonas deanei (previously classified as Crithidia deanei ) (Teixeira et al 2011) which hosts a betaproteobacteria of the Alcaligenacea family in its cytoplasm. This symbiosis benefits the protozoan host because the bacterium contains genes that encode enzymes that complete essential biosynthetic pathways (Alves et al 2011, 2013, Klein et al 2013, Motta et al 2013). On the other hand, the aposymbiotic (APO) A. deanei lacks the betaproteobacteria.…”

“…Genome sequence analysis and nutritional assays reveal that the symbiont complements essential biosynthetic pathways of the trypanosomatid such as the production of haeme, amino acids (aas), vitamins and purine/pyrimidine bases (Alves et al 2011, 2013, Klein et al 2013, Motta et al 2013). Therefore, the endosymbiosis in this trypanosomatid constitutes a mutualistic association where participants co-evolved leading to mutual dependence in which the cured APO protozoa is unable to colonise insects and the isolated bacterium is unable to replicate in culture media (de Souza & Motta 1999).…”

A Comparative In Silico Study of the Antioxidant Defense Gene Repertoire of Distinct Lifestyle Trypanosomatid Species

“…The absence of ODC in S. culicis was explored by Alves et al67 In this monoxenous parasitic organism, endosymbiont-coded enzymes promote the interconversion of agmatine into putrescine. Agmatine is synthesized by arginine decarboxylase, which is exclusively present in the genomes of S. culicis and A. deanei endosymbionts but absent in all other studied trypanosomatids 67…”