Abstract

BackgroundThe endosymbiosis in trypanosomatids is characterized by co-evolution between one bacterium and its host protozoan in a mutualistic relationship, thus constituting an excellent model to study organelle origin in the eukaryotic cell. In this association, an intense metabolic exchange is observed between both partners: the host provides energetic molecules and a stable environment to a reduced wall symbiont, while the bacterium is able to interfere in host metabolism by enhancing phospholipid production and completing essential biosynthesis pathways, such as amino acids and hemin production. The bacterium envelope presents a reduced cell wall which is mainly composed of cardiolipin and phosphatidylcholine, being the latter only common in intracellular prokaryotes. Phosphatidylinositol (PI) is also present in the symbiont and host cell membranes. This phospholipid is usually related to cellular signaling and to anchor surface molecules, which represents important events for cellular interactions.MethodsIn order to investigate the production of PI and its derivatives in symbiont bearing trypanosomatids, aposymbiotic and wild type strains of Angomonas deanei, as well as isolated symbionts, were incubated with [3H]myo-inositol and the incorporation of this tracer was analyzed into inositol-containing molecules, mainly phosphoinositides and lipoproteins. Gene searches and their phylogenies were also performed in order to investigate the PI synthesis in symbiontbearing trypanosomatids.ResultsOur results showed that the bacterium did not incorporate the tracer and that both strains produced similar quantities of PI and its derivatives, indicating that the symbiont does not influence the production of these metabolites. Gene searches related to PI synthesis revealed that the trypanosomatid genome contains an inositol transporter, PI synthase and the myo-inositol synthase. Thus, the host is able to produce PI either from exogenous myo-inositol (inositol transporter) or from myo-inositol synthesized de novo. Phylogenetic analysis using other organisms as references indicated that, in trypanosomatids, the genes involved in PI synthesis have a monophyletic origin. In accordance with experimental data, sequences for myo-inositol transport or for myo-inositol and PI biosynthesis were not found in the symbiont.ConclusionsAltogether, our results indicate that the bacterium depends on the host to obtain PI.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-015-0854-x) contains supplementary material, which is available to authorized users.

Highlights

  • The endosymbiosis in trypanosomatids is characterized by co-evolution between one bacterium and its host protozoan in a mutualistic relationship, constituting an excellent model to study organelle origin in the eukaryotic cell

  • We investigated the production of PI, phosphatidylinositol monophosphate (PIP), and phosphatidylinositol biphosphate (PIP2) in A. deanei and its aposymbiotic strain in order to verify whether the bacterium influences the PI metabolism of the protozoan host

  • Phosphoinositide formation in A. deanei Wild type and aposymbiotic strains of A. deanei were grown in culture medium containing [3H]myo-inositol in order to quantify the incorporation of this tracer in PI and in phosphoinositides

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Summary

Introduction

The endosymbiosis in trypanosomatids is characterized by co-evolution between one bacterium and its host protozoan in a mutualistic relationship, constituting an excellent model to study organelle origin in the eukaryotic cell In this association, an intense metabolic exchange is observed between both partners: the host provides energetic molecules and a stable environment to a reduced wall symbiont, while the bacterium is able to interfere in host metabolism by enhancing phospholipid production and completing essential biosynthesis pathways, such as amino acids and hemin production. Most protozoa in this family are non-pathogenic to humans and inhabit only invertebrate hosts during the whole life cycle Between these monoxenics, six species, including Angomonas deanei, maintain an obligatory symbiotic relationship with an intracellular bacterium [2,3]. The presence of the symbiont is related to alterations in trypanosomatid ultrastructure [14], surface charge [15], and carbohydrate plasma membrane composition [16]

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