Phosphatidylcholine synthesis inCrithidia deanei: the influence of the endosymbiont

Abstract

In this study, the role of phospholipid biosynthetic pathways was investigated in the establishment of the mutualistic relationship between the trypanosomatid protozoan Crithidia deanei and its symbiotic bacterium. Although the endosymbiont displays two unit membranes, it lacks a typical Gram-negative cell wall. As in other intracellular bacteria, phosphatidylcholine is a major component of the symbiont envelope. Here, it was shown that symbiont-bearing C. deanei incorporates more than two-fold (32)Pi into phospholipids as compared with the aposymbiotic strain. The major phospholipid synthesized by both strains was phosphatidylcholine, followed by phosphatidylethanolamine and phosphatidylinositol. Cellular fractioning indicated that (32)Pi-phosphatidylcholine is the major phospholipid component of the isolated symbionts, as well as of mitochondria. Although the data indicated that isolated symbionts synthesized phospholipids independently of the trypanosomatid host, a key finding was that the isolated bacteria synthesized mostly phosphatidylethanolamine, rather than phosphatidylcholine. These results indicate that phosphatidylcholine production by the symbiont depends on metabolic exchanges with the host protozoan. Insight about the mechanisms underlying lipid biosynthesis in symbiont-bearing C. deanei might help to understand how the prokaryote/trypanosomatid relation has evolved in the establishment of symbiosis.

Predicting the Proteins of Angomonas deanei, Strigomonas culicis and Their Respective Endosymbionts Reveals New Aspects of the Trypanosomatidae Family

“…Interestingly, this last step of the pathway is not found in the S. culicis endosymbiont. Importantly, both symbionts lack genes that encode proteins of PC biosynthetic pathways, reinforcing the idea that this phospholipid is mainly obtained from the host protozoa [5]. Remarkably, phoshpatidylglycerophosphatase A, which produces the intermediate phosphatidylglycerol necessary for cardiolipin biosynthesis, was not found in either protozoa but is present in both symbionts.…”

“…The sphingophospholipid (SPL) content in A. deanei and its symbiont has been previously described, with phosphatidylcholine (PC) representing the major SPL in the host, whereas cardiolipin predominates in the symbiotic bacterium [5], [80]. The synthetic pathway of phosphatidylglycerol from glycerol phosphate is present in both host trypanosomatids (Table S16).…”

“…In this obligatory association, the endosymbiont is unable to survive and replicate once isolated from the host, whereas aposymbiotic protozoa are unable to colonize insects [4], [5]. The symbiont is surrounded by two membrane units and presents a reduced peptidoglycan layer, which is essential for cell division and morphological maintenance [6].…”

“…Furthermore, the bacterium enhances the formation of polyamines, which results in high rates of cell proliferation in endosymbiont-bearing trypanosomatids compared to other species of the family [12]. Conversely, the host cell supplies phosphatidylcholine, which composes the endosymbiont envelope [5], and ATP produced through the activity of protozoan glycosomes [13].…”

Effects of miltefosine on the proliferation, ultrastructure, and phospholipid composition of Angomonas deanei, a trypanosomatid protozoan that harbors a symbiotic bacterium

“…This agreed with our previous works, which showed that PE is an essential constituent of the symbiotic bacterium membranes (Palmié‐Peixoto et al ., ). Once isolated from the protozoan, the symbiont is able to produce phospholipids, especially PE, independently of the host cell (Azevedo‐Martins et al ., ). However, it is noteworthy that the symbiosis in trypanosomatids is an obligatory relationship with extensive metabolic exchanges (reviewed by Motta, ) and that the bacterium may obtain part of PC or PC precursors from the host (Azevedo‐Martins et al ., ).…”