Endosymbiosis in trypanosomatid protozoa: the bacterium division is controlled during the host cell cycle

Abstract

Mutualism is defined as a beneficial relationship for the associated partners and usually assumes that the symbiont number is controlled. Some trypanosomatid protozoa co-evolve with a bacterial symbiont that divides in coordination with the host in a way that results in its equal distribution between daughter cells. The mechanism that controls this synchrony is largely unknown, and its comprehension might provide clues to understand how eukaryotic cells evolved when acquiring symbionts that later became organelles. Here, we approached this question by studying the effects of inhibitors that affect the host exclusively in two symbiont-bearing trypanosomatids, Strigomonas culicis and Angomonas deanei. We found that inhibiting host protein synthesis using cycloheximide or host DNA replication using aphidicolin did not affect the duplication of bacterial DNA. Although the bacteria had autonomy to duplicate their DNA when host protein synthesis was blocked by cycloheximide, they could not complete cytokinesis. Aphidicolin promoted the inhibition of the trypanosomatid cell cycle in the G1/S phase, leading to symbiont filamentation in S. culicis but not in A. deanei. Treatment with camptothecin blocked the host protozoa cell cycle in the G2 phase and induced the formation of filamentous symbionts in both species. Oryzalin, which affects host microtubule polymerization, blocked trypanosomatid mitosis and abrogated symbiont division. Our results indicate that host factors produced during the cell division cycle are essential for symbiont segregation and may control the bacterial cell number.

Reduction of Tubulin Expression in Angomonas deanei by RNAi Modifies the Ultrastructure of the Trypanosomatid Protozoan and Impairs Division of Its Endosymbiotic Bacterium

“…More interesting in this case is that the knockdown of atubulin lead to symbiont filamentation, which is in agreement with our previous studies showing that the symbiont division is coordinated with the host nucleus (Motta 2010). Moreover, compounds that specifically arrest the protozoan cell cycle, as well as tubulin polymerization caused symbiont filamentation (Catta-Preta et al 2015). The results further confirmed our hypothesis that the host cell cytoskeleton plays a role in the endosymbiont division, which may represent a way to control the number of bacteria.…”

“…Moreover, compounds that specifically arrest the protozoan cell cycle, as well as tubulin polymerization caused symbiont filamentation (Catta‐Preta et al. ). The results further confirmed our hypothesis that the host cell cytoskeleton plays a role in the endosymbiont division, which may represent a way to control the number of bacteria.…”

Development of a toolbox to dissect host-endosymbiont interactions and protein trafficking in the trypanosomatid Angomonas deanei

“…The absence of ETP1 orthologues in any other organism makes it difficult to predict a cellular function of this protein. Recently, it was shown that specifically inhibiting the A. deanei cell cycle or translation, affects the division of its endosymbiont [41]. This raises the speculative possibility that ETP1 and/or other nuclear-encoded proteins targeted to the endosymbiont might play a role in controlling its cell cycle.…”

Trypanosomatids Are Much More than Just Trypanosomes: Clues from the Expanded Family Tree

“…putative provision of ATP and phosphatidylcholine to the bacterium, which is likely reciprocated by providing the protist with heme, vitamins, purines, and some essential amino acids ( Figure 2). The molecular basis of the host-endosymbiont relationships has been studied so far only in the subfamily Strigomonadinae, for which the genomes are available [21][22][23].…”