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.

Highlights

  • Symbiotic relationships between unicellular organisms, such as protozoa and bacteria, constitute interesting models for the investigation of organelle division and segregation during the cell cycle

  • Seven trypanosomatid species co-evolve with a single obligate bacterium that divides in synchronization with the host cell, providing an opportunity to study cell cycle regulation and the evolution of symbiotic associations (Motta et al, 2010; Brum et al, 2014)

  • In A. deanei, the S- and G2-phase populations constituted 9.7 and 22% of the total population, respectively (Figures 1C–E), while 15.7% of S. culicis cells were in S phase, and 35.4% were in G2 phase (Figures 1F–H)

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Summary

Introduction

Symbiotic relationships between unicellular organisms, such as protozoa and bacteria, constitute interesting models for the investigation of organelle division and segregation during the cell cycle. Symbiont division is controlled by the host protozoan contains circular and interlocked DNA (kDNA). Such protozoa constitute interesting models to investigate the mechanisms that orchestrate the equal distribution of structures between daughter cells (Steinert and Van Assel, 1967; Crosgrove and Skeen, 1970; Woodward and Gull, 1990). Seven trypanosomatid species co-evolve with a single obligate bacterium that divides in synchronization with the host cell, providing an opportunity to study cell cycle regulation and the evolution of symbiotic associations (Motta et al, 2010; Brum et al, 2014). Symbiont-bearing trypanosomatids were reclassified into three genera: Angomonas, Strigomonas, and Kentomonas (Teixeira et al, 2011; Votýpka et al, 2014)

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