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

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 betwee...

Full description

Bibliographic Details
Main Authors: Carolina Moura Costa Catta Preta, Felipe eBrum, Camila eDa Silva, Aline eZuma, Maria Carolina eElias, Wanderley eDe Souza, Sergio eSchenkman, Maria Cristina Machado Motta
Format: Article
Language:English
Published: Frontiers Media S.A. 2015-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2015.00520/full
_version_ 1818982195875807232
author Carolina Moura Costa Catta Preta
Felipe eBrum
Camila eDa Silva
Aline eZuma
Maria Carolina eElias
Wanderley eDe Souza
Sergio eSchenkman
Maria Cristina Machado Motta
author_facet Carolina Moura Costa Catta Preta
Felipe eBrum
Camila eDa Silva
Aline eZuma
Maria Carolina eElias
Wanderley eDe Souza
Sergio eSchenkman
Maria Cristina Machado Motta
author_sort Carolina Moura Costa Catta Preta
collection DOAJ
description 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.
first_indexed 2024-12-20T17:43:22Z
format Article
id doaj.art-a13150c5d2c14521a010cb37800c9f70
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-12-20T17:43:22Z
publishDate 2015-06-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-a13150c5d2c14521a010cb37800c9f702022-12-21T19:31:03ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2015-06-01610.3389/fmicb.2015.00520130220Endosymbiosis in trypanosomatid protozoa: the bacterium division is controlled during the host cell cycleCarolina Moura Costa Catta Preta0Felipe eBrum1Camila eDa Silva2Aline eZuma3Maria Carolina eElias4Wanderley eDe Souza5Sergio eSchenkman6Maria Cristina Machado Motta7Universidade Federal do Rio de JaneiroUniversidade Federal do Rio de JaneiroUniversidade Federal do Rio de JaneiroUniversidade Federal do Rio de JaneiroButantanUniversidade Federal do Rio de JaneiroUniversidade Federal de São PauloUniversidade Federal do Rio de JaneiroMutualism 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.http://journal.frontiersin.org/Journal/10.3389/fmicb.2015.00520/fullCell CycleSymbiosisTrypanosomatid protozoaCell evolutiondivision control
spellingShingle Carolina Moura Costa Catta Preta
Felipe eBrum
Camila eDa Silva
Aline eZuma
Maria Carolina eElias
Wanderley eDe Souza
Sergio eSchenkman
Maria Cristina Machado Motta
Endosymbiosis in trypanosomatid protozoa: the bacterium division is controlled during the host cell cycle
Frontiers in Microbiology
Cell Cycle
Symbiosis
Trypanosomatid protozoa
Cell evolution
division control
title Endosymbiosis in trypanosomatid protozoa: the bacterium division is controlled during the host cell cycle
title_full Endosymbiosis in trypanosomatid protozoa: the bacterium division is controlled during the host cell cycle
title_fullStr Endosymbiosis in trypanosomatid protozoa: the bacterium division is controlled during the host cell cycle
title_full_unstemmed Endosymbiosis in trypanosomatid protozoa: the bacterium division is controlled during the host cell cycle
title_short Endosymbiosis in trypanosomatid protozoa: the bacterium division is controlled during the host cell cycle
title_sort endosymbiosis in trypanosomatid protozoa the bacterium division is controlled during the host cell cycle
topic Cell Cycle
Symbiosis
Trypanosomatid protozoa
Cell evolution
division control
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2015.00520/full
work_keys_str_mv AT carolinamouracostacattapreta endosymbiosisintrypanosomatidprotozoathebacteriumdivisioniscontrolledduringthehostcellcycle
AT felipeebrum endosymbiosisintrypanosomatidprotozoathebacteriumdivisioniscontrolledduringthehostcellcycle
AT camilaedasilva endosymbiosisintrypanosomatidprotozoathebacteriumdivisioniscontrolledduringthehostcellcycle
AT alineezuma endosymbiosisintrypanosomatidprotozoathebacteriumdivisioniscontrolledduringthehostcellcycle
AT mariacarolinaeelias endosymbiosisintrypanosomatidprotozoathebacteriumdivisioniscontrolledduringthehostcellcycle
AT wanderleyedesouza endosymbiosisintrypanosomatidprotozoathebacteriumdivisioniscontrolledduringthehostcellcycle
AT sergioeschenkman endosymbiosisintrypanosomatidprotozoathebacteriumdivisioniscontrolledduringthehostcellcycle
AT mariacristinamachadomotta endosymbiosisintrypanosomatidprotozoathebacteriumdivisioniscontrolledduringthehostcellcycle