Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-12T21:20:58.276Z Has data issue: false hasContentIssue false
  • English
  • Français

Structural Characterization of the Cell Division Cycle in Strigomonas culicis, an Endosymbiont-Bearing Trypanosomatid

Published online by Cambridge University Press:  03 January 2014

Felipe Lopes Brum ,
Carolina Moura Costa Catta-Preta ,
Wanderley de Souza ,
Sergio Schenkman ,
Maria Carolina Elias  and
Maria Cristina Machado Motta
Felipe Lopes Brum
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil
Carolina Moura Costa Catta-Preta
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil
Wanderley de Souza
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil Instituto Nacional de Metrologia, Normalização e Qualidade Industrial - Inmetro, Rio de Janeiro, RJ, 25250-020, Brazil
Sergio Schenkman
Affiliation:
Departamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal de São Paulo, São Paulo, SP, 04023-062, Brazil
Maria Carolina Elias
Affiliation:
Laboratório Especial de Ciclo Celular, Instituto Butantan, São Paulo, SP, 05503-900, Brazil
Maria Cristina Machado Motta*
Affiliation:
Laboratório de Ultraestrutura Celular Hertha Meyer, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil Instituto Nacional de Ciência e Tecnologia em Biologia Estrutural e Bioimagens, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, 21941-590, Brazil
*
*Corresponding author. E-mail: [email protected]
Get access

Abstract

Strigomonas culicis (previously referred to as Blastocrithidia culicis) is a monoxenic trypanosomatid harboring a symbiotic bacterium, which maintains an obligatory relationship with the host protozoan. Investigations of the cell cycle in symbiont harboring trypanosomatids suggest that the bacterium divides in coordination with other host cell structures, particularly the nucleus. In this study we used light and electron microscopy followed by three-dimensional reconstruction to characterize the symbiont division during the cell cycle of S. culicis. We observed that during this process, the symbiotic bacterium presents different forms and is found at different positions in relationship to the host cell structures. At the G1/S phase of the protozoan cell cycle, the endosymbiont exhibits a constricted form that appears to elongate, resulting in the bacterium division, which occurs before kinetoplast and nucleus segregation. During cytokinesis, the symbionts are positioned close to each nucleus to ensure that each daughter cell will inherit a single copy of the bacterium. These observations indicated that the association of the bacterium with the protozoan nucleus coordinates the cell cycle in both organisms.

Keywords

cell cyclecoordinated divisionendosymbiosismicroscopy analysisorganelle positioning3D reconstructiontrypanosomatids
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 20 , Issue 1 , February 2014 , pp. 228 - 237
Copyright
Copyright © Microscopy Society of America 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

Both authors contributed equally to this work.

References

Alves, J.M.P., Serrano, M.G., Silva, F.M., Voegtly, L.J., Matveyev, A., Teixeira, M.M.G., Camargo, E.P. & Buck, G.A. (2013). Genome evolution and phylogenomic analysis of Candidatus kinetoplastibacterium, the betaproteobacterial endosymbionts of Strigomonas and Angomonas . Genome Biol Evol Adv Access 5, 338–350.CrossRefGoogle ScholarPubMed
Ambit, A., Fasel, N., Coombs, G.H. & Mottram, J.C. (2008). An essential role for the Leishmania major metacaspase in cell cycle progression. Cell Death Differ 15, 113–122.CrossRefGoogle ScholarPubMed
Andrade, I.S., Vianez-Junior, J.L., Goulard, C.L., Homble, F., Ruysschaert, J.M., Almeida Von, W.M., Bisch, P.M., De Souza, W., Mohana-Borges, R. & Motta, M.C. (2011). Characterization of a porin channel in the endosymbiont of the trypanosomatid protozoan Crithidia deanei . Microbiology 157, 2818–2830.CrossRefGoogle ScholarPubMed
Bhattacharya, A. & Ghosh, M. (1985). Cell cycle of Leishmania donovani . Indian J Exp Biol 23, 629–634.Google ScholarPubMed
Cosgrove, W.B. & Skeen, M.J. (1970). The cell cycle in Crithidia fasciculata. Temporal relationships between synthesis of deoxyribonucleic acid in the nucleus and in the kinetoplast. J Protozool 17, 172–177.CrossRefGoogle ScholarPubMed
De Souza, W. (2002). Basic cell biology of Trypanosoma cruzi . Curr Pharm Des 8, 269–285.Google Scholar
Elias, M.C., Da Cunha, J.P., Faria, F.P., Mortara, R.A. & Freymuller, E. (2007). Morphological events during the Trypanosoma cruzi cell cycle. Protist 158, 147–157.Google Scholar
Girard-Dias, W., Alcântara, C.L., Cunha-e-Silva, N., De Souza, W. & Miranda, K. (2012). On the ultrastructural organization of Trypanosoma cruzi using cryopreparation methods and electron tomography. Histochem Cell Biol 138, 821–831.Google Scholar
Hammarton, T.C. (2007). Cell cycle regulation in Trypanosoma brucei . Mol Biochem Parasitol 153, 1–8.Google Scholar
Jensen, R.E. & Englund, P.T. (2012). Network news: Replication of kinetoplast DNA. Annu Rev Microbiol 66, 473–491.CrossRefGoogle ScholarPubMed
Kuroiwa, T. (2010). Mechanisms of organelle division and inheritance and their implications regarding the origin of eukaryotic cells. Proc Japan Acad Series B Phys and Biol Sci 86, 455–471.Google Scholar
Lacomble, S., Vaughan, S., Gadelha, C., Morphew, M.K. & Shaw, M.K. (2009). Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography. J Cell Sci 122, 1081–1090.Google Scholar
Lemgruber, L., Kudryashev, M., Dekiwadia, C., Rigiar, D.T., Baum, J., Stahiberg, H., Ralph, S.A. & Frischknecht, F. (2013). Cryo-electron tomography reveals four-membrane architecture of the Plasmodium apicoplast. Malar J 12, 12–25.Google Scholar
Matthews, K.R., Sherwin, T. & Kull, K. (1995). Mitochondrial genome repositioning during the differentiation of the African trypanosome between life cycle forms is microtubule mediated. J Cell Sci 108, 2231–2239.Google Scholar
McKean, P.G. (2003). Coordination of cell cycle and cytokinesis in Trypanosoma brucei . Curr Opin Microbiol 6, 600–607.CrossRefGoogle ScholarPubMed
Minocha, N., Kumar, D., Rajanala, K. & Saha, S. (2011). Kinetoplast morphology and segregation pattern as a marker for cell cycle progression in Leishmania donovani . J Euk Microbiol 58, 249–253.Google Scholar
Miranda, K., Pace, D.A., Contron, R., Rodrigues, J.C., Fang, J., Smith, A., Rohloff, P., Coelho, E., De Haas, F., De Souza, W., Coppens, I., Sibley, L.D. & Moreno, S.N. (2010). Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole. Mol Microbiol 76, 1358–1375.Google Scholar
Motta, M.C., Picchi, G.F., Palmie-Peixoto, I.V., Rocha, M.R., De Carvalho, T.M., Morgado-Diaz, J., De Souza, W., Goldenberg, S. & Fragoso, S.P. (2004). The microtubule analog protein, FtsZ, in the endosymbiont of trypanosomatid protozoa. J Eukaryot Microbiol 4, 394–401.Google Scholar
Motta, M.C.M. (2010). Endosymbiosis in trypanosomatids as a model to study cell evolution. Open Parasitol J 4, 139–147.Google Scholar
Motta, M.C.M., Azevedo-Martins, A.C., De Souza, S.S., Catta-Preta, C.M.C., Silva, R., Klein, C.C., Gonzaga, L., Cunha, O.L., Ciapina, L.P., Brocchi, M., Colabardini, A.C., Lima, B.A., Machado, C.R., Soares, C.M.A., Probst, C.M., Menezes, C.B.A., Bartholomeu, D.C., Gradia, D.F., Payoni, D.P., Grisard, E.C., Fantinatti-Garboggini, F., Marchini, F.K., Rodrigues-Luiz, G.F., Wagner, G., Goldman, G.H., Sagot, M.F., Pereira, M., Stoco, P.H., Mendonça-Neto, R.P., Teixeira, S.M.R., Maciel, T.E.F., Mendes, T.A.O., Ürményi, T.P., De Souza, M.W., Schenkman, S. & Vasconcelos, A.T. (2013). Predicting the proteins of Angomonas deanei, Strigomonas culicis and their respective endosymbionts reveals new aspects of the trypanosomatidae family. PLoS One 8, e60209. Google Scholar
Motta, M.C.M., Catta-Preta, C.M.C., Schenkman, S., Azevedo-Martins, A.C., Miranda, K., Elias, M.C. & De Souza, W. (2010). The bacterium endosymbiont of Crithidia deanei undergoes coordinated division with the host cell nucleus. PLoS One 5, e12415. Google Scholar
Motta, M.C.M., Monteiro-Leal, L.H., De Souza, W., Almeida, D.F. & Ferreira, L.C.S. (1997). Detection of penicillin-binding proteins in endosymbionts of the trypanosomatid Crithidia deanei . J Euk Microbiol 44, 492–496.Google Scholar
Motta, M.C.M., Soares, M.J. & De Souza, W. (1991). Freeze-fracture study of endosymbiont bearing trypanosomatids of the Crithidia genus. Micr Electr Biol Cel 15, 131–144.Google Scholar
Novy, F.G., McNeal, W.J. & Torrey, H.N. (1907). The trypanosomes of mosquitoes and other insects. J Infective Dis 4, 223–276.Google Scholar
Ogbadoyi, E., Ersfeld, K., Robinson, D., Sherwin, T. & Gull, K. (2000). Architecture of the Trypanosoma brucei nucleus during interphase and mitosis. Chromosoma 108, 501–513.Google Scholar
Paredes-Santos, T.C., de Souza, W. & Attias, M. (2012). Dynamics and 3D organization of secretory organelles of Toxoplasma gondii . J Struct Biol 177(2), 420–430.Google Scholar
Ramos, T.C., Freymuller-Haapalainen, E. & Schenkman, S. (2011). Three-dimensional reconstruction of Trypanosoma cruzi epimastigotes and organelle distribution along the cell division cycle. Cytometry Part A: J Int Soc Analyt Cytol 79, 538–544.Google Scholar
Siegel, T.N., Hekstra, D.R. & Cross, G.A.M. (2008). Analysis of the Trypanosoma brucei cell cycle by quantitative DAPI imaging. Mol Biochem Parasitol 160, 171–174.CrossRefGoogle ScholarPubMed
Sinha, K.M., Hines, J.C. & Ray, D.S. (2006). Cell cycle-dependent localization and properties of a second mitochondria DNA ligase in Crithidia fasciculata . Eukaryot Cell 5, 54–61.Google Scholar
Soares, M.J. & De Souza, W. (1987). Freeze-fracture study of the endosymbiont of Blastocrithidia culicis . J Protozool 35, 370–374.Google Scholar
Striepen, B., Crawford, M.J., Shaw, M.K., Tilney, L.G., Seeber, F. & Roos, D.S. (2000). The plastid of Toxoplasma gondii is divided by association with the centrosomes. J Cell Biol 151, 1423–1434.Google Scholar
Teixeira, M.M., Borghesan, T.C., Ferreira, R.C., Santos, M.A., Takata, M., Campaner, C.S., Nunes, V.L., Milder, R.V., De Souza, W. & Camargo, E.P. (2011). Phylogenetic validation of the genera Angomonas and Strigomonas of trypanosomatids harboring bacterial endosymbionts with the description of new species of trypanosomatids and of proteobacterial symbionts. Protist 162, 503–524.Google Scholar
Warren, L.G. (1960). Metabolism of Schizotrypanum cruzi, Chagas 1. Effect of culture age and substrate concentration on respiratory rate. J Parasitol 46, 529–539.Google Scholar
Wheller, R.J., Gluenz, E. & Gull, K. (2011). The cell cycle of Leishmania: Morphogenetic events and their implications for parasite biology. Mol Microbiol 79, 647–662.Google Scholar
Williams, A.F. (1971). Dynamics of microbial populations. In System Analysis and Simulation Ecology, Patten, B. (Ed.), pp. 247–262. New York: Academic Press.Google Scholar
Woodward, R. & Gull, K. (1990). Timing of nuclear and kinetoplast DNA replication and early morphological events in the cell cycle of Trypanosoma brucei . J Cell Sci 5, 49–57.CrossRefGoogle Scholar

Brum Supplementary Material

Movie 1

Download Brum Supplementary Material(Video)
Video 184.9 MB

Brum Supplementary Material

Movie 2

Download Brum Supplementary Material(Video)
Video 200.4 MB

Brum Supplementary Material

Movie 3

Download Brum Supplementary Material(Video)
Video 153.8 MB