Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis
Since Acanthamoeba polyphaga mimivirus (APMV) was identified in 2003, several other giant viruses of amoebae have been isolated, highlighting the uniqueness of this group. In this context, the tupanviruses were recently isolated from extreme environments in Brazil, presenting virions with an outstan...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-04-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.00671/full |
| _version_ | 1818485410359148544 |
|---|---|
| author | Lorena C. F. Silva Rodrigo Araújo Lima Rodrigues Graziele Pereira Oliveira Fabio Pio Dornas Bernard La Scola Erna G. Kroon Jônatas S. Abrahão |
| author_facet | Lorena C. F. Silva Rodrigo Araújo Lima Rodrigues Graziele Pereira Oliveira Fabio Pio Dornas Bernard La Scola Erna G. Kroon Jônatas S. Abrahão |
| author_sort | Lorena C. F. Silva |
| collection | DOAJ |
| description | Since Acanthamoeba polyphaga mimivirus (APMV) was identified in 2003, several other giant viruses of amoebae have been isolated, highlighting the uniqueness of this group. In this context, the tupanviruses were recently isolated from extreme environments in Brazil, presenting virions with an outstanding tailed structure and genomes containing the most complete set of translation genes of the virosphere. Unlike other giant viruses of amoebae, tupanviruses present a broad host range, being able to replicate not only in Acanthamoeba sp. but also in other amoebae, such as Vermamoeba vermiformis, a widespread, free-living organism. Although the Tupanvirus cycle in A. castellanii has been analyzed, there are no studies concerning the replication of tupanviruses in other host cells. Here, we present an in-depth microscopic study of the replication cycle of Tupanvirus in V. vermiformis. Our results reveal that Tupanvirus can enter V. vermiformis and generate new particles with similar morphology to when infecting A. castellanii cells. Tupanvirus establishes a well-delimited electron-dense viral factory in V. vermiformis, surrounded by lamellar structures, which appears different when compared with different A. castellanii cells. Moreover, viral morphogenesis occurs entirely in the host cytoplasm within the viral factory, from where complete particles, including the capsid and tail, are sprouted. Some of these particles have larger tails, which we named “supertupans.” Finally, we observed the formation of defective particles, presenting abnormalities of the tail and/or capsid. Taken together, the data presented here contribute to a better understanding of the biology of tupanviruses in previously unexplored host cells. |
| first_indexed | 2024-12-10T16:08:35Z |
| format | Article |
| id | doaj.art-2a8c0b69277c4db9be226180109ac464 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-10T16:08:35Z |
| publishDate | 2019-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-2a8c0b69277c4db9be226180109ac4642022-12-22T01:42:10ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-04-011010.3389/fmicb.2019.00671444187Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformisLorena C. F. Silva0Rodrigo Araújo Lima Rodrigues1Graziele Pereira Oliveira2Fabio Pio Dornas3Bernard La Scola4Erna G. Kroon5Jônatas S. Abrahão6Laboratório de Vírus, Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilLaboratório de Vírus, Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilLaboratório de Vírus, Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilFaculdade de Ciências Básicas e da Saúde, Departamento de Farmácia, Universidade Federal do Vale do Jequitinhonha e Mucuri, Diamantina, BrazilFaculté de Médecine, Aix-Marseille Université, Marseille, FranceLaboratório de Vírus, Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilLaboratório de Vírus, Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilSince Acanthamoeba polyphaga mimivirus (APMV) was identified in 2003, several other giant viruses of amoebae have been isolated, highlighting the uniqueness of this group. In this context, the tupanviruses were recently isolated from extreme environments in Brazil, presenting virions with an outstanding tailed structure and genomes containing the most complete set of translation genes of the virosphere. Unlike other giant viruses of amoebae, tupanviruses present a broad host range, being able to replicate not only in Acanthamoeba sp. but also in other amoebae, such as Vermamoeba vermiformis, a widespread, free-living organism. Although the Tupanvirus cycle in A. castellanii has been analyzed, there are no studies concerning the replication of tupanviruses in other host cells. Here, we present an in-depth microscopic study of the replication cycle of Tupanvirus in V. vermiformis. Our results reveal that Tupanvirus can enter V. vermiformis and generate new particles with similar morphology to when infecting A. castellanii cells. Tupanvirus establishes a well-delimited electron-dense viral factory in V. vermiformis, surrounded by lamellar structures, which appears different when compared with different A. castellanii cells. Moreover, viral morphogenesis occurs entirely in the host cytoplasm within the viral factory, from where complete particles, including the capsid and tail, are sprouted. Some of these particles have larger tails, which we named “supertupans.” Finally, we observed the formation of defective particles, presenting abnormalities of the tail and/or capsid. Taken together, the data presented here contribute to a better understanding of the biology of tupanviruses in previously unexplored host cells.https://www.frontiersin.org/article/10.3389/fmicb.2019.00671/fullTupanvirusviral characterizationviral cyclegiant virusesVermamoeba vermiformis |
| spellingShingle | Lorena C. F. Silva Rodrigo Araújo Lima Rodrigues Graziele Pereira Oliveira Fabio Pio Dornas Bernard La Scola Erna G. Kroon Jônatas S. Abrahão Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis Frontiers in Microbiology Tupanvirus viral characterization viral cycle giant viruses Vermamoeba vermiformis |
| title | Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis |
| title_full | Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis |
| title_fullStr | Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis |
| title_full_unstemmed | Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis |
| title_short | Microscopic Analysis of the Tupanvirus Cycle in Vermamoeba vermiformis |
| title_sort | microscopic analysis of the tupanvirus cycle in vermamoeba vermiformis |
| topic | Tupanvirus viral characterization viral cycle giant viruses Vermamoeba vermiformis |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.00671/full |
| work_keys_str_mv | AT lorenacfsilva microscopicanalysisofthetupanviruscycleinvermamoebavermiformis AT rodrigoaraujolimarodrigues microscopicanalysisofthetupanviruscycleinvermamoebavermiformis AT grazielepereiraoliveira microscopicanalysisofthetupanviruscycleinvermamoebavermiformis AT fabiopiodornas microscopicanalysisofthetupanviruscycleinvermamoebavermiformis AT bernardlascola microscopicanalysisofthetupanviruscycleinvermamoebavermiformis AT ernagkroon microscopicanalysisofthetupanviruscycleinvermamoebavermiformis AT jonatassabrahao microscopicanalysisofthetupanviruscycleinvermamoebavermiformis |