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Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host
BACKGROUND: The family Trypanosomatidae encompasses parasitic flagellates, some of which cause serious vector-transmitted diseases of humans and domestic animals. However, insect-restricted parasites represent the ancestral and most diverse group within the family. They display a range of unusual fe...
Autores principales: | , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7712620/ https://www.ncbi.nlm.nih.gov/pubmed/33267865 http://dx.doi.org/10.1186/s12915-020-00916-y |
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author | Kostygov, Alexei Y. Frolov, Alexander O. Malysheva, Marina N. Ganyukova, Anna I. Chistyakova, Lyudmila V. Tashyreva, Daria Tesařová, Martina Spodareva, Viktoria V. Režnarová, Jana Macedo, Diego H. Butenko, Anzhelika d’Avila-Levy, Claudia M. Lukeš, Julius Yurchenko, Vyacheslav |
author_facet | Kostygov, Alexei Y. Frolov, Alexander O. Malysheva, Marina N. Ganyukova, Anna I. Chistyakova, Lyudmila V. Tashyreva, Daria Tesařová, Martina Spodareva, Viktoria V. Režnarová, Jana Macedo, Diego H. Butenko, Anzhelika d’Avila-Levy, Claudia M. Lukeš, Julius Yurchenko, Vyacheslav |
author_sort | Kostygov, Alexei Y. |
collection | PubMed |
description | BACKGROUND: The family Trypanosomatidae encompasses parasitic flagellates, some of which cause serious vector-transmitted diseases of humans and domestic animals. However, insect-restricted parasites represent the ancestral and most diverse group within the family. They display a range of unusual features and their study can provide insights into the biology of human pathogens. Here we describe Vickermania, a new genus of fly midgut-dwelling parasites that bear two flagella in contrast to other trypanosomatids, which are unambiguously uniflagellate. RESULTS: Vickermania has an odd cell cycle, in which shortly after the division the uniflagellate cell starts growing a new flagellum attached to the old one and preserves their contact until the late cytokinesis. The flagella connect to each other throughout their whole length and carry a peculiar seizing structure with a paddle-like apex and two lateral extensions at their tip. In contrast to typical trypanosomatids, which attach to the insect host’s intestinal wall, Vickermania is separated from it by a continuous peritrophic membrane and resides freely in the fly midgut lumen. CONCLUSIONS: We propose that Vickermania developed a survival strategy that relies on constant movement preventing discharge from the host gut due to intestinal peristalsis. Since these parasites cannot attach to the midgut wall, they were forced to shorten the period of impaired motility when two separate flagella in dividing cells interfere with each other. The connection between the flagella ensures their coordinate movement until the separation of the daughter cells. We propose that Trypanosoma brucei, a severe human pathogen, during its development in the tsetse fly midgut faces the same conditions and follows the same strategy as Vickermania by employing an analogous adaptation, the flagellar connector. |
format | Online Article Text |
id | pubmed-7712620 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-77126202020-12-03 Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host Kostygov, Alexei Y. Frolov, Alexander O. Malysheva, Marina N. Ganyukova, Anna I. Chistyakova, Lyudmila V. Tashyreva, Daria Tesařová, Martina Spodareva, Viktoria V. Režnarová, Jana Macedo, Diego H. Butenko, Anzhelika d’Avila-Levy, Claudia M. Lukeš, Julius Yurchenko, Vyacheslav BMC Biol Research Article BACKGROUND: The family Trypanosomatidae encompasses parasitic flagellates, some of which cause serious vector-transmitted diseases of humans and domestic animals. However, insect-restricted parasites represent the ancestral and most diverse group within the family. They display a range of unusual features and their study can provide insights into the biology of human pathogens. Here we describe Vickermania, a new genus of fly midgut-dwelling parasites that bear two flagella in contrast to other trypanosomatids, which are unambiguously uniflagellate. RESULTS: Vickermania has an odd cell cycle, in which shortly after the division the uniflagellate cell starts growing a new flagellum attached to the old one and preserves their contact until the late cytokinesis. The flagella connect to each other throughout their whole length and carry a peculiar seizing structure with a paddle-like apex and two lateral extensions at their tip. In contrast to typical trypanosomatids, which attach to the insect host’s intestinal wall, Vickermania is separated from it by a continuous peritrophic membrane and resides freely in the fly midgut lumen. CONCLUSIONS: We propose that Vickermania developed a survival strategy that relies on constant movement preventing discharge from the host gut due to intestinal peristalsis. Since these parasites cannot attach to the midgut wall, they were forced to shorten the period of impaired motility when two separate flagella in dividing cells interfere with each other. The connection between the flagella ensures their coordinate movement until the separation of the daughter cells. We propose that Trypanosoma brucei, a severe human pathogen, during its development in the tsetse fly midgut faces the same conditions and follows the same strategy as Vickermania by employing an analogous adaptation, the flagellar connector. BioMed Central 2020-12-02 /pmc/articles/PMC7712620/ /pubmed/33267865 http://dx.doi.org/10.1186/s12915-020-00916-y Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Kostygov, Alexei Y. Frolov, Alexander O. Malysheva, Marina N. Ganyukova, Anna I. Chistyakova, Lyudmila V. Tashyreva, Daria Tesařová, Martina Spodareva, Viktoria V. Režnarová, Jana Macedo, Diego H. Butenko, Anzhelika d’Avila-Levy, Claudia M. Lukeš, Julius Yurchenko, Vyacheslav Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host |
title | Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host |
title_full | Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host |
title_fullStr | Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host |
title_full_unstemmed | Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host |
title_short | Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host |
title_sort | vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7712620/ https://www.ncbi.nlm.nih.gov/pubmed/33267865 http://dx.doi.org/10.1186/s12915-020-00916-y |
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