Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid <italic toggle="yes">Leptomonas pyrrhocoris</italic>

ABSTRACT Current understanding of flagellum/cilium length regulation focuses on a few model organisms with flagella of uniform length. Leptomonas pyrrhocoris is a monoxenous trypanosomatid parasite of firebugs. When cultivated in vitro, L. pyrrhocoris duplicates every 4.2 ± 0.2 h, representing the s...

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Autores principales:	Cynthia Y. He, Adarsh Singh, Vyacheslav Yurchenko
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	flagellar length regulation Leptomonas pyrrhocoris trypanosomatids flagellum disassembly Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/56c930afc2e5482796f1543a95577e89
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spelling	oai:doaj.org-article:56c930afc2e5482796f1543a95577e892021-11-15T15:54:47ZCell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid <italic toggle="yes">Leptomonas pyrrhocoris</italic>10.1128/mBio.02424-192150-7511https://doaj.org/article/56c930afc2e5482796f1543a95577e892019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02424-19https://doaj.org/toc/2150-7511ABSTRACT Current understanding of flagellum/cilium length regulation focuses on a few model organisms with flagella of uniform length. Leptomonas pyrrhocoris is a monoxenous trypanosomatid parasite of firebugs. When cultivated in vitro, L. pyrrhocoris duplicates every 4.2 ± 0.2 h, representing the shortest doubling time reported for trypanosomatids so far. Each L. pyrrhocoris cell starts its cell cycle with a single flagellum. A new flagellum is assembled de novo, while the old flagellum persists throughout the cell cycle. The flagella in an asynchronous L. pyrrhocoris population exhibited a vast length variation of ∼3 to 24 μm, casting doubt on the presence of a length regulation mechanism based on a single balance point between the assembly and disassembly rate in these cells. Through imaging of live L. pyrrhocoris cells, a rapid, partial disassembly of the existing, old flagellum is observed upon, if not prior to, the initial assembly of a new flagellum. Mathematical modeling demonstrated an inverse correlation between the flagellar growth rate and flagellar length and inferred the presence of distinct, cell cycle-dependent disassembly mechanisms with different rates. On the basis of these observations, we proposed a min-max model that could account for the vast flagellar length range observed for asynchronous L. pyrrhocoris. This model may also apply to other flagellated organisms with flagellar length variation. IMPORTANCE Current understanding of flagellum biogenesis during the cell cycle in trypanosomatids is limited to a few pathogenic species, including Trypanosoma brucei, Trypanosoma cruzi, and Leishmania spp. The most notable characteristics of trypanosomatid flagella studied so far are the extreme stability and lack of ciliary disassembly/absorption during the cell cycle. This is different from cilia in Chlamydomonas and mammalian cells, which undergo complete absorption prior to cell cycle initiation. In this study, we examined flagellum duplication during the cell cycle of Leptomonas pyrrhocoris. With the shortest duplication time documented for all Trypanosomatidae and its amenability to culture on agarose gel with limited mobility, we were able to image these cells through the cell cycle. Rapid, cell cycle-specific flagellum disassembly different from turnover was observed for the first time in trypanosomatids. Given the observed length-dependent growth rate and the presence of different disassembly mechanisms, we proposed a min-max model that can account for the flagellar length variation observed in L. pyrrhocoris.Cynthia Y. HeAdarsh SinghVyacheslav YurchenkoAmerican Society for Microbiologyarticleflagellar length regulationLeptomonas pyrrhocoristrypanosomatidsflagellum disassemblyflagellar length regulationMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	flagellar length regulation Leptomonas pyrrhocoris trypanosomatids flagellum disassembly flagellar length regulation Microbiology QR1-502
spellingShingle	flagellar length regulation Leptomonas pyrrhocoris trypanosomatids flagellum disassembly flagellar length regulation Microbiology QR1-502 Cynthia Y. He Adarsh Singh Vyacheslav Yurchenko Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid <italic toggle="yes">Leptomonas pyrrhocoris</italic>
description	ABSTRACT Current understanding of flagellum/cilium length regulation focuses on a few model organisms with flagella of uniform length. Leptomonas pyrrhocoris is a monoxenous trypanosomatid parasite of firebugs. When cultivated in vitro, L. pyrrhocoris duplicates every 4.2 ± 0.2 h, representing the shortest doubling time reported for trypanosomatids so far. Each L. pyrrhocoris cell starts its cell cycle with a single flagellum. A new flagellum is assembled de novo, while the old flagellum persists throughout the cell cycle. The flagella in an asynchronous L. pyrrhocoris population exhibited a vast length variation of ∼3 to 24 μm, casting doubt on the presence of a length regulation mechanism based on a single balance point between the assembly and disassembly rate in these cells. Through imaging of live L. pyrrhocoris cells, a rapid, partial disassembly of the existing, old flagellum is observed upon, if not prior to, the initial assembly of a new flagellum. Mathematical modeling demonstrated an inverse correlation between the flagellar growth rate and flagellar length and inferred the presence of distinct, cell cycle-dependent disassembly mechanisms with different rates. On the basis of these observations, we proposed a min-max model that could account for the vast flagellar length range observed for asynchronous L. pyrrhocoris. This model may also apply to other flagellated organisms with flagellar length variation. IMPORTANCE Current understanding of flagellum biogenesis during the cell cycle in trypanosomatids is limited to a few pathogenic species, including Trypanosoma brucei, Trypanosoma cruzi, and Leishmania spp. The most notable characteristics of trypanosomatid flagella studied so far are the extreme stability and lack of ciliary disassembly/absorption during the cell cycle. This is different from cilia in Chlamydomonas and mammalian cells, which undergo complete absorption prior to cell cycle initiation. In this study, we examined flagellum duplication during the cell cycle of Leptomonas pyrrhocoris. With the shortest duplication time documented for all Trypanosomatidae and its amenability to culture on agarose gel with limited mobility, we were able to image these cells through the cell cycle. Rapid, cell cycle-specific flagellum disassembly different from turnover was observed for the first time in trypanosomatids. Given the observed length-dependent growth rate and the presence of different disassembly mechanisms, we proposed a min-max model that can account for the flagellar length variation observed in L. pyrrhocoris.
format	article
author	Cynthia Y. He Adarsh Singh Vyacheslav Yurchenko
author_facet	Cynthia Y. He Adarsh Singh Vyacheslav Yurchenko
author_sort	Cynthia Y. He
title	Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid <italic toggle="yes">Leptomonas pyrrhocoris</italic>
title_short	Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid <italic toggle="yes">Leptomonas pyrrhocoris</italic>
title_full	Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid <italic toggle="yes">Leptomonas pyrrhocoris</italic>
title_fullStr	Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid <italic toggle="yes">Leptomonas pyrrhocoris</italic>
title_full_unstemmed	Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid <italic toggle="yes">Leptomonas pyrrhocoris</italic>
title_sort	cell cycle-dependent flagellar disassembly in a firebug trypanosomatid <italic toggle="yes">leptomonas pyrrhocoris</italic>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/56c930afc2e5482796f1543a95577e89
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Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid <italic toggle="yes">Leptomonas pyrrhocoris</italic>

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