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Cell Cycle-Dependent Flagellar Disassembly in a Firebug Trypanosomatid Leptomonas pyrrhocoris.
mBio ( IF 5.1 ) Pub Date : 2019-11-26 , DOI: 10.1128/mbio.02424-19
Cynthia Y He 1 , Adarsh Singh 2, 3 , Vyacheslav Yurchenko 4, 5
Affiliation  

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.

中文翻译:

萤火虫锥虫类Leptomonas pyrrhocoris的细胞周期依赖性鞭毛分解。

目前对鞭毛/纤毛长度调节的理解集中在鞭毛长度一致的一些模型生物上。猪热单胞菌是萤火虫的一种单一的锥虫寄生虫。当在体外培养时,吡咯氏乳杆菌每4.2±0.2 h复制一次,这是迄今为止报道的锥虫的最短倍增时间。每个吡咯菌的细胞都以单个鞭毛开始其细胞周期。新的鞭毛从头开始组装,而旧的鞭毛在整个细胞周期中持续存在。异步吡咯球菌种群中的鞭毛表现出约3至24μm的巨大长度变化,这使人们怀疑基于这些细胞中组装和拆卸速率之间的单个平衡点的长度调节机制的存在。通过对活吡咯菌的活细胞进行成像,如果不是在新鞭毛的初次组装之前,则观察到现有旧鞭毛的部分拆卸。数学建模表明鞭毛生长速率和鞭毛长度之间呈反比关系,并推断存在不同速率的不同细胞周期依赖性拆卸机制。基于这些观察结果,我们提出了一个最小-最大模型,该模型可以解释观察到的异步拟南芥的鞭毛长度范围。该模型还可以应用于鞭毛长度发生变化的其他鞭毛生物。重要信息目前对锥虫的细胞周期中鞭毛生物发生的了解仅限于一些致病物种,包括布鲁氏锥虫,克鲁斯锥虫和利什曼原虫。迄今为止研究的锥虫鞭毛鞭毛最显着的特征是细胞周期中的极端稳定性和睫状组织的分解/吸收不足。这与衣藻和哺乳动物细胞中的纤毛不同,纤毛在细胞周期开始之前会完全吸收。在这项研究中,我们检查了拟南芥(Leptomonas pyrrhocoris)细胞周期中的鞭毛复制,记录了所有锥虫科的最短复制时间,以及其在有限流动性的琼脂糖凝胶上培养的能力,我们能够通过细胞周期对这些细胞进行成像。首次在锥虫中观察到与周转不同的细胞周期特异性鞭毛快速分解。鉴于观察到的长度依赖性生长速率和存在不同的分解机制,
更新日期:2019-11-01
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