On the possibility of yet a third kinetochore system in the protist phylum Euglenozoa.

IF 5.1 1区 生物学 Q1 MICROBIOLOGY
mBio Pub Date : 2024-10-30 DOI:10.1128/mbio.02936-24
Corinna Benz, Maximilian W D Raas, Pragya Tripathi, Drahomíra Faktorová, Eelco C Tromer, Bungo Akiyoshi, Julius Lukeš
{"title":"On the possibility of yet a third kinetochore system in the protist phylum Euglenozoa.","authors":"Corinna Benz, Maximilian W D Raas, Pragya Tripathi, Drahomíra Faktorová, Eelco C Tromer, Bungo Akiyoshi, Julius Lukeš","doi":"10.1128/mbio.02936-24","DOIUrl":null,"url":null,"abstract":"<p><p>Transmission of genetic material from one generation to the next is a fundamental feature of all living cells. In eukaryotes, a macromolecular complex called the kinetochore plays crucial roles during chromosome segregation by linking chromosomes to spindle microtubules. Little is known about this process in evolutionarily diverse protists. Within the supergroup Discoba, Euglenozoa forms a speciose group of unicellular flagellates-kinetoplastids, euglenids, and diplonemids. Kinetoplastids have an unconventional kinetochore system, while euglenids have subunits that are conserved among most eukaryotes. For diplonemids, a group of extremely diverse and abundant marine flagellates, it remains unclear what kind of kinetochores are present. Here, we employed deep homology detection protocols using profile-versus-profile Hidden Markov Model searches and AlphaFold-based structural comparisons to detect homologies that might have been previously missed. Interestingly, we still could not detect orthologs for most of the kinetoplastid or canonical kinetochore subunits with few exceptions including a putative centromere-specific histone H3 variant (cenH3/CENP-A), the spindle checkpoint protein Mad2, the chromosomal passenger complex members Aurora and INCENP, and broadly conserved proteins like CLK kinase and the meiotic synaptonemal complex proteins SYCP2/3 that also function at kinetoplastid kinetochores. We examined the localization of five candidate kinetochore-associated proteins in the model diplonemid, <i>Paradiplonema papillatum. Pp</i>CENP-A shows discrete dots in the nucleus, implying that it is likely a kinetochore component. <i>Pp</i>Mad2, <i>Pp</i>CLK<sup>KKT10/19</sup>, <i>Pp</i>SYCP2L1<sup>KKT17/18</sup>, and <i>Pp</i>INCENP reside in the nucleus, but no clear kinetochore localization was observed. Altogether, these results point to the possibility that diplonemids evolved a hitherto unknown type of kinetochore system.</p><p><strong>Importance: </strong>A macromolecular assembly called the kinetochore is essential for the segregation of genetic material during eukaryotic cell division. Therefore, characterization of kinetochores across species is essential for understanding the mechanisms involved in this key process across the eukaryotic tree of life. In particular, little is known about kinetochores in divergent protists such as Euglenozoa, a group of unicellular flagellates that includes kinetoplastids, euglenids, and diplonemids, the latter being a highly diverse and abundant component of marine plankton. While kinetoplastids have an unconventional kinetochore system and euglenids have a canonical one similar to traditional model eukaryotes, preliminary searches detected neither unconventional nor canonical kinetochore components in diplonemids. Here, we employed state-of-the-art deep homology detection protocols but still could not detect orthologs for the bulk of kinetoplastid-specific nor canonical kinetochore proteins in diplonemids except for a putative centromere-specific histone H3 variant. Our results suggest that diplonemids evolved kinetochores that do not resemble previously known ones.</p>","PeriodicalId":18315,"journal":{"name":"mBio","volume":null,"pages":null},"PeriodicalIF":5.1000,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"mBio","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/mbio.02936-24","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Transmission of genetic material from one generation to the next is a fundamental feature of all living cells. In eukaryotes, a macromolecular complex called the kinetochore plays crucial roles during chromosome segregation by linking chromosomes to spindle microtubules. Little is known about this process in evolutionarily diverse protists. Within the supergroup Discoba, Euglenozoa forms a speciose group of unicellular flagellates-kinetoplastids, euglenids, and diplonemids. Kinetoplastids have an unconventional kinetochore system, while euglenids have subunits that are conserved among most eukaryotes. For diplonemids, a group of extremely diverse and abundant marine flagellates, it remains unclear what kind of kinetochores are present. Here, we employed deep homology detection protocols using profile-versus-profile Hidden Markov Model searches and AlphaFold-based structural comparisons to detect homologies that might have been previously missed. Interestingly, we still could not detect orthologs for most of the kinetoplastid or canonical kinetochore subunits with few exceptions including a putative centromere-specific histone H3 variant (cenH3/CENP-A), the spindle checkpoint protein Mad2, the chromosomal passenger complex members Aurora and INCENP, and broadly conserved proteins like CLK kinase and the meiotic synaptonemal complex proteins SYCP2/3 that also function at kinetoplastid kinetochores. We examined the localization of five candidate kinetochore-associated proteins in the model diplonemid, Paradiplonema papillatum. PpCENP-A shows discrete dots in the nucleus, implying that it is likely a kinetochore component. PpMad2, PpCLKKKT10/19, PpSYCP2L1KKT17/18, and PpINCENP reside in the nucleus, but no clear kinetochore localization was observed. Altogether, these results point to the possibility that diplonemids evolved a hitherto unknown type of kinetochore system.

Importance: A macromolecular assembly called the kinetochore is essential for the segregation of genetic material during eukaryotic cell division. Therefore, characterization of kinetochores across species is essential for understanding the mechanisms involved in this key process across the eukaryotic tree of life. In particular, little is known about kinetochores in divergent protists such as Euglenozoa, a group of unicellular flagellates that includes kinetoplastids, euglenids, and diplonemids, the latter being a highly diverse and abundant component of marine plankton. While kinetoplastids have an unconventional kinetochore system and euglenids have a canonical one similar to traditional model eukaryotes, preliminary searches detected neither unconventional nor canonical kinetochore components in diplonemids. Here, we employed state-of-the-art deep homology detection protocols but still could not detect orthologs for the bulk of kinetoplastid-specific nor canonical kinetochore proteins in diplonemids except for a putative centromere-specific histone H3 variant. Our results suggest that diplonemids evolved kinetochores that do not resemble previously known ones.

关于原生动物门中可能存在第三个动核系统的问题。
遗传物质代代相传是所有活细胞的基本特征。在真核生物中,一种被称为动核的大分子复合物通过将染色体与纺锤体微管连接起来,在染色体分离过程中发挥着至关重要的作用。人们对进化过程中多种多样的原生生物的这一过程知之甚少。在 Discoba 超群中,Euglenozoa 形成了一个由单细胞鞭毛虫--动核细胞、Euglenid 和 diplonemids 组成的特殊群体。内生鞭毛虫有一个非常规的动核系统,而外生鞭毛虫的亚基在大多数真核生物中都是保守的。双鞭毛虫是一类种类繁多、数量巨大的海洋鞭毛虫,目前还不清楚它们的动核是哪一种。在这里,我们采用了深度同源性检测协议,利用profile-vers-us-profile隐马尔可夫模型搜索和基于AlphaFold的结构比较来检测以前可能被忽略的同源性。有趣的是,我们仍然无法检测到大多数动点细胞或典型动点支链亚基的同源物,只有少数例外,包括推测的中心粒特异性组蛋白 H3 变体(cenH3/CENP-A)、纺锤体检查点蛋白 Mad2、染色体客体复合体成员 Aurora 和 INCENP,以及广泛保守的蛋白,如 CLK 激酶和减数分裂突触复合体蛋白 SYCP2/3,它们也在动点细胞的动点支链上发挥作用。我们研究了五种候选动点相关蛋白在模式双鞭毛目(Paradiplonema papillatum)中的定位情况。PpCENP-A 在细胞核中显示出离散的小点,这意味着它很可能是一个动点元件。PpMad2、PpCLKKKT10/19、PpSYCP2L1KKT17/18 和 PpINCENP 位于细胞核中,但没有观察到明确的动点定位。总之,这些结果表明,双子叶植物可能进化出了一种迄今未知的动核系统:重要性:在真核细胞分裂过程中,遗传物质的分离离不开一种被称为动核的大分子组装体。因此,要了解真核生命树中这一关键过程所涉及的机制,就必须确定不同物种动核的特征。特别是,人们对不同原生动物(如优格伦动物)中的动核知之甚少,优格伦动物是一类单细胞鞭毛虫,包括动核细胞、优格伦动物和双鞭毛虫,后者是海洋浮游生物中种类繁多、数量巨大的组成部分。动核鞭毛虫有一个非常规的动核系统,而尤格林鞭毛虫有一个与传统模式真核生物类似的标准动核系统,但初步搜索发现双鞭毛虫中既没有非常规的也没有标准的动核元件。在这里,我们采用了最先进的深度同源性检测方案,但除了一种推测的中心粒特异性组蛋白 H3 变体外,仍然无法在双膜动物中检测到大部分动点细胞特异性或标准动点核心蛋白的同源物。我们的研究结果表明,双螺旋虫进化出的动核与之前已知的动核并不相似。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
mBio
mBio MICROBIOLOGY-
CiteScore
10.50
自引率
3.10%
发文量
762
审稿时长
1 months
期刊介绍: mBio® is ASM''s first broad-scope, online-only, open access journal. mBio offers streamlined review and publication of the best research in microbiology and allied fields.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信