Distribution of membrane trafficking system components across ciliate diversity highlights heterogenous organelle-associated machinery.

IF 3.6 3区 生物学 Q3 CELL BIOLOGY
Traffic Pub Date : 2022-04-01 Epub Date: 2022-03-01 DOI:10.1111/tra.12834
Elisabeth Richardson, Joel B Dacks
{"title":"Distribution of membrane trafficking system components across ciliate diversity highlights heterogenous organelle-associated machinery.","authors":"Elisabeth Richardson,&nbsp;Joel B Dacks","doi":"10.1111/tra.12834","DOIUrl":null,"url":null,"abstract":"<p><p>The ciliate phylum is a group of protists noted for their unusual membrane trafficking system and apparent environmental ubiquity; as highly successful microbial predators, they are found in all manner of environments and the ability for specific species to adapt to extremely challenging conditions makes them valued as bioindicators. Ciliates have also been used for many years as cell biological models because of their large cell size and ease of culturing, and for many fundamental cell structures, particularly membrane-bound organelles, ciliates were some of the earliest organisms in which these were observed via microscopy. In this study, we carried out a comparative genomic survey of selected membrane trafficking proteins in a pan-ciliate transcriptome and genome dataset. We observed considerable loss of membrane trafficking system (MTS) proteins that would indicate a loss of machinery that is generally conserved across eukaryotic diversity, even after controlling for potentially incomplete genome representation. In particular, the complete DSL1 complex was missing in all surveyed ciliates. This protein complex has been shown as involved in peroxisome biogenesis in some model systems, and a paucity of DSL1 components has been indicative of degenerate peroxisome. However, Tetrahymena thermophila (formerly Tetrahymena pyroformis) was one of the original models for visualizing peroxisomes. Conversely, the AP3 complex essential for mucocyst maturation in T. thermophila, is poorly conserved despite the presence of secretory lysosome-related organelles across ciliate diversity. We discuss potential resolutions for these apparent paradoxes in the context of the heterogenous distribution of MTS machinery across the diversity of ciliates.</p>","PeriodicalId":23207,"journal":{"name":"Traffic","volume":"23 4","pages":"208-220"},"PeriodicalIF":3.6000,"publicationDate":"2022-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"8","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Traffic","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1111/tra.12834","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2022/3/1 0:00:00","PubModel":"Epub","JCR":"Q3","JCRName":"CELL BIOLOGY","Score":null,"Total":0}
引用次数: 8

Abstract

The ciliate phylum is a group of protists noted for their unusual membrane trafficking system and apparent environmental ubiquity; as highly successful microbial predators, they are found in all manner of environments and the ability for specific species to adapt to extremely challenging conditions makes them valued as bioindicators. Ciliates have also been used for many years as cell biological models because of their large cell size and ease of culturing, and for many fundamental cell structures, particularly membrane-bound organelles, ciliates were some of the earliest organisms in which these were observed via microscopy. In this study, we carried out a comparative genomic survey of selected membrane trafficking proteins in a pan-ciliate transcriptome and genome dataset. We observed considerable loss of membrane trafficking system (MTS) proteins that would indicate a loss of machinery that is generally conserved across eukaryotic diversity, even after controlling for potentially incomplete genome representation. In particular, the complete DSL1 complex was missing in all surveyed ciliates. This protein complex has been shown as involved in peroxisome biogenesis in some model systems, and a paucity of DSL1 components has been indicative of degenerate peroxisome. However, Tetrahymena thermophila (formerly Tetrahymena pyroformis) was one of the original models for visualizing peroxisomes. Conversely, the AP3 complex essential for mucocyst maturation in T. thermophila, is poorly conserved despite the presence of secretory lysosome-related organelles across ciliate diversity. We discuss potential resolutions for these apparent paradoxes in the context of the heterogenous distribution of MTS machinery across the diversity of ciliates.

跨纤毛虫多样性的膜运输系统组分的分布突出了细胞器相关机制的异质性。
纤毛虫门是一群原生生物,以其不同寻常的膜运输系统和明显的环境普遍性而闻名;作为非常成功的微生物捕食者,它们在各种环境中都有发现,特定物种适应极具挑战性条件的能力使它们被视为生物指标。纤毛虫也被用作细胞生物学模型多年,因为它们的细胞大小大,易于培养,并且对于许多基本的细胞结构,特别是膜结合细胞器,纤毛虫是最早通过显微镜观察到的生物之一。在这项研究中,我们在泛纤毛虫转录组和基因组数据集中对选定的膜运输蛋白进行了比较基因组调查。我们观察到相当大的膜运输系统(MTS)蛋白质的损失,这将表明在真核生物多样性中通常保守的机制的损失,即使在控制潜在的不完整基因组代表之后。特别是,所有被调查的纤毛虫都缺少完整的DSL1复合体。在一些模型系统中,该蛋白复合物已被证明参与过氧化物酶体的生物发生,并且DSL1成分的缺乏表明过氧化物酶体退化。然而,嗜热四膜虫(原焦状四膜虫)是可视化过氧化物酶体的原始模型之一。相反,尽管在纤毛虫多样性中存在与分泌溶酶体相关的细胞器,但嗜热t细胞粘液囊成熟所必需的AP3复合物的保守性很差。我们讨论潜在的解决方案,这些明显的悖论在背景下的异质分布的MTS机械跨越纤毛虫的多样性。
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
Traffic
Traffic 生物-细胞生物学
CiteScore
8.10
自引率
2.20%
发文量
50
审稿时长
2 months
期刊介绍: Traffic encourages and facilitates the publication of papers in any field relating to intracellular transport in health and disease. Traffic papers span disciplines such as developmental biology, neuroscience, innate and adaptive immunity, epithelial cell biology, intracellular pathogens and host-pathogen interactions, among others using any eukaryotic model system. Areas of particular interest include protein, nucleic acid and lipid traffic, molecular motors, intracellular pathogens, intracellular proteolysis, nuclear import and export, cytokinesis and the cell cycle, the interface between signaling and trafficking or localization, protein translocation, the cell biology of adaptive an innate immunity, organelle biogenesis, metabolism, cell polarity and organization, and organelle movement. All aspects of the structural, molecular biology, biochemistry, genetics, morphology, intracellular signaling and relationship to hereditary or infectious diseases will be covered. Manuscripts must provide a clear conceptual or mechanistic advance. The editors will reject papers that require major changes, including addition of significant experimental data or other significant revision. Traffic will consider manuscripts of any length, but encourages authors to limit their papers to 16 typeset pages or less.
×
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