MamF样蛋白是参与细菌细胞器组装的遥远Tic20同源物-动脉网

MamF-like proteins are distant Tic20 homologs involved in organelle assembly in bacteria

Nature 等信源发布 2024-12-09 21:50

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AbstractOrganelle-specific protein translocation systems are essential for organelle biogenesis and maintenance in eukaryotes but thought to be absent from prokaryotic organelles. Here, we demonstrate that MamF-like proteins are crucial for the formation and functionality of bacterial magnetosome organelles.

摘要细胞器特异性蛋白质易位系统对于真核生物中细胞器的生物发生和维持至关重要，但被认为在原核细胞器中不存在。在这里，我们证明了MamF样蛋白对于细菌磁小体细胞器的形成和功能至关重要。

Deletion of mamF-like genes in the Alphaproteobacterium Magnetospirillum gryphiswaldense results in severe defects in organelle positioning, biomineralization, and magnetic navigation. These phenotypic defects result from the disrupted targeting of a subset of magnetosomal proteins that contain C-terminal glycine-rich integral membrane domains.

在Alphaproteobacterium Magnetospirillum gryphiswaldense中删除mamF样基因会导致细胞器定位，生物矿化和磁导航方面的严重缺陷。这些表型缺陷是由于含有富含C端甘氨酸的整合膜结构域的磁小体蛋白子集的靶向被破坏所致。

Phylogenetic analyses reveal an ancient evolutionary link between MamF-like proteins and plastidial Tic20. Our findings redefine the molecular roles of MamF-like proteins and suggest that organelle-specific protein targeting systems also play a role in bacterial organelle formation..

系统发育分析揭示了MamF样蛋白与质体Tic20之间的古老进化联系。我们的发现重新定义了MamF样蛋白的分子作用，并表明细胞器特异性蛋白靶向系统也在细菌细胞器形成中起作用。。

IntroductionEukaryotes possess complex preprotein translocases of chloroplasts or mitochondria (Tic/Toc or Tim/Tom) to ensure biogenesis and maintenance of these organelles. Strikingly, both translocases have a mixed phylogenetic origin and likely evolved by combining new eukaryotic proteins with bacterial subunits of endosymbiotic origin1,2,3,4.

引言真核生物具有复杂的叶绿体或线粒体前蛋白转位酶（Tic/Toc或Tim/Tom），以确保这些细胞器的生物发生和维持。引人注目的是，这两种转位酶都具有混合的系统发育起源，并且可能通过将新的真核蛋白与内共生起源的细菌亚基1,2,3,4结合而进化。

However, no organelle-specific protein translocases equivalent to the eukaryotic machineries have been identified among bacteria yet5. Hence, bacterial organelle biogenesis must proceed through distinct mechanisms.Magnetosomes, unique magnetic organelles6, for example, emerge from the cell membrane by invagination7.

然而，在细菌yet5中没有发现与真核机器相当的细胞器特异性蛋白质转位酶。因此，细菌细胞器的生物发生必须通过不同的机制进行。例如，磁小体，独特的磁性细胞器6，通过内陷从细胞膜中出现7。

It has been hypothesized that in Magnetospirillum gryphiswaldense MSR-1 and related Alphaproteobacteria, this process is induced by the assembly of magnetosome-specific protein complexes within the cytoplasmic membrane that initiate magnetosome membrane (MM) formation through a molecular crowding-like membrane-bending mechanism8.

据推测，在Magnetospirillum gryphiswaldense MSR-1和相关的Alphaproteobacteria中，这一过程是由细胞质膜内磁小体特异性蛋白复合物的组装诱导的，该复合物通过分子拥挤样膜弯曲机制启动磁小体膜（MM）形成8。

Thereby, magnetosome-specific proteins, which are encoded within a compact genomic magnetosome island (MAI), supposedly become integrated into the MM during its invagination. Some magnetosome proteins, however, follow different targeting routes. Mms6 and MamD (also known as Mms7), for example, are translocated into preexisting magnetosomes in a folded state upon induction of magnetite biomineralization9,10.

因此，在紧凑的基因组磁小体岛（MAI）中编码的磁小体特异性蛋白在其内陷过程中被整合到MM中。然而，一些磁小体蛋白遵循不同的靶向途径。例如，Mms6和MamD（也称为Mms7）在诱导磁铁矿生物矿化后以折叠状态转移到先前存在的磁小体中9,10。

Nevertheless, the precise molecular mechanisms governing magnetosome assembly and protein targeting remained largely elusive.Immediately following MM formation, the embedded magnetosome proteins facilitate subsequent steps of magnetosome biogenesis like iron uptake into the magnetosome lumen, initiation of magnetite (Fe3O4) biomineralization and magnetite crystal growth11.

然而，控制磁小体组装和蛋白质靶向的精确分子机制仍然难以捉摸。在MM形成后，嵌入的磁小体蛋白立即促进磁小体生物发生的后续步骤，如铁吸收到磁小体腔中，开始磁铁矿（Fe3O4）生物矿化和磁铁矿晶体生长11。

The small inte.

小inte。

Data availability

数据可用性

All data supporting the findings of this study are included in the main text, the supplementary materials or the supplementary data files. Uncropped versions of blots/gels, swim halos in agar plates and bacterial two-hybrid assay agar plates are supplied in the Source data file provided with this paper.

支持本研究结果的所有数据均包含在正文，补充材料或补充数据文件中。本文提供的源数据文件中提供了未裁剪版本的印迹/凝胶，琼脂平板中的游泳晕和细菌双杂交测定琼脂平板。

The mass spectrometry proteomics data generated in this study have been deposited to the ProteomeXchange (http://proteomecentral.proteomexchange.org) consortium via the PRIDE partner repository70 under the accession code PXD032959. The accession codes of structures and AlphaFold models used for analysis are 7XZI (Tic20); AF-A4U547-F1-model_v2 (MmsF, accession date 18.03.2022). Source data are provided with this paper..

这项研究中产生的质谱蛋白质组学数据已保存到ProteomeXchange(http://proteomecentral.proteomexchange.org)财团通过PRIDE partner repository70，登录号为PXD032959。用于分析的结构和AlphaFold模型的登录号是7XZI（Tic20）；AF-A4U547-F1-model\u v2（MmsF，加入日期为2022年3月18日）。本文提供了源数据。。

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Download referencesAcknowledgementsWe would like to thank Gabriele Zaus and Ulrike Brandauer for technical assistance as well as Stephanie Bauer and Michael Gass for help during immunoblot analysis, two-hybrid assays, strain, and plasmid construction. The authors are grateful for financial support by the German Research Foundation (DFG, grants UE200/1-1 and INST 91/374-1 LAGG) (RU) and the Federal Ministry of Education and Research (BMBF, grant MagBioFab) (RU).FundingOpen Access funding enabled and organized by Projekt DEAL.Author informationAuthors and AffiliationsDepartment of Microbiology, University of Bayreuth, Bayreuth, GermanyAnja Paulus, Frederik Ahrens, Annika Schraut, Hannah Hofmann, Tim Schiller & René UebeMicrobial Proteomics, Institute of Microbiology, University of Greifswald, Greifswald, GermanyThomas Sura & Dörte BecherAuthorsAnja PaulusView author publicationsYou can also search for this author in.

下载参考文献致谢我们要感谢Gabriele Zaus和Ulrike Brandauer的技术援助，以及Stephanie Bauer和Michael Gass在免疫印迹分析，双杂交分析，菌株和质粒构建过程中的帮助。作者感谢德国研究基金会（DFG，grants UE200/1-1和INST 91/374-1 LAGG）（RU）和联邦教育与研究部（BMBF，grant MagBioFab）（RU）的财政支持。资金开放获取资金由Projekt交易启用和组织。作者信息作者和所属机构Bayreuth大学微生物学系，Bayreuth，GermanyAnja Paulus，Frederik Ahrens，Annika Schraut，Hannah Hofmann，Tim Schiller＆RenéUebeMicrobial Proteomics，Greifswald大学微生物学研究所，Greifswald，GermanyThomas Sura＆Dörte BecherAuthorsAnja PaulusView作者出版物您也可以在中搜索这位作者。

PubMed Google ScholarFrederik AhrensView author publicationsYou can also search for this author in

PubMed谷歌学者Frederik AhrensView作者出版物您也可以在

PubMed Google ScholarAnnika SchrautView author publicationsYou can also search for this author in

PubMed Google ScholarAnnika SchrautView作者出版物您也可以在

PubMed Google ScholarHannah HofmannView author publicationsYou can also search for this author in

PubMed Google ScholarHannah HofmannView作者出版物您也可以在

PubMed Google ScholarTim SchillerView author publicationsYou can also search for this author in

PubMed Google ScholarTim SchillerView作者出版物您也可以在

PubMed Google ScholarThomas SuraView author publicationsYou can also search for this author in

PubMed Google ScholarThomas SuraView作者出版物您也可以在

PubMed Google ScholarDörte BecherView author publicationsYou can also search for this author in

PubMed Google ScholarDörte BecherView作者出版物您也可以在

PubMed Google ScholarRené UebeView author publicationsYou can also search for this author in

PubMed Google ScholarRenéUebeView作者出版物您也可以在

PubMed Google ScholarContributionsConceptualization and methodology: RU. Investigation: AP, FA, AS, TSc, HH and RU (conducted the biochemical and cell biological studies), TSu and DB (performed MS proteomics and analyzed MS data). Formal analysis: RU. Funding acquisition: RU.

PubMed谷歌学术贡献概念和方法：RU。调查：AP，FA，AS，TSc，HH和RU（进行了生化和细胞生物学研究），TSu和DB（进行了MS蛋白质组学和MS数据分析）。正式分析：RU。资金获取：RU。

Supervision: RU. Writing - Original draft: AP and RU. Writing - Review & editing: all authors.Corresponding authorCorrespondence to.

监督：RU。写作-原稿：AP和RU。写作-评论和编辑：所有作者。对应作者对应。

René Uebe.Ethics declarations

勒内·尤贝。道德宣言

Competing interests

相互竞争的利益

The authors declare no competing interests.

作者声明没有利益冲突。

Peer review

同行评审

Peer review information

同行评审信息

Nature Communications thanks Juan Wan and the other, anonymous, reviewers for their contribution to the peer review of this work. A peer review file is available.

Nature Communications感谢Juan Wan和其他匿名审稿人对这项工作的同行评审做出的贡献。同行评审文件可用。

Additional informationPublisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.Supplementary informationSupplementary InformationDescription of Additional Supplementary FilesSupplementary Data 1Supplementary Data 2Supplementary Data 3Supplementary Data 4Supplementary Data 5Reporting SummaryPeer Review fileSource dataSource DataRights and permissions.

Additional informationPublisher的注释Springer Nature在已发布地图和机构隶属关系中的管辖权主张方面保持中立。补充信息补充信息其他补充文件的描述补充数据1补充数据2补充数据3补充数据4补充数据5报告摘要同行评审文件源数据源数据权限。

Open Access This 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.

开放获取本文是根据知识共享署名4.0国际许可证授权的，该许可证允许以任何媒体或格式使用，共享，改编，分发和复制，只要您对原始作者和来源给予适当的信任，提供知识共享许可证的链接，并指出是否进行了更改。

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.

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Reprints and permissionsAbout this articleCite this articlePaulus, A., Ahrens, F., Schraut, A. et al. MamF-like proteins are distant Tic20 homologs involved in organelle assembly in bacteria.

转载和许可本文引用本文Paulus，A.，Ahrens，F.，Schraut，A。等人。MamF样蛋白是参与细菌细胞器组装的远距离Tic20同源物。

Nat Commun 15, 10657 (2024). https://doi.org/10.1038/s41467-024-55121-0Download citationReceived: 11 April 2024Accepted: 26 November 2024Published: 09 December 2024DOI: https://doi.org/10.1038/s41467-024-55121-0Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

Nat Commun 1510657（2024）。https://doi.org/10.1038/s41467-024-55121-0Download引文收到日期：2024年4月11日接受日期：2024年11月26日发布日期：2024年12月9日OI：https://doi.org/10.1038/s41467-024-55121-0Share本文与您共享以下链接的任何人都可以阅读此内容：获取可共享链接对不起，本文目前没有可共享的链接。复制到剪贴板。

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