Jan Löwe Linda A. Amos Editors Filamentous Protein Polymers
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Subcellular Biochemistry 84 Jan Löwe Linda A. Amos Editors Prokaryotic Cytoskeletons Filamentous Protein Polymers Active in the Cytoplasm of Bacterial and Archaeal Cells Subcellular Biochemistry Volume 84 Series editor J. Robin Harris, University of Mainz, Mainz, Germany International advisory editorial board T. Balla, National Institutes of Health, NICHD, Bethesda, USA Tapas K. Kundu, JNCASR, Bangalore, India A. Holzenburg, The University of Texas Rio Grande Valley, Harlingen, USA S. Rottem, The Hebrew University, Jerusalem, Israel X. Wang, Jiangnan University, Wuxi, China The book series SUBCELLULAR BIOCHEMISTRY is a renowned and well recognized forum for disseminating advances of emerging topics in Cell Biology and related subjects. All volumes are edited by established scientists and the individual chapters are written by experts on the relevant topic. The individual chapters of each volume are fully citable and indexed in Medline/Pubmed to ensure maximum visibility of the work. More information about this series at http://www.springer.com/series/6515 Jan Löwe • Linda A. Amos Editors Prokaryotic Cytoskeletons Filamentous Protein Polymers Active in the Cytoplasm of Bacterial and Archaeal Cells Editors Jan Löwe Linda A. Amos Structural Studies Division Structural Studies Division MRC Laboratory of Molecular Biology MRC Laboratory of Molecular Biology Cambridge, UK Cambridge, UK ISSN 0306-0225 Subcellular Biochemistry ISBN 978-3-319-53045-1 ISBN 978-3-319-53047-5 (eBook) DOI 10.1007/978-3-319-53047-5 Library of Congress Control Number: 2017939597 © Springer International Publishing AG 2017 Chapter 3 is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/). For further details see license information in the chapter. This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer International Publishing AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Preface Until the 1990s, it was assumed that the absence of a cytoskeleton, comprised of intracellular dynamic protein filaments that generate long-range order, is a defining characteristic of all archaea and bacteria, distinguishing them from eukaryotic cells. Bacterial DNA was thought to be attached to the cell wall, so that, after replica- tion, a chromosome pair would be segregated by wall extension. Division of the cell into two would then occur by construction of a new central partition. Plasmids, small pieces of DNA and other molecular entities such as protein complexes were thought to travel through prokaryotic cells without guidance, through diffusion. These views began to break down when FtsZ protein was found to locate, as a ringlike filamentous structure, at the cell division site, and this widely distributed protein was shown to be a homologue of eukaryotic tubulin. The absence of a cyto- skeleton in archaea and bacteria was finally abandoned in 2003, when other bacte- rial proteins, already known to have amino acid sequence homology to eukaryotic actin, were shown to form intracellular filaments with similarity to F-actin. Soon after that, bacterial plasmid systems were discovered that used actin-like or tubulin- like protein filaments to effect segregation. Since then, many other types of filament have been discovered; some are unique to prokaryotes, in a surprising variety of biological contexts, but many are related to eukaryotic cytoskeletal filaments. With important discoveries being made in archaea as well as bacteria, the field has expanded enormously to warrant the dedication of a whole book to known pro- karyotic filament structures, together with current theories and controversies regard- ing the mechanisms by which the filaments carry out their diverse functions, that go well beyond what similarities with eukaryotic homologues would suggest. What has emerged, in particular, is that prokaryotes lack the motor proteins asso- ciated with eukaryotic cytoskeletal filaments and that intracellular motility often depends on the activity and dynamics of the filaments themselves. As described in the various chapters of the book, these cytomotive filaments have been found to exhibit treadmilling, dynamic instability and relative sliding. In other words, our view of a bacterium has undergone a truly remarkable revolution. Cambridge, UK Jan Löwe Linda A. Amos v Contents 1 Overview of the Diverse Roles of Bacterial and Archaeal Cytoskeletons ................................................................... 1 Linda A. Amos and Jan Löwe 2 E. coli Cell Cycle Machinery .................................................................. 27 Joe Lutkenhaus and Shishen Du 3 Cell Cycle Machinery in Bacillus subtilis .............................................. 67 Jeff Errington and Ling Juan Wu 4 Cytoskeletal Proteins in Caulobacter crescentus: Spatial Orchestrators of Cell Cycle Progression, Development, and Cell Shape ................................................................ 103 Kousik Sundararajan and Erin D. Goley 5 FtsZ Constriction Force – Curved Protofilaments Bending Membranes ............................................................................... 139 Harold P. Erickson and Masaki Osawa 6 Intermediate Filaments Supporting Cell Shape and Growth in Bacteria .......................................................................... 161 Gabriella H. Kelemen 7 FtsZ-ring Architecture and Its Control by MinCD ............................. 213 Piotr Szwedziak and Debnath Ghosal 8 Bacterial Actins ....................................................................................... 245 Izoré and Fusinita van den Ent 9 Bacterial Nucleoid Occlusion: Multiple Mechanisms for Preventing Chromosome Bisection During Cell Division .............. 267 Maria A. Schumacher vii viii Contents 10 Structure and Dynamics of Actin-Like Cytomotive Filaments in Plasmid Segregation ......................................................... 299 Pananghat Gayathri and Shrikant Harne 11 Tubulin-Like Proteins in Prokaryotic DNA Positioning ...................... 323 Gero Fink and Christopher H.S. Aylett 12 The Structure, Function and Roles of the Archaeal ESCRT Apparatus .................................................................................. 357 Rachel Y. Samson, Megan J. Dobro, Grant J. Jensen, and Stephen D. Bell 13 Archaeal Actin-Family Filament Systems ............................................. 379 Ann-Christin Lindås, Karin Valegård, and Thijs J.G. Ettema 14 The Tubulin Superfamily in Archaea .................................................... 393 Christopher H.S. Aylett and Iain G. Duggin 15 Reconstitution of Protein Dynamics Involved in Bacterial Cell Division ........................................................................ 419 Martin Loose, Katja Zieske, and Petra Schwille Index ................................................................................................................. 445 About the Editors Jan Löwe gained his PhD in 1996 at the Max Planck Institute of Biochemistry, Martinsried, with Robert Huber, having helped to solve the crystal structures of large protein complexes known as proteasomes and thermosomes. He then moved to Cambridge to work in LAA’s group at MRC-LMB, where he solved the structure of FtsZ, a bacterial tubulin homologue. In 1998, he set up his own group at MRC- LMB and began working on the structures and functions of a wide range of bacterial proteins involved in cell division and organisation. In particular, he has investigated the prokaryotic actin-related proteins, as well as a range of tubulin-related filaments. In addition to X-ray crystallography, his group uses electron microscopy and elec- tron cryo-tomography to determine the structures of bacterial cytoskeletal filaments, together with light microscopy to follow their activity. He is a fellow of the Royal Society (London), a member of EMBO and a fellow of Leopoldina (German National Academy of Sciences). In 2010, he was promoted to be joint head of the Structural Studies Division of MRC-LMB in Cambridge, and in 2016, he became deputy director of the entire institute. http://scholar.google.co.uk/citations?user=0XTmVmoAAAAJ&hl=en http://orcid.org/0000-0002-5218-6615 Linda A. Amos began working