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Planctomycetes and Methanotrophic Verrucomicrobia PDF hosted at the Radboud Repository of the Radboud University Nijmegen The following full text is a publisher's version. For additional information about this publication click this link. http://hdl.handle.net/2066/149508 Please be advised that this information was generated on 2021-10-08 and may be subject to change. Cell biology of anammox Planctomycetes and methanotrophic Verrucomicrobia The cell envelope of anammox Planctomycetes Muriel van Teeseling Cell biology of anammox Planctomycetes and methanotrophic Verrucomicrobia Part i The cell envelope of anammox Planctomycetes Muriel van Teeseling Muriel van Teeseling (2015) Cell biology of anammox Planctomycetes and methanotrophic Verrucomicrobia. PhD thesis, Radboud University Nijmegen. This PhD project was financially supported by ERC AG 232937. Printing of this thesis was financially supported by SIAM gravitation grant 024002002 and by the Netherlands Society of Medical Microbiology (NVMM) and the Royal Netherlands Society for Microbiology (KNVM). Cover: Freeze‐fractured Methylacidimicrobium fagopyrum cell by Muriel van Teeseling. Print: Gildeprint Drukkerijen, Enschede, the Netherlands. ISBN: 978‐94‐6233‐163‐1. Cell biology of anammox Planctomycetes and methanotrophic Verrucomicrobia Proefschrift ter verkrijging van de graad van doctor aan de Radboud Universiteit Nijmegen op gezag van de rector magnificus, volgens besluit van het college van decanen in het openbaar te verdedigen op woensdag 13 januari 2016 om 14.30 uur precies door Muriël Caroline Frieda van Teeseling geboren op 25 december 1986 te Naarden Promotor Prof. dr. ir. M.S.M. Jetten Copromotor dr. L. van Niftrik Manuscriptcommissie Prof. dr. C. Mariani Prof. dr. W. Bitter (Vrije Universiteit Amsterdam) Prof. dr. S‐V. Albers (Albert‐Ludwigs‐Universität Freiburg, Duitsland) Contents Summary 3 (i) Samenvatting 5 (i) Chapter 1 General introduction 9 (i) Chapter 2 A new addition to the cell plan of anammox bacteria: 25 (i) Kuenenia stuttgartiensis has a protein surface layer (S‐layer) as outermost layer of the cell Chapter 3 The abundant protein Kustd1878 of the anammox 49 (i) Planctomycete Kuenenia stuttgartiensis is a pore‐forming outer membrane protein Chapter 4 Lipopolysaccharides in Planctomycetes: present or absent? 67 (i) Chapter 5 Anammox Planctomycetes have a peptidoglycan cell wall 89 (i) Chapter 6 Integration and Outlook 103 (i) References 121 (i) Acknowledgements 147 (i) Curriculum vitae 153 (i) Publication list 154 (i) 1 (i) 2 (i) Summary Anammox bacteria perform anaerobic ammonium oxidation and play an important role in the biological nitrogen cycle. They are applied to efficiently remove ammonium and nitrite from wastewater via a biochemically highly interesting mechanism involving hydrazine as intermediate and dinitrogen gas as end product. Anammox bacteria are also of particular interest to cell biologists. They belong to the Planctomycetes, a phylum characterized by a unique cell organization. Most Planctomycetes have two compartments, of which the innermost was interpreted as an intracytoplasmic compartment. Anammox bacteria have a third compartment that acts as a prokaryotic organelle in which the anammox reaction takes place. The anammox cell thus consists of the following compartments (from the outside inwards): the paryphoplasm, the riboplasm and the anammoxosome. An interesting aspect of all Planctomycetes is the cell envelope, which was proposed to lack peptidoglycan and an outer membrane. This is striking since almost all bacteria contain peptidoglycan in their cell envelope. Furthermore all bacteria classified as Gram‐negative additionally contain an outer membrane surrounding the peptidoglycan layer. Especially for anammox bacteria, many questions about the cell envelope remain, such as: Which components does the cell envelope contain? What are the characteristics of the outermost membrane (previously defined as a cytoplasmic membrane)? The research presented in this part of the thesis therefore aims to elucidate which components constitute the cell envelope of the model anammox species Kuenenia stuttgartiensis. With the new results we were able to answer the question if, as was postulated, this organism truly forms an exception to the Gram‐negative cell plan. Chapter 1 provides an introduction into bacterial cell (envelope) organization, (anammox) Planctomycetes and their cell biology. The results of chapter 2 show that a new layer was discovered as the outermost structure of the K. stuttgartiensis cell. This so‐called surface layer (S‐layer) consists of proteins and forms a symmetrical pattern. The S‐layer was characterized via freeze‐etching followed by transmission electron microscopy (TEM). Enrichment of this S‐layer led to the identification of the glycoprotein that builds this structure: Kustd1514. Two main glycan components were retrieved from Kustd1514 and their composition was elucidated via mass spectrometry coupled to liquid chromatography in combination with monosaccharide analysis. Immunogold localization using an antibody generated against Kustd1514 verified that this protein indeed forms the observed S‐layer. To investigate if the outermost membrane has characteristics of an outer membrane, most notably lipopolysaccharide (LPS) as specific lipids and outer membrane proteins (OMPs) as specific proteins, chapter 3 and chapter 4 describe in‐depth investigations of this membrane. The purification and characterization of a specific OMP, Kustd1878, are described in chapter 3. The structure of Kustd1878 was investigated via bioinformatics, suggesting the protein has an OMP‐specific ß‐barrel structure. Pore‐forming function, a typical characteristic of OMPs, was verified by membrane bilayer assays. Immunogold localization using an antibody generated against the purified protein furthermore suggested the presence of this protein in the outermost membrane of K. stuttgartiensis that can best be described as an outer membrane. 3 (i) Chapter 4 aims at elucidating if LPS, the main component of the outer leaflet of outer membranes, is present in K. stuttgartiensis and the two non‐anammox Planctomycetes Planctopirus limnophila and Rhodopirellula baltica. Genes necessary for the synthesis of lipid A, the part of the LPS that is anchored in the membrane, were identified in the genome of all three species and in the transcriptome of K. stuttgartiensis. Gel electrophoresis indicated the presence of LPS in all three species and polymyxin B, an antibiotic that disrupts the outer membrane upon binding to LPS, caused disruption of the membranes of R. baltica and to a lesser extent of K. stuttgartiensis and P. limnophila. However, the LPS components KDO and lipid A were not detected in K. stuttgartiensis via mass spectrometry methods. Therefore, the presence of LPS in the three Planctomycetes species seems plausible, but additional experiments are needed for further verification. In chapter 5 the proposed absence of peptidoglycan in anammox bacteria was revisited. Cryo‐TEM of vitreous sections identified a layer in between the cytoplasmic and outermost membrane in K. stuttgartiensis. When using a peptidoglycan isolation protocol, characteristic sacculi were observed. These sacculi disintegrated upon treatment with lysozyme, an agent that cleaves the sugar backbone of peptidoglycan. In addition, the presence of peptidoglycan was demonstrated in growing cultures by fluorescent probes that are built in during peptidoglycan synthesis. The presence of peptidoglycan in K. stuttgartiensis was ultimately proven when muropeptide analysis showed the composition of the sacculi to be typical for Gram‐negative peptidoglycan. Based on the results of the previous chapters, chapter 6 reaches the conclusion that (anammox) Planctomycetes can best be interpreted as Gram‐negative bacteria. This chapter furthermore gives an overview of the cell envelope of anammox bacteria, and describes key questions and associated hypotheses and experiments in order to come to a thorough understanding of the cell biology of (anammox) Planctomycetes. 4 (i) Samenvatting Anammoxbacteriën voeren anaërobe ammonium‐oxidatie uit en spelen een belangrijke rol in de biologische stikstofcyclus. Ze worden toegepast om op efficiënte wijze ammonium en nitriet uit afvalwater te verwijderen via een biochemisch zeer interessant mechanisme met hydrazine als tussenproduct en stikstofgas als eindproduct. Anammoxbacteriën zijn daarnaast bijzonder interessant voor celbiologen. Ze behoren tot de Planctomyceten, een phylum dat door een unieke celorganisatie gekarakteriseerd wordt. De meeste Planctomyceten hebben twee compartimenten waarvan de binnenste werd beschouwd als een intracytoplasmatisch compartiment. Anammoxbacteriën hebben daarnaast een derde compartiment dat functioneert als prokaryoot organel waarin de anammoxreactie plaatsvindt. Anammoxbacteriën bestaan dus uit de volgende compartimenten (van buiten naar binnen): het paryphoplasma, het riboplasma en het anammoxosoom. Een interessant aspect van alle Planctomyceten is de celenvelop, waarvan men aannam dat hierin zowel peptidoglycaan als een buitenmembraan ontbrak. Dit is opvallend aangezien bijna alle bacteriën peptidoglycaan bevatten in hun celenvelop. Daarnaast hebben alle bacteriën die als Gram‐negatief worden geklassificeerd een peptidoglycaan omringende buitenmembraan. In het bijzonder voor anammoxbacteriën zijn er nog veel open vragen over de celenvelop, zoals: Uit welke componenten bestaat de celenvelop? Wat zijn de karakteristieken van de buitenste membraan (dat voorheen als cytoplasmatisch
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