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  • 1 Microbiology Monographs

    Series Editor: Alexander Steinbüchel

  • Inclusions in Prokaryotes

    Volume Editor: Jessup M. Shively

    With 68 Figures, 11 in color


  • Volume Editor:

    Dr. Jessup M. Shively Prof. Emeritus of Biochemistry Department of Genetics and Biochemistry Clemson University Clemson SC 29634 USA e-mail:

    Series Editor:

    Professor Dr. Alexander Steinbüchel Institut für Molekulare Mikrobiologie und Biotechnologie Westfälische Wilhelms-Universität Corrensstraße 3 48149 Münster Germany e-mail:

    Library of Congress Control Number: 2006921109

    ISSN 1862-5576 ISBN-10 3-540-26205-9 Springer Berlin Heidelberg New York ISBN-13 978-3-540-26205-3 Springer Berlin Heidelberg New York DOI 10.1007/11497073

    This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broad- casting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer. Violations are liable for prosecution under the German Copyright Law.

    Springer is a part of Springer Science+Business Media

    c© Springer-Verlag Berlin Heidelberg 2006 Printed in Germany

    The use of registered names, trademarks, 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.

    Editor: Dr. Christina Eckey, Heidelberg Desk Editor: Dr. Jutta Lindenborn, Heidelberg Cover design: eStudio Calamar S.L., Spain Typesetting and Production: LE-TEX Jelonek, Schmidt & Vöckler GbR, Leipzig

    Printed on acid-free paper 149/3100 YL – 5 4 3 2 1 0

  • Preface to the Series

    Microbiology is a still rapidly growing field with impact to a variety of basic and applied areas. The increase in knowledge about microbial physiology, cell structure, biotechnological capabilities and other aspects of microorganisms still continues to increase dramatically despite all the tremendous and fasci- nating achievements made already in the past. The speed by which new knowl- edge is revealed seems even to increase due to the enormous amount of data unravelled by the many microbial genome projects, by new methods and so- phisticated techniques recently developed and by exploring the diversity of mi- croorganisms. The new Springer book series Microbiology Monographs aims to cover hot topics and fields in which considerable progress was made recently. The series will cover topics like inclusions in prokaryotes, predatory prokary- otes, magnetoreception and magnetosomes in bacteria, palaeomicrobiology and past infections, uncultivable microorganisms, microbial endosymbionts, bacterial resistance, extremophilic microorganisms, analyses of genome se- quences and structures, microorganisms as cell factories for chemicals and fuels, metabolic engineering, gene transfer and expression systems or dis- tinct physiological groups of bacteria to mention only a few topics that are in preparation.

    Each volume will focus on a selected microbiological topic. A well known expert in this field, who was invited as volume editor, will carefully compile a team of expert scientists that will contribute about 10 to 15 comprehensive review articles. These articles will cover all relevant aspects of the respective volume and will be carefully refereed. Each year several volumes of Micro- biology Monographs shall be published. It will be an ‘open’ book series, and suggestions from the scientific community for specific topics are highly wel- come.

    Publishing of this new book series would certainly not have been possible without the expertise and engagement of the volume editors and the authors who contributed to a particular volume. I am very grateful to them that they committed their valuable time, knowledge and enthusiasm to this project.

    It has also to be acknowledged that the publisher Springer recognized the demand for this book series, and that the volume could be produced in such high technical quality including colour photographs. Furthermore, publishing all volumes online in addition to the print edition releasing the individual

  • VI Preface to the Series

    chapters Online First before publication of the book, makes the contents of the chapter much more rapidly available to the scientific community. I have in particular to thank Christina Eckey, Jutta Lindenborn and Dieter Czeschlik for their initiative to start this new book series and for their very helpful suggestions and constructive ideas.

    I am very much convinced that the readers of Microbiology Monographswill recognize the joint efforts of all contributors, that they will enjoy reading the books and that they will profit from the compiled knowledge.

    Münster, Germany Alexander Steinbüchel

  • Preface

    In prior coverage of prokaryote inclusions (Pankratz and Bowen 1963; Lang 1968; Shively 1974; Allen 1984; Shively et al. 1988; Jensen 1993; Shively et al. 1998) all of the authors appeared to use a broad definition of “inclusion”, i.e., a discrete, particulate, separate body in the cytoplasm of the prokaryotic cell. As we carefully searched the literature and began considering topics for this volume, it became obvious that in order to stay within an appropriate length, a more restrictive definition of “inclusion” needed to be invoked. This necessity was brought about primarily by two factors, the expansion of the number of “discrete, particulate, separate bodies” described, as well as the apparent wealth of material published on both the earlier and more recently discovered structures in prokaryotes (see material in this Volume as well as Volume 2 of the series Microbiology Monographs).

    Thus, for this volume, we redefined “inclusion” as “a discrete body resulting from synthesis of a metabolic product/reserve.” Further explanation of the definition can be found in Chapter 1 and will become clearer as the reader ex- amines ensuing chapters. Using this new definition, we selected eight topics for chapters: sulfur globules, polyphosphate granules and acidicalcisomes, glyco- gen inclusions, polyhydroxyalkanoate granules, wax ester and triacylglycerol inclusions, cyanophycin inclusions, insecticidal protein crystals, and protein inclusion bodies of recombinant bacteria. Many other, less common inclusions have been reported in a variety of prokaryotes, generally with only limited to moderate research relating to occurrence, structure and function (Pankratz and Bowen 1963; Jensen and Bowen 1970; Shively 1974; Allen 1984; Jensen 1993). It was deemed appropriate to call attention to a few of these inclusions by adding them as cameo chapters in Part 2 of this volume.

    Four of our “primary” inclusions, sulfur, polyphosphate, glycogen, and cyanophycin, were discovered more than 100 years ago. Insecticidal protein crystals were seen in 1915, but their identity was not confirmed until 1953. Although lipid bodies were discovered in 1893, it was not until 1926, 1976, and 1985 that poly(3-hydroxybutyrate), triacylglycerols, and wax esters were firmly established as lipoidal inclusions, respectively. Gene cloning brought about the eventual expression of recombinant proteins, and the first of many inclusions was observed in 1982. Brief descriptions of the inclusions along with the documentation of their discoveries are presented in Chapter 1. Since

  • VIII Preface

    most of the inclusions have been known for such a long period of time many readers are likely to question why we need a review. Has there not already been adequate coverage? To our knowledge, a comprehensive review of all of these inclusions together, in one volume, has never been accomplished. The closest to achieving this would be that of Shively et al. (1974). Having them all together provides the opportunity to compare the structures and the re- search approaches used in their characterization. Also, as noted above, there is still a sizable research interest in the inclusions. This became even more obvious to us when Chapter 1 was developed. Thirty percent of the references used to document inclusion descriptions and discovery were published in or after 1990. The continuing interest in the inclusions is further substantiated if one examines the reference lists of the eight submitted manuscripts; references published in or after 1990 varied from 45–92% (average = 69%), in or after 2000 from 11–41% (average = 31%). What are the driving forces behind this con- tinuing interest? First, the complete characterization of an inclusion including related areas, e.g. biosynthesis and reutilization of the accumulated material(s), is an arduous undertaking. In many cases it is still incomplete. Second, new discoveries relating to an inclusion are not uncommon. As an example, poly(3- hydroybutyrate) was firmly established as a polyhydroxyalkonate (PHA) in 1926; hydroxyvalerate was reported as a constituent in 1974; there are now ap- proximately 150 PHAs, and even a new class of biopolymers related to PHAs, the polythioesters, was recently discovered. There are numerous other exam- ples. Finally, new approaches relating to the potential use of the biopolymers have been developed for many of the biopolymers as well as for their modifi- cation and biosynthesis. We look forward to


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