Microbial BioEnergy: Production

Different Ways for Production The four possible ways for producing H2 , by exploiting microbial activities, are shown here. Biophotolysis : H 2 production by microalgae (through H 2-ase) or

(through H 2-ase or N 2-ase) by using low potential reductants derived from either water or stored sugars via the photosynthetic machinery. Photofermentation : H2 production by anoxygenic photosynthetic (through

N 2 -ase) by using reductants obtained from the oxidation of organic compounds as well as solar energy used through . Dark : H2 production by mesophilic or thermophilic chemoheterotrophic bacteria (through H 2-ase) by using reductants and energy obtained from the oxidation of organic compounds.

Microbial Electrolysis Cell (MEC): H2 production by means of cathodic proton reduction with applied potential exploiting the low redox potential produced by exoelectrogenic bacteria at the anode. This fi gure is adapted from Fig. 1.3 in Chap. 1 of this book. Advances in Photosynthesis and Respiration Including Bioenergy and Related Processes

VOLUME 38

Series Editors: GOVINDJEE* ( University of Illinois at Urbana- Champaign, IL , U.S.A )

THOMAS D. SHARKEY ( Michigan State University, East Lansing , MI , U.S.A ) * Founding Series Editor

Advisory Editors: Elizabeth AINSWORTH, United States Department of Agriculture, Urbana , IL , U.S.A. Basanti BISWAL, Sambalpur University , Jyoti Vihar , Odisha , India Robert E. BLANKENSHIP, Washington University, St Louis, MO , U.S.A. Ralph BOCK, Max Planck Institute of Molecular Plant Physiology , Postdam - Golm, Germany Julian J. EATON-RYE, University of Otago, Dunedin, New Zealand Wayne FRASCH, Arizona State University, Tempe , AZ , U.S.A. Johannes MESSINGER, Umeå University, Umeå , Sweden Masahiro SUGIURA, Nagoya City University, Nagoya, Japan Davide ZANNONI, University of Bologna, Bologna , Italy Lixin ZHANG, Institute of Botany , Beijing, China

The book series A DVANCES IN PHOTOSYNTHESIS AND RESPIRATION Including Bioenergy and Related Processes provides a comprehensive and state-of-the-art account of research in photosynthesis, respiration and related processes. Virtually all life on our planet Earth ultimately depends on photosynthetic energy capture and conversion to energy- rich organic molecules. These are used for food, fuel, and fi ber. Photosynthesis is the source of almost all bioenergy on Earth. The fuel and energy uses of photosynthesized products and processes have become an important area of study, and competition between food and fuel has led to resurgence in photosynthesis research. This series of books spans topics from physics to agronomy and medicine; from femtosecond processes through season-long production to evolutionary changes over the course of the history of the Earth; from the photophysics of light absorption, excitation energy transfer in the antenna to the reaction centers, where the highly-efficient primary conversion of light energy to charge separation occurs, through the electrochemistry of intermediate electron transfer, to the physiology of whole organisms and ecosystems; and from X-ray crystallography of proteins to the morphology of organelles and intact organisms. In addition to photosynthesis in natural systems, genetic engineering of photosynthesis and artifi cial photosynthesis is included in this series. The goal of the series is to offer beginning researchers, advanced undergraduate students, graduate students, and even research specialists, a comprehensive, up-to-date picture of the remarkable advances across the full scope of research on photosynthesis and related energy processes. The purpose of this series is to improve understanding of photosynthesis and respiration at many levels both to improve basic understanding of these important processes and to enhance our ability to use photosynthesis for the improvement of the human condition.

For further volumes: www.springer.com/series/5599 Microbial BioEnergy:

Edited by Davide Zannoni University of Bologna Bologna Italy

and Roberto De Philippis University of Florence Florence Italy Editors Davide Zannoni Roberto De Philippis Department of Pharmacy Department of AgriFood Production and BioTechnology (FaBiT) and Environmental Sciences University of Bologna University of Florence Bologna , Italy Florence , Italy [email protected] Institute of Chemistry of Organometallic Compounds (ICCOM), CNR, Sesto Fiorentino, Florence, Italy roberto.dephilippis@unifi .it

ISSN 1572-0233 ISSN 2215-0102 (electronic) ISBN 978-94-017-8553-2 ISBN 978-94-017-8554-9 (eBook) DOI 10.1007/978-94-017-8554-9 Springer Dordrecht Heidelberg New York London

Library of Congress Control Number: 2014932831

© Springer Science+Business Media Dordrecht 2014 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifi cally the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfi lms 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. Exempted from this legal reservation are brief excerpts in connection with reviews or scholarly analysis or material supplied specifi cally for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Duplication of this publication or parts thereof is permitted only under the provisions of the Copyright Law of the Publisher’s location, in its current version, and permission for use must always be obtained from Springer. Permissions for use may be obtained through RightsLink at the Copyright Clearance Center. Violations are liable to prosecution under the respective Copyright Law. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specifi c statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. While the advice and information in this book are believed to be true and accurate at the date of publication, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein.

Printed on acid-free paper

Springer is part of Springer Science+Business Media (www.springer.com) This book is dedicated to the memory of

Hans Gaffron (1902–1979) and Howard Gest (1921–2012) pioneers of the microbial based hydrogen gas production

From the Series Editors

Advances in Photosynthesis and Respiration Including Bioenergy and Related Processes Volume 38: Microbial BioEnergy: Hydrogen Production

W e are delighted to announce the publication Professor of General Microbiology, at the of volume 38 in this series. The title of our University of Bologna, Italy; he is an autho- series Advances in Photosynthesis and rity on the structure and the function of Respiration was already updated in volume membrane redox-complexes in microbes, 35 to include the subtitle: Including and a pioneer of bioenergetics and genomics Bioenergy and Related Processes . Earlier, of microbial remediation of metals in many the front cover of each volume had a distinc- systems. More importantly, his present focus tive white background and color palette; is on the production of hydrogen by thermo- from volume 35, it has been changed to a philic bacteria and electricity from microbial web-friendly green background; and each systems. De Philippis is an Associate volume begins with a unique fi gure, repre- Professor of Microbial Biotechnology at the senting the book. Further, the publisher, University of Florence, Italy. He is an authority Springer, makes the front matter of all of the on exopolysaccharide-producing cyanobac- volumes freely available online. Links to teria and their biotechnological exploitation each volume are given under “Our Books: and, more importantly, in the last 15 years he Published Volumes.” Readers may also has been deeply involved in studies on the notice that this volume and the past few vol- photofermentative production of hydrogen umes have had color fi gures integrated into indoors and outdoors and on the effi cient con- the chapters, instead of being collected in version of light energy into hydrogen energy. one section of the book. This improvement was possible because of changes in how the books are produced. Another change is that This Book: Volume 38 references to chapters in books are now being tracked by bibliographic services. This Microbial BioEnergy: Hydrogen Production will help authors provide evidence of the is a comprehensive book covering most of importance of their work. We hope that these the processes important for the microbial updates will maintain the importance of hydrogen production. It provides a broad these edited volumes in the dissemination of coverage of this emerging research fi eld and, the science of photosynthesis and bioenergy. in our opinion, it should be accessible to We are delighted to announce that volume advanced undergraduates, graduate students, 38 is the fi rst one to deal with the new and researchers needing to broaden their direction “Including Bioenergy and Related knowledge on the photosynthetic and fer- Processes.” We are indeed fortunate to have mentation processes applied to hydrogen gas two distinguished authorities with us as edi- generation. For biologists, biochemists, bio- tors of this new volume 38: Davide Zannoni, physicists and microbiologists, this volume and Roberto De Philippis. Zannoni is a provides a solid and quick starting base to

vii viii get into biotechnological problems of Turkey, USA). We give special thanks to “microbial bioenergy.” We believe that this each and every author for their valuable con- volume will also be of interest to teachers tribution to the successful production of this of advanced undergraduate and graduate unique book: students in chemical engineering and bio- Francisco Gabriel A cién-Fernández technology needing a single reference book (Spain; Chap. 13 ); Alessandra Adessi (Italy; on the latest understanding of the critical Chap. 12 ); Giacomo Antonioni (Italy; Chap. 15 ); aspects of microbial bioenergy production. Sara E. Blumer-Schuette (USA; Chap. 8 ); The Preface of this book appropriately Hermann Bothe (Germany; Chap. 6 ); states “Solar energy is the source of most of Martina C appelletti (Italy; Chap. 9 ); the living organisms on Earth so that the Jonathan M. Conway (USA; Chap. 8 ); overall effi ciency of oxygenic and/or non- Roberto D e Philippis (Italy; Chap. 12 ); oxygenic photosynthesis, when used to gen- Alexandra Dubini (USA; Chap. 5 ); Carrie erate biomass, bioenergy and biofuels, is a Eckert (USA; Chap. 5); Ela Eroglu critical point to be considered.” This volume (Australia; Chap. 11); Inci Eroglu (Turkey; in our series, however, not only provides a Chap. 11); José M. F ernández-Sevilla comprehensive view of the current under- (Spain; Chap. 13); Juan C. Fontecilla-Camps standing of the photosynthetic mechanisms (France; Chap. 2 ); Dario Frascari (Italy; linked to bio-hydrogen production but also Chap. 15 ); Maria L. G hirardi (USA; Chap. 5 ); extends this view to the anaerobic-dark Ufuk Gündüz (Turkey; Chap. 11 ); Patrick processes involved in transforming the C. H allenbeck (Canada; Chap. 1 ); Robert solar-generated biomass into bio-hydrogen M. K elly (USA; Chap. 8 ); Paul W. King (USA; along with an in-depth coverage of both Chap. 5 ); Sergey Kosourov (Russia; Chap. 14 ); structural and functional aspects of the main Pierre-Pol L iebgott (France; Chap. 3 ); enzymes involved, such as nitrogenases and Pin-Ching M aness (USA; Chap. 5 ); James hydrogenases . B. McKinlay (USA; Chap. 7 ); Emilio In our opinion, this book has been appro- Molina-Grima (Spain; Chap. 13 ); David priately dedicated to Hans Gaffron (1902– W. Mulder (USA; Chap. 5 ); William E. Newton 1979) and Howard Gest (1921–2012), (USA; Chap. 6 ); Paulo O liveira (Portugal; founders of the microbial based hydrogen Chap. 4 ); Bernard Ollivier (France; Chap. 9 ); gas production technologies. One of us Ebru Özgür (Turkey; Chap. 11 ); Catarina (Govindjee) is fortunate to have known per- C. P acheco (Portugal; Chap. 4 ); Anne Postec sonally both these giants of photosynthesis (France; Chap. 9 ); John M. R egan (USA; research. Among the various other discover- Chap. 10 ); Marc Rousset (France; Chap. 3 ); ies, Gaffron was the fi rst to observe, in 1942, Paula T amagnini (Portugal; Chap. 4 ); hydrogen production by green under Anatoly Tsygankov (Russia; Chap. 14 ); sulfur starvation, while Gest was the fi rst to Anne Volbeda (France; Chap. 2 ); Hengjing describe, in 1949, hydrogen-production by Y an (USA; Chap. 10 ); Jianping Yu (USA; purple non-sulfur phototrophic bacteria (See Chap. 5 ); Meral Yücel (Turkey; Chap. 11 ); below for information on “Discoveries in Davide Z annoni (Italy; Chap. 9 ); Jeffrey Photosynthesis” volume 20, in our series, V. Zurawski (USA; Chap. 8 ). where these discoveries are described).

Our Books: Published Volumes Authors We list below information on all the 37 vol- The current book contains 15 chapters writ- umes that have been published thus far (see ten by 42 international authors from 10 dif- http://www.springer.com/series/5599 for the ferent countries (Australia, Canada, France, web site of the series). Electronic access to Germany, Italy, Portugal, Russia, Spain, individual chapters depends on subscription ix

(ask your librarian) but Springer provides • Volume 32 (2011): C 4 Photosynthesis and free downloadable front matter as well as Related CO 2 Concentrating Mechanisms , indexes at the above site. As of July, 2011, edited by Agepati S. Raghavendra and Rowan Tables of Contents have been available for all Sage, from India and Canada. Nineteen the volumes. The available web sites of the chapters, 425 pp, Hardcover, ISBN: 978- books in the Series are listed below. 90-481-9406-3 [http://www.springer.com/ • Volume 37 (2014) Photosynthesis in life+sciences/plant+sciences/book/978-90- Bryophytes and Early Land Plants, edited by 481-9406-3 ] David T. Hanson and Steven K. Rice, from • Volume 31 (2010): The Chloroplast: USA. Eighteen chapters, approx. 500 pp, Basics and Applications, edited by Hardcover, ISBN: 978-94-007-6987-8 (HB) Constantin Rebeiz (USA), Christoph ISBN 978-94-007-6988-5 (e-book) [ http:// Benning (USA), Hans J. Bohnert (USA), www.springer.com/life+sciences/ Henry Daniell (USA), J. Kenneth Hoober plant+sciences/book/978-94-007-6987-8 ] (USA), Hartmut K. Lichtenthaler (Germany), • Volume 36 (2013) Plastid Development in Archie R. Portis (USA), and Baishnab C. Leaves During Growth and Senescence , Tripathy (India). Twenty-fi ve chapters, 451 edited by Basanti Biswal, Karin Krupinska pp, Hardcover, ISBN: 978-90-481-8530-6 and Udaya Biswal, from India and Germany. [ http://www.springer.com/life+sciences/ Twenty-eight chapters, 837 pp, Hardcover, plant+sciences/book/978-90-481-8530-6 ] ISBN: 978-94-007-5723-3 (HB) ISBN 978-94- • Volume 30 (2009): Lipids in Photosynthesis: XXXXX (e-book) [ http://www.springer.com/ Essential and Regulatory Functions , edited life+sciences/plant+sciences/ by Hajime Wada and Norio Murata, both from book/978-94-007-5723-3 ] Japan. Twenty chapters, 506 pp, Hardcover, • Volume 35 (2012) Genomics of Chloroplasts ISBN: 978-90-481-2862-4; e-book, ISBN: and Mitochondria , edited by Ralph Bock 978-90-481-2863-1 [ http://www.springer.com/ and Volker Knoop, from Germany. Nineteen life+sciences/plant+sciences/book/978- chapters, 475 pp, Hardcover, ISBN: 978-94- 90-481-2862-4 ] 007-2919-3 (HB) ISBN 978-94-007-2920-9 • Volume 29 (2009): Photosynthesis in (e-book) [http://www.springer.com/life+ Silico: Understanding Complexity from sciences/plant+sciences/book/978-94-007- Molecules, edited by Agu Laisk, Ladislav 2919-3 ] Nedbal, and Govindjee, from Estonia, The • Volume 34 (2012) Photosynthesis – Plastid Czech Republic, and USA. Twenty chap- Biology, Energy Conversion and Carbon ters, 525 pp, Hardcover, ISBN: 978-1- Assimilation , edited by Julian Eaton-Rye, 4020-9236-7 [ http://www.springer.com/ Baishnab C. Tripathy, and Thomas D. Sharkey, life+sciences/plant+sciences/ from New Zealand, India, and USA. Thirty- book/978-1-4020-9236-7 ] three chapters, 854 pp, Hardcover, ISBN: 978- • Volume 28 (2009): The Purple Phototrophic 94-007-1578-3 (HB) ISBN 978-94-007-1579-0 Bacteria , edited by C. Neil Hunter, Fevzi (e-book) [http://www.springer.com/life+ Daldal, Marion C. Thurnauer and J. Thomas sciences/plant+sciences/book/978-94-007- Beatty, from UK, USA and Canada. Forty- 1578-3 ] eight chapters, 1053 pp, Hardcover, ISBN: • Volume 33 (2012): Functional Genomics 978-1-4020-8814-8 [ http://www.springer.com/ and Evolution of Photosynthetic Systems , life+sciences/plant+sciences/book/ edited by Robert L. Burnap and Willem 978-1-4020-8814-8 ] F. J. Vermaas, from USA. Fifteen chapters, • Volume 27 (2008): Sulfur Metabolism 428 pp, ISBN: 978-94-007- 1532–5 [ http:// in Phototrophic Organisms, edited by www.springer.com/life+sciences/book/ Christiane Dahl, Rüdiger Hell, David Knaff 978-94-007-1532-5 ] and Thomas Leustek, from Germany and USA. x

Twenty-four chapters, 551 pp, Hardcover, Adams, William W. Adams III and Autar ISBN: 978-4020-6862-1 [http://www.springer. K. Mattoo, from USA. Twenty-one chapters, com/life+sciences/plant+sciences/ 380 pp, Hardcover, ISBN: 978-14020-3564-7 book/978-1-4020-6862-1 ] [ http://www.springer.com/life+sciences/ • Volume 26 (2008): Biophysical Techniques plant+sciences/book/978-1-4020-3564-7 ] Photosynthesis, Volume II, edited by Thijs • Volume 20 (2006): Discoveries in Aartsma and Jörg Matysik, both from The Photosynthesis , edited by Govindjee, Netherlands. Twenty-four chapters, 548 pp, J. Thomas Beatty, Howard Gest and John Hardcover, ISBN: 978-1-4020-8249-8 [ http:// F. Allen, from USA, Canada and UK. One www.springer.com/life+sciences/ hundred and eleven chapters, 1304 pp, plant+sciences/book/978-1-4020-8249-8 ] Hardcover, ISBN: 978-1-4020-3323-0 [ http:// • Volume 25 (2006): Chlorophylls and www.springer.com/life+sciences/ Bacteriochlorophylls: , plant+sciences/book/978-1-4020-3323-0 ] Biophysics, Functions and Applications , • Volume 19 (2004): Chlorophyll a Fluo- edited by Bernhard Grimm, Robert J. Porra, rescence: A Signature of Photosynthesis , Wolfhart Rüdiger, and Hugo Scheer, from edited by George C. Papageorgiou and Germany and Australia. Thirty-seven chapters, Govindjee, from Greece and USA. Thirty- 603 pp, Hardcover, ISBN: 978-1-40204515-8 one chapters, 820 pp, Hardcover, ISBN: [ http://www.springer.com/life+sciences/ 978-1-4020-3217-2 [ http://www.springer.com/ plant+sciences/book/978-1-4020-4515-8 ] life+sciences/biochemistry+%26+biophysics/ • Volume 24 (2006): Photosystem I: The book/978-1-4020-3217-2 ] Light-Driven Plastocyanin: Ferredoxin • Volume 18 (2005): Plant Respiration: From Oxidoreductase , edited by John H. Golbeck, Cell to Ecosystem , edited by Hans Lambers from USA. Forty chapters, 716 pp, Hardcover, and Miquel Ribas-Carbo, from Australia and ISBN: 978-1-40204255-3 [http://www.springer. Spain. Thirteen chapters, 250 pp, Hardcover, com/life+sciences/plant+sciences/ ISBN: 978-14020-3588-3 [http://www. book/978-1-4020-4255-3 ] springer.com/life+sciences/plant+sciences/ • Volume 23 (2006): The Structure and book/978-1-4020-3588-3 ] Function of Plastids, edited by Robert R. • Volume 17 (2004): Plant Mitochondria: Wise and J. Kenneth Hoober, from USA. From Genome to Function , edited by David Twenty-seven chapters, 575 pp, Softcover, Day, A. Harvey Millar and James Whelan, ISBN: 978-1-4020-6570–6; Hardcover, ISBN: from Australia. Fourteen chapters, 325 pp, 978-1-4020-4060-3 [ http://www.springer. Hardcover, ISBN: 978-1-4020-2399-6 com/life+sciences/plant+sciences/book/ [ http://www.springerlink.com/content/ 978-1-4020-4060-3 ] 978-1-7923-2399-6 ] • Volume 22 (2005): Photosystem II: The • Volume 16 (2004): Respiration in Light-Driven Water: Plastoquinone Archaea and Bacteria: Diversity of Oxidoreductase , edited by Thomas Prokaryotic Respiratory Systems, edited J. Wydrzynski and Kimiyuki Satoh, from by Davide Zannoni, from Italy. Thirteen Australia and Japan. Thirty-four chapters, 786 chapters, 310 pp, Hardcover, ISBN: 978- pp, Hardcover, ISBN: 978-1-4020-4249-2 14020-2002-5 [ http://www.springer.com/ [ http://www.springer.com/life+sciences/ life+sciences/plant+sciences/ plant+sciences/book/978-1-4020-4249-2 ] book/978-1-4020-2002-5 ] • Volume 21 (2005): Photoprotection, • Volume 15 (2004): Respiration in Archaea Photoinhibition, Gene Regulation, and and Bacteria: Diversity of Prokaryotic Environment , edited by Barbara Demmig- Electron Transport Carriers , edited by xi

Davide Zannoni, from Italy. Thirteen chapters, Twenty-four chapters, 644 pp, Hardcover, 350 pp, Hardcover, ISBN: 978-1-4020-2001-8 ISBN: 978-07923-6143-5 [ http://www.springer. [ http://www.springer.com/life+sciences/ com/life+sciences/plant+sciences/book/ biochemistry+%26+biophysics/ 978-0-7923-6143-5 ] book/978-1-4020-2001-8 ] • Volume 8 (1999): The • Volume 14 (2004): Photosynthesis in Algae , of Carotenoids , edited by Harry A. Frank, edited by Anthony W. Larkum, Susan Douglas Andrew J. Young, George Britton and and John A. Raven, from Australia, Canada Richard J. Cogdell, from USA and UK. and UK. Nineteen chapters, 500 pp, Hardcover, Twenty chapters, 420 pp, Hardcover, ISBN: ISBN: 978-0-7923-6333-0 [http://link. 978-0-7923-5942-5 [ http://www.springer. springer.com/book/10.1007/978-94-007- com/life+sciences/plant+sciences/book/ 1038-2/page/1 ] 978-0-7923-5942-5 ] • Volume 13 (2003): Light-Harvesting • Volume 7 (1998): The Molecular Biology of Antennas in Photosynthesis , edited by Chloroplasts and Mitochondria in Beverley R. Green and William W. Parson, Chlamydomonas, edited by Jean David from Canada and USA. Seventeen chapters, Rochaix, Michel Goldschmidt-Clermont and 544 pp, Hardcover, ISBN: 978-07923-6335-4 Sabeeha Merchant, from Switzerland and [ http://www.springer.com/life+sciences/ USA. Thirty-six chapters, 760 pp, Hardcover, plant+sciences/book/978-0-7923-6335- ISBN: 978-0-7923-5174-0 [ http://www. 4?otherVersion=978-90-481-5468-5 ] springer.com/life+sciences/plant+sciences/ • Volume 12 (2003): Photosynthetic Nitrogen book/978-0-7923-5174-0 ] Assimilation and Associated Carbon and • Volume 6 (1998): Lipids in Photosynthesis: Respiratory Metabolism, edited by Christine Structure, Function and Genetics, edited H. Foyer and Graham Noctor, from UK and by Paul-André Siegenthaler and Norio France. Sixteen chapters, 304 pp, Hardcover, Murata, from Switzerland and Japan. Fifteen ISBN: 978-07923-6336-1 [ http://www. chapters, 332 pp, Hardcover, ISBN: 978-0- springer.com/life+sciences/plant+sciences/ 7923-5173-3 [ http://www.springer.com/ book/978-0-7923-6336-1 ] life+sciences/plant+sciences/ • Volume 11 (2001): Regulation of book/978-0-7923-5173-3 ] Photosynthesis, edited by Eva-Mari Aro and • Volume 5 (1997): Photosynthesis and the Bertil Andersson, from Finland and Sweden. Environment, edited by Neil R. Baker, from Thirty-two chapters, 640 pp, Hardcover, UK. Twenty chapters, 508 pp, Hardcover, ISBN: 978-0-7923-6332-3 [ http://www. ISBN: 978-07923-4316-5 [http://www. springer.com/life+sciences/plant+sciences/ springer.com/life+sciences/plant+sciences/ book/978-0-7923-6332-3 ] book/978-0-7923-4316-5 ] • Volume 10 (2001): Photosynthesis: • Volume 4 (1996): Oxygenic Photosynthesis: Photobiochemistry and Photobiophysics , The Light Reactions , edited by Donald edited by Bacon Ke, from USA. Thirty-six R. Ort and Charles F. Yocum, from USA. chapters, 792 pp, Softcover, ISBN: 978-0-7923- Thirty-four chapters, 696 pp, Softcover: ISBN: 6791-8; Hardcover: ISBN: 978-0-7923-6334-7 978-0-7923-3684–6; Hardcover, ISBN: 978- [ http://www.springer.com/life+sciences/ 0-7923-3683-9 [ http://www.springer.com/life+ plant+sciences/book/978-0-7923-6334-7 ] sciences/plant+sciences/book/978-0- • Volume 9 (2000): Photosynthesis: Physio- 7923-3683-9 ] logy and Metabolism , edited by Richard • Volume 3 (1996): Biophysical Techniques in C. Leegood, Thomas D. Sharkey and Susanne Photosynthesis, edited by Jan Amesz and von Caemmerer, from UK, USA and Australia. Arnold J. Hoff, from The Netherlands. xii

Twenty-four chapters, 426 pp, Hardcover, • Non-Photochemical Quenching (NPQ) and ISBN: 978-0-7923-3642-6 [ http://www. Energy Dissipation in Plants, Algae and springer.com/life+sciences/plant+sciences/ Cyanobacteria (Editors: Barbara Demmig- book/978-0-7923-3642-6 ] Adams, Győző Garab and Govindjee) • Volume 2 (1995): Anoxygenic Photo- • Cytochrome Complexes: Evolution, Structures, synthetic Bacteria , edited by Robert Energy Transduction, and Signaling (Editors: E. Blankenship, Michael T. Madigan and Carl William Cramer and Toivo Kallas) E. Bauer, from USA. Sixty-two chapters, 1331 • Photosynthesis for Bioenergy (Editors: pp, Hardcover, ISBN: 978-0-7923-3682-8 Elizabeth A. Ainsworth and Stephen P. Long) [ http://www.springer.com/life+sciences/ In addition to the above contracted books, plant+sciences/book/978-0-7923-3681-5 ] the following topics are under consideration: • Volume 1 (1994): The Molecular Biology of Cyanobacteria , edited by Donald R. Bryant, • Algae, Cyanobacteria: Biofuel and Bioenergy from USA. Twenty-eight chapters, 916 pp, • Artifi cial Photosynthesis Hardcover, ISBN: 978-1-4020-2400-9 [ http:// • ATP Synthase www.springerlink.com/content/978-1-4020- • Bacterial Respiration II 2400-9 ] • Carotenoids II • Cyanobacteria II Further information on these books and • Ecophysiology ordering instructions can be found at < http:// • Evolution of Photosynthesis www.springer.com/series/5599 >. References to all chapters of volumes 1–31 can be found • Global Aspects of Photosynthesis at < http://www.life.illinois.edu/govindjee/g/ • Green Bacteria and Heliobacteria References.html >. (For volumes 32–35, pdf • Interactions between Photosynthesis and other fi les of the entire Front Matter are also avail- Metabolic Processes able here.) • Limits of Photosynthesis: Where do we go Special 25 % discounts are available to from here members of the International Society of • Photosynthesis, Biomass and Bioenergy Photosynthesis Research, ISPR . See Stress < http://www.springer.com/ispr >. • Plant Respiration II If you have any interest in editing/co- Future Advances in Photosynthesis editing any of the above listed books, or and Respiration and Other Related being an author, please send an e-mail to Books Tom Sharkey ([email protected]) and/or to Govindjee at [email protected]. Suggestions The readers of the current series are encour- for additional topics are also welcome. aged to watch for the publication of the In view of the interdisciplinary character forthcoming books (not necessarily arranged of research in photosynthesis and respira- in the order of future appearance): tion, it is our earnest hope that this series of books will be used in educating students • The Structural Basis of Biological Energy and researchers not only in Plant Sciences, Generation (Editor: Martin Hohmann- Molecular and Cell Biology, Integrative Marriott) [This book is almost ready to go to Biology, Biotechnology, Agricultural the typesetters] Sciences, Microbiology, Biochemistry, • Canopy Photosynthesis: From Basics to Chemical Biology, Biological Physics, and Applications (Editors: Kouki Hikosaka, Ülo Biophysics, but also in Bioengineering, Niinemets and Niels P. R. Anten) Chemistry, and Physics. xiii

Acknowledgments their friendly working relation with us that led to the production of this book. We take this opportunity to thank and con- gratulate Davide Zannoni and Roberto October 24, 2013 Govindjee De Philippis for their outstanding editorial work; they have, indeed, done a fantastic job, Department of Plant Biology, not only in editing, but also in organizing this Department of Biochemistry and Center book for all of us, and for their highly profes- of Biophysics & Quantitative Biology sional dealing with the reviewing process. University of Illinois at Urbana-Champaign, We thank all the 42 authors of this book Urbana, IL 61801, USA (see the list above); without their authoritative [email protected] chapters, there would be no such volume. We give special thanks to A. Lakshmi Praba, Thomas D. Sharkey SPi Global, India for directing the typeset- Department of Biochemistry ting of this book; her expertise has been cru- and Molecular Biology cial in bringing this book to completion. We Michigan State University, owe Jacco Flipsen, Andre Tournois, and East Lansing, MI 48824, USA Ineke Ravesloot (of Springer) thanks for [email protected]

Series Editors

The above photograph shows the 1965 Z-Scheme that Govindjee had made when he, with Eugene Rabinowitch, had coined the term P680 for the reaction center of Photosystem II. From left to right: Rebecca Slattery (a graduate student of Donald R. Ort), Robert Koester (a graduate student of Lisa Ainsworth), and Govindjee. Photo by Joan Huber taken in May, 2013.

Govindjee , who uses one name only, was short-wavelength form of chlorophyll (Chl) a born on October 24, 1932, in Allahabad, functioning in the Chl b -containing system, India. Since 1999, he has been Professor now called PS II; of the two-light effect in Emeritus of Biochemistry, Biophysics, and Chl a fl uorescence; and, with his wife Rajni, Plant Biology at the University of Illinois at of the two-light effect (Emerson enhance- Urbana-Champaign (UIUC), Urbana, IL, ment) in NADP reduction in chloroplasts. USA. He obtained his B.Sc. (Chemistry and His major achievements, with many col- Biology) and M.Sc. (Botany: Plant laborators, include an understanding Physiology) in 1952 and 1954 from the of the basic relationships between Chl a University of Allahabad. Govindjee studied fl uorescence and photosynthetic reactions; a “Photosynthesis” at the UIUC under two unique role of bicarbonate/carbonate on the pioneers of photosynthesis, Robert Emerson electron acceptor side of PS II, particularly and Eugene Rabinowitch, obtaining his Ph.D. in the protonation events involving the QB in 1960, in Biophysics. He is best known for binding region in PSII; molecular under- his research on excitation energy transfer, standing of thermoluminescence in plants, light emission, primary photoche mistry, and algae and cyanobacteria; the fi rst picosecond electron transfer in “Photosystem II” (PS II, measurements on the primary photoche- water-plastoquinone oxidoreductase). His mistry of PS II; and the fi rst use of Chl early research included the discovery of a a fl uorescence lifetime measurements in

xv xvi understanding photoprotection, by plants “Photosynthesis” (Guest Editor: Julian and algae, against excess light. His current Eaton-Rye); (2) in 2008, through a special focus is on the “History of Photosynthesis International Symposium on “Photosynthesis Research,” on “Photosynthesis Education,” in a Global Perspective,” at the University of and on “What to Learn from Natural Indore, India; (3) in 2012, through dedica- Photosynthesis to do Artifi cial Photo- tion to him of volume 34 of this series, cele- synthesis.” He has served on the faculty of brating his 80th year; (4) in 2012, through the UIUC for approximately 40 years. another book Photosynthesis: Overviews on Govindjee’s honors include: Fellow of the Recent Progress and Future Perspectives , American Association of Advancement of honoring him for his outstanding research Science (AAAS); Distinguished Lecturer of and teaching of photosynthesis and for being the School of Life Sciences, UIUC; Fellow a global leader for stimulating photosyn- and Lifetime Member of the National thesis research throughout the world ; and Academy of Sciences (India); President of (5) in 2013, through two special volumes of the American Society for Photobiology Photosynthesis Research, on “Photosyn- (1980–1981); Fulbright Scholar (1956), thesis Education”, which also celebrates his Fulbright Senior Lecturer (1998) and 80th birthday (Guest Editors: Suleyman Fulbright Specialist (2012); Honorary Allakhverdiev; Jian-Ren Shen and Gerald President of the 2004 International Edwards). Govindjee is coauthor of Photo- Photosynthesis Congress (Montréal, synthesis (John Wiley, 1969) and editor of Canada); the fi rst recipient of the Lifetime many books, published by several publishers Achievement Award of the Rebeiz including Academic Press and Springer. Foundation for Basic Biology, 2006; 2007 Since 2007, each year Govindjee and recipient of the Communication Award of Rajni Govindjee Award for Excellence in the International Society of Photosynthesis Biological Sciences is being given to gra- Research (ISPR); 2008 recipient of the duate students by the Department of Plant Liberal Arts & Sciences (LAS) Lifetime Biology at the UIUC. Starting in 2014, these Achievement Award of the UIUC. Further, awards will alternate between Department of Govindjee was honored (1) in 2007, through Biochemistry (even years) and Department two special volumes of Photosynthesis of Plant Biology (odd years). For further Research , celebrating his 75th birthday and information on Govindjee, see his website for his 50-year dedicated research in http://www.life.illinois.edu/govindjee .

Thomas D. (Tom) Sharkey obtained his interests center on the biochemistry and Bachelor’s degree in Biology in 1974 from biophysics of gas exchange between plants Lyman Briggs College, a residential science and the atmosphere. Photosynthetic gas college at Michigan State University, East exchange, especially carbon dioxide uptake Lansing, Michigan, USA. After 2 years as a and use, and isoprene emission from plants, research technician in the federally funded are the two major research topics in his labo- Plant Research Laboratory at Michigan State ratory. Among his contributions are mea- University under the mentorship of Prof. surements of the carbon dioxide concentration Klaus Raschke, Tom entered the Ph.D. pro- inside leaves, studies of the resistance to dif- gram in the same lab, and graduated in 1980. fusion of carbon dioxide within the meso- Postdoctoral research was carried out with phyll of leaves of C3 plants, and an exhaustive Prof. Graham Farquhar at the Australian study of short-term feedback effects on National University, in Canberra, where he carbon metabolism. As part of the study of co-authored a landmark review on photosyn- short-term feedback effects, Tom’s research thesis and stomatal conductance that contin- group demonstrated that maltose is the major ues to receive much attention 30 years after form of carbon export from chloroplasts at its publication. For 5 years, Tom worked at night, and made signifi cant contributions to the Desert Research Institute together with the elucidation of the pathway by which leaf Prof. Barry Osmond, followed by 20 years as starch is converted to sucrose at night. In the a Professor of Botany at the University of isoprene research fi eld, Tom is recognized Wisconsin in Madison. In 2008, Tom became as the leading advocate for thermotolerance Professor and Chair of the Department of of photosynthesis as the explanation for Biochemistry and Molecular Biology at why plants emit isoprene. In addition, his Michigan State University. Tom’s research laboratory has cloned many of the genes

xvii xviii that underlie isoprene synthesis, and he has Carbon Assimilation, Advances in published many papers on the biochemical Photosynthesis and Respiration Including regulation of isoprene synthesis. Tom Bioenergy and Related Processes, Julian has coedited three books: T.D. Sharkey, J. Eaton-Rye, Baishnab C. Tripathy and E.A. Holland and H.A. Mooney (Eds.) Trace Thomas D. Sharkey (Eds.) Springer. Tom Gas Emissions from Plants , Academic, San joined the series founder Govindjee as Series Diego, CA, 1991; R.C. Leegood, T.D. Sharkey, Co-editor from Volume 31 of this series. and S. von Caemmerer (Eds.) Physiology Tom is currently the Chairperson of the and Metabolism, Advances in Photosynthesis Department of Biochemistry and Molecular (and Respiration), Volume 9 of this Series, Biology, Michigan State University, East Kluwer (now Springer), Dordrecht, 2000; Lansing, Michigan. For further information and Volume 34 of this series Photosynthesis: see his web page at: < http://www.bmb.msu. Plastid Biology, Energy Conversion and edu/faculty/sharkey/Sharkey/index.html > Contents

From the Series Editors vii

Series Editors xv

Preface xxv

The Editors xxvii

Contributors xxxi

Author Index xxxv

Part I: General and Molecular Aspects of Bio-Hydrogen Generation

1 Bioenergy from Microorganisms: An Overview 3–21 Patrick C. Hallenbeck Summary 3 I. Climate Change and Future Energy Challenges 4 II. A Wide Variety of Biofuels 6 III. The Microbial Production of Hydrogen 11 References 19

2 Structural Foundations for O2 Sensitivity and O2 Tolerance in [NiFe]-Hydrogenases 23–41 Anne Volbeda and Juan C. Fontecilla-Camps Summary 23 I. Introduction 24 II. [NiFe]-Hydrogenases 25

III. Structural Studies of O2-Sensitive [NiFe]-Hydrogenases 27 IV. Structural Studies of O2-Resistant [NiFeSe]-Hydrogenases 29 V. Structural Studies of O2-Tolerant Membrane-Bound [NiFe]-Hydrogenases 30 VI. Regulation of Hydrogenase Expression and Activity: The Example of Escherichia coli 32 VII. [NiFe]-Hydrogenase Maturation 33 VIII. Biotechnological Applications 35 IX. Conclusions 37 References 37

xix xx

3 Engineering Hydrogenases for H2 Production: Bolts and Goals 43–77 Marc Rousset and Pierre-Pol Liebgott Summary 43 I. Introduction 44 II. Classifi cation and Physiological Properties of Hydrogenases46 III. Maturation of Hydrogenases: Specifi c and Complex Process56

IV. Enzyme and Metabolic Engineering to Improve H2 Production 58 V. Conclusion 70 References 70

4 H2 Production Using Cyanobacteria/Cyanobacterial Hydrogenases: From Classical to Synthetic Biology Approaches 79–99 Catarina C. Pacheco , Paulo Oliveira , and Paula Tamagnini Summary 79 I. Introduction 80 II. Transcriptional Regulation and Maturation of Cyanobacterial Hydrogenases 81

III. Strategies to Improve Cyanobacterial H2 Production 83 IV. Conclusions and Future Perspectives 93 References 94

5 Hydrogen Production by Water Biophotolysis 101–135 Maria L. Ghirardi , Paul W. King , David W. Mulder , Carrie Eckert , Alexandra Dubini , Pin-Ching Maness , and Jianping Yu Summary 101 I. Introduction 102 II. Hydrogenases 109 III. Ferredoxin Network in Chlamydomonas reinhardtii 117

IV. Barriers to H2 Photoproduction 118 References 121

6 Nitrogenase-Dependent Hydrogen Production by Cyanobacteria 137–153 Hermann Bothe and William E. Newton Summary 137 I. Introduction 138 II. Nitrogenases in Cyanobacteria 138 III. Hydrogen Production by Nitrogenases 141 IV. Hydrogen Formation in Heterocystous Cyanobacteria 142 V. Hydrogen Formations by Unicellular Cyanobacteria 145 VI. Conclusion 149 References 149 xxi

7 Systems Biology of Photobiological Hydrogen Production by Purple Non-sulfur Bacteria 155–176 James B. McKinlay Summary 155 I. Introduction 156 II. Purple Non-sulfur Bacteria in the Light of Genomics and Systems Biology 158 III. Deciphering and Engineering the Metabolic

and Regulatory Mechanisms Involved in H2 Production 162 IV. Future Directions for a System- Level Understanding

of Photobiological H2 Production 169 References 172

8 The Extremely Thermophilic Genus Caldicellulosiruptor: Physiological and Genomic Characteristics for Complex Conversion to Molecular Hydrogen 177–195 Jeffrey V. Zurawski , Sara E. Blumer-Schuette , Jonathan M. Conway , and Robert M. Kelly , Summary 177 I. Introduction 178 II. Extracellular Deconstruction of Lignocellulosic Biomass 179 III. Carbohydrate Transport 184 IV. Intermediary Metabolism 186 V. Metabolism of Fuel Production 188 References 192

9 Members of the Order Thermotogales: From Microbiology to Hydrogen Production 197–224 Martina Cappelletti , Davide Zannoni , Anne Postec , and Bernard Ollivier Summary 197 I. Introduction 198 II. Habitat 198 III. Metabolic Features 202 IV. Hydrogen Production by Thermotogales spp. 206 V. Future Perspectives 218 References 219

10 Bioelectrochemical Systems for Indirect Biohydrogen Production 225–233 John M. Regan and Hengjing Yan Summary 225 I. Principles of Microbial Electrolysis Cells 226 II. Microbial Catalysts at the Anode 229 III. Cathode Reaction 229 References 231 xxii

Part II: Applied Aspects in Biohydrogen Production

11 Applications of Photofermentative Hydrogen Production 237–267 Inci Eroglu , Ebru Ö zgü r , Ela Eroglu , Meral Yü cel , and Ufuk Gü ndü z Summary 238 I. Introduction 238 II. Guidelines for Effective Photofermentative Hydrogen Production 239 III. Utilization of Waste Materials for Photofermentative Hydrogen Production 242 IV. Photofermentative Hydrogen Production with Dark Fermenter Effluents 246 V. Optimization of Hydrogen Yield 254 VI. Efficiency Analysis 260 VII. Future Prospects 260 References 262

12 Photosynthesis and Hydrogen Production in Purple Non Sulfur Bacteria: Fundamental and Applied Aspects 269–290 Alessandra Adessi and Roberto De Philippis Summary 269 I. Introduction 270

II. The H2 Production Process in Purple Bacteria 270 III. Anoxygenic Photosynthesis 272 IV. Photosynthetic Efficiency (PE) 277 V. Substrate to Hydrogen Conversion (SC) 282 VI. Process Bottlenecks – Conclusions 283 References 285

13 Photobioreactors Design for Hydrogen Production 291–320 José Maria Fer ná ndez-Sevilla , Francisco Gabriel Acié n-Fer ná ndez , and Emilio Molina-Grima Summary 291 I. Introduction 292

II. Major Routes for the Photobiological H2 Production 293 III. Major Factors Impacting on Photobioreactor Performance 295 IV. Principles for Photobioreactors Design and Scale Up 298 V. Concluding Remarks 316 References 317 xxiii

14 Immobilization of Photosynthetic Microorganisms for Efficient Hydrogen Production 321–347 Anatoly Tsygankov and Sergey Kosourov Summary 321 I. Introduction 322 II. Methods of Immobilization 322 III. Mechanical Support and Photobioreactors for Immobilized Photosynthetic Microorganisms 330 IV. Hydrogen Production by Purple Bacteria 331 V. Hydrogen Production by Immobilized Microalgae 332 VI. Hydrogen Production by Immobilized Cyanobacteria 337 VII. Concluding Remarks 341 References 342

15 Hydrogen Production and Possible Impact on Global Energy Demand: Open Problems and Perspectives 349–356 Davide Zannoni , Giacomo Antonioni , Dario Frascari , and Roberto De Philippis Summary 349 I. Introduction 350 II. Hydrogen as Energy Carrier 350 III. Hydrogen Storage: An Open Problem 351 IV. Safety Issues in the Use of Hydrogen as a Fuel 354 V. Economical and Political Issues 354 VI. Conclusions 355 References 355

Subject Index 357–366

Preface

There is a general consensus in considering microbial hydrogen production in natural the use of fossil fuels (petroleum, natural gas habitats is the fact that although a large and coal) as the cause of serious environ- number of bacteria, belonging to different mental problems. Because the amount of taxonomic groups, possess the capability to energy derived from these fossil reserves is produce hydrogen, free hydrogen of biologi- close to 80 % of the entire World’s energy cal origin can hardly be captured in nature consumption, there is a pressing need of new, because hydrogen-producing and hydrogen- non-polluting and sources consuming microorganisms live in the same (Report of the International Energy Agency, natural environments. 2010). Although hydrogen (H 2 ) is not a pri- Bio-hydrogen production has been known mary energy source, it has been considered a for almost a century and research directed at promising alternative to fossil fuels. By defi - applying this process to a practical means of nition, an energy source is such only if useful hydrogen fuel production has been carried out energy can be directly extracted or recovered for over a quarter of a century. A milestone in from it; in this respect, H 2 is an “energy car- bio-hydrogen research was the observation by rier” as it is derived from an energy reservoir Hans Gaffron, while working at the University and it can be used, like electricity, for the of Chicago in 1939, that algae can generate “transport” of energy from the production hydrogen by both fermentation and photo- site to the sites of its use. The main conse- chemistry (H. Gaffron (1939) Reduction of quence of this feature is that hydrogen can be CO2 with H2 in green plants. Nature 143:204– produced only by consuming primary energy 205). Ten years later, Gest and Kamen (H. sources, which at the moment are mainly Gest and M.D. Kamen (1949) Photoproduction fossil fuels. However, there are at least two of molecular hydrogen by Rhodospirillum properties making the use of hydrogen quite rubrum. Science 109: 558–559) discovered attractive, namely: its large presence in the light-dependent production of hydrogen in nature, even if usually linked with other parallel to nitrogen fi xation by the facultative atoms, e.g. with oxygen in water or with photosynthetic bacterium Rhodospirillum oxygen, carbon and other elements in organic rubrum. Notably, in “ Memoir of a 1949 rail- compounds, and the possibility to use it way journey with photosynthetic bacteria ” without releasing pollutants or greenhouse (Photosynthesis Res 61: 91–96), H. Gest gases (GHGs) in the atmosphere. Inte- (1999) commented on this discovery as “A restingly, hydrogen can also be produced by serendipic observation at the Hopkins Marine exploiting the metabolic features of several Station of Stanford University in 1948 led to microorganisms in a carbon neutral process the discovery that anoxygenic photosynthetic that has been called “biological hydrogen bacteria can fi x molecular nitrogen … and production”. Bio-hydrogen production is generate hydrogen”. One of us (Zannoni D), also characterized by important advantages while working as an associate researcher at over the thermochemical and electrochemical the St. Louis University Medical School in techniques currently utilized or under study. 1978, was fortunate enough to have known Indeed, microbiological processes can pro- personally H. Gest, Professor of Microbiology duce hydrogen using renewable resources, in at the University of Bloomington (Indiana). carbon neutral processes operating at room He remembers that they had a long discussion temperature and pressure, and with low envi- on the way to defi ne what it is now recog- ronmental impact. A negative aspect of the nized as the “accessory oxidant-dependent

xxv xxvi fermentation in photosynthetic bacteria” ity of several genome sequences and their (See: The Photo trophic Bacteria: Anaerobic metabolic features open new perspectives for Life in the Light, J.G. Ormerod Ed., 1983, vol biohydrogen generation. Bioelectrochemical 4, University of California Press, Blackwell systems coupled to indirect hydrogen pro- Sc. Pub.). Enormous advances have been duction are reviewed in Chap. 8 . These sys- made since then on genetics, biochemistry, tems are not subjected to the hydrogen yield and biotechnological applications of photo- constraints and have been proven to work synthetic bacteria and the present book, with any biodegradable organic substrate. entitled Microbial BioEnergy: Hydrogen Chapters 11 , 12 , 13 , and 14 are mostly dedi- Production is a compendium overviewing cated to photobioreactors using purple non- most of the processes important for the micro- sulfur bacteria and microalgae. This section bial hydrogen production including bacterial of the book examines in detail how hydrogen hydrogen photo-generation. production depends on various kinds of The book begins with a chapter on bio- organic wastes, on the photosynthetic effi - energy from microorganisms describing ciency and light distribution. The basic prin- some of the challenges in meeting future ciples for designing photobioreactors in energy needs in order to address climate mass culture for biofuel are also examined changes through the development of bioen- along with the advantages and limitations of ergy (Chap. 1). Critical factors in mature immobilized cell-systems for hydrogen pho- technologies and future directions in nascent toproduction. The volume ends with a chap- technologies are also reviewed. The volume ter (Chap. 15) dealing with the unconventional includes a section (Chaps. 2 , 3 , 4 , and 5 ) cov- concept that if hydrogen is used as an energy ering structural, molecular, and functional carrier, there are consistent benefi ts to be aspects of hydrogenases as effi cient biologi- expected, depending on how hydrogen is cal catalysts for the production of molecular generated. The existing technical problems hydrogen and, consequently, its oxidation a lying ahead for the creation of an apparent way to get rid of the excess reducing power “Hydrogen Based Society” are examined in cyanobacteria and green algae. As cyano- and it is concluded that they will be solved bacteria are unique organisms that accom- within a reasonable period of time. modate both oxygenic photosynthesis and Following the suggestion of the Series nitrogen fi xation, they are extensively editors, Govindjee and Tom Sharkey, we covered in Chap. 6 with respect to their pro- are deeply honored to dedicate this book to duction of ammonium concomitantly with Hans Gaffron (1902–1979) and Howard Gest hydrogen formation. Solar energy is also used (1921–2012). by photosynthetic purple non-sulfur bacteria to generate hydrogen gas from organic Davide Zannoni sources via the enzyme nitrogenase. Chapter 7 Department of Pharmacy focuses on the advances that have been and BioTechnology (FaBiT) made in hydrogen generation through the use University of Bologna of systems biology approaches such as Irnerio 42, 40126 Bologna , Italy genomics, transcriptomics and 13 C-fl uxomics [email protected] in Rhodopseudomonas palustris CGA009. Roberto De Philippis Chapters 8 and 9 cover two emerging research Department of AgriFood Production fi elds in hydrogen production: the use of and Environmental Sciences thermophilic and hyperthermophilic micro- P.zzale delle Cascine 24, organisms of the genera Caldicellulosiruptor 50144 Firenze , Italy and Thermotoga . As these genera utilize an extraordinary array of substrates that are Institute of Chemistry of Organometallic converted by dark-fermentation to hydrogen Compounds (ICCOM), CNR, Sesto at effi ciencies approaching the “Thauer Fiorentino, Florence, Italy limit” of 4 mol H2 /mol glucose, the availabil- roberto.dephilippis@unifi .it The Editors

Davide Zannoni , Professor of General Scotland U.K.; Département de Biologie Microbiology, received the doctoral degree Cellulaire et Moléculaire, Centre National in Biological Sciences, in 1973, from the Recherche Scientifi que (CNRS), Commis- University of Bologna, Italy; his thesis was sariat à l’Energie Atomique (CEA) Saclay on the Bioenergetics of the facultative Gif-sur-Yvette, France; Department of photosynthetic bacterium Rhodobacter (Rb.) Microbiology, University of Göttingen, capsulatus. During 1977–1978, he was a Göttingen, Germany, to investigate both the research fellow of the North Atlantic Treaty structure and the function of membrane Organization (NATO) at the St. Louis Medical redox-complexes in a variety of microbial School, Department of Biochemistry, genera. Zannoni’s scientifi c interests now St. Louis MO, USA, under the supervision include bioenergetics and genomics of of Prof. Barry L. Marrs. In 1979, he was microbial remediation of metals and metal- appointed Lecturer in Plant Biochemistry, loids in planktonic cells and biofi lms of and in 1981, he was promoted to become Rb. capsulatus and Pseudomonas pseudoal- Associate Professor of Plant Biochemistry, caligenes , molecular mechanisms of bacte- at the Faculty of Sciences, University of rial movement (chemo- and photo-taxis) and Bologna. As a research fellow of the biofi lm formation, alkane and naphthenic European Molecular Biology Organization acid degradation by Rhodococcus spp., the (EMBO) in 1981, 1983 and 1991, he visited use of microbial biofi lms as electricity- several European laboratories, namely: producing systems, and, fi nally, bio-hydrogen Department of Biochemistry and Micro- anaerobic production by Thermotoga. biology, St. Andrews University, St. Andrews Zannoni’s pioneering work on hydrogen

xxvii xxviii metabolism in Rb. capsulatus began in 1981 of Biology of the University of Bologna. He (European Community Solar Energy is presently acting as a Coordinator of the Research & Development). He is author and/ Master’s degree in Molecular & Industrial or co-author of more than 130 publications Biotechnology at the Department of in international research journals, and he has Pharmacy & Bio-Technology, University of published several research as well as text- Bologna – Alma Mater Studiorum, Italy. See books for students. From 2004 to 2010, Prof. his website < http://www.unibo.it/docenti/ Zannoni has been the Head of the Department davide.zannoni > for further information.

Roberto De Philippis , Associate Professor Production and Environmental Sciences. He of Microbial Biotechnology, received his is, at the same time, an Associate Researcher Laurea degree in Chemistry from the at the Institute of Chemistry of Organometa- University of Florence, Italy, in 1978; his llic Compounds, Italian National Research thesis was on the chemical interactions Council (ICCOM-CNR), Florence. His between nucleic acids and amino acids, as research activity is mainly concerned with studied by means of NMR and EPR tech- the physiology and biochemistry of photo- niques. During 1978 – 1981, he was a research synthetic bacteria. In particular, Roberto is scientist at the Research Center on Plastic studying the physiology and the possible Polymers at “Montedison” SpA, Milan, biotechnological exploitation of photo- Italy; during 1981–1983 he was responsible trophic microorganisms in the production of for the scientifi c and technical aspects of biopolymers of industrial interest or in pro- Baker’s yeast production at a Food Industry cesses related to the production of energy in Florence. During 1984–1990, he was a from renewable resources or for the treat- Research Fellow at the Institute of ment of polluted waters. He is also involved Agricultural and Technical Microbiology, in studies on the formation of phototrophic University of Florence. During 1990–2001, biofi lms on monuments or in the stabiliza- he served as a Lecturer at the Department of tion of desert soils by the use of phototrophic Food and Microbiological Science and microorganisms. He has been hosted for his Technology, University of Florence. From research by several Institutions in China, 2001, he has been an Associate Professor of India, Israel, Mexico, Portugal and USA. He Microbial Biotechnology at the University has published more than 80 scientifi c papers of Florence, Department of Agrifood in international peer -reviewed journals, ten

xxix xxx chapters in books, and has participated in From 2010, he has been a Delegate for Italy more than 90 international and national in the IEA-HIA (International Energy Congresses. During 1999–2001, Roberto Agency-Hydrogen Implementing Agreement) was Secretary/Treasurer, and currently, he is New Annex 21 “Bio-inspired and Biological President-elect of the International Society Hydrogen”. See the following website for for Applied Phycology. He is an Assistant further information: http://www.unifi .it/p- Editor of the Journal of Applied Phycology . doc-2012-200001-D-3f2a3d29392930.html Contributors

Francisco Gabriel Acién-Fernández Roberto De Philippis Department of Chemical Engineering , Department of Agrifood Production and University of Almería, Almería , Spain Environmental Sciences , University of [email protected] Florence, Florence , Italy Alessandra Adessi Institute of Chemistry of Organometallic Department of Agrifood Production and Compounds (ICCOM), CNR, Sesto Environmental Sciences , University of Fiorentino, Florence, Italy Florence, Florence , Italy roberto.dephilippis@unifi .it alessandra.adessi@unifi .it Alexandra Dubini Giacomo Antonioni National Renewable Energy Laboratory , Department of Civil, Chemical, Golden , CO , USA Environmental and Materials Engineering [email protected] (DICAM), University of Bologna , Carrie Eckert Bologna , Italy National Renewable Energy Laboratory , [email protected] Golden , CO , USA Sara E. Blumer-Schuette [email protected] Department of Chemical and Biomolecular Ela Eroglu Engineering , North Carolina State School of Chemistry and Biochemistry, University , Raleigh , NC , USA Centre for Strategic Nano-Fabrication, [email protected] The University of Western Australia , Hermann Bothe Perth , Australia Botanical Institute , The University [email protected] of Cologne , Cologne , Germany Inci Eroglu [email protected] Department of Chemical Engineering , Martina Cappelletti Middle East Technical University , Laboratory of General and Applied Ankara , Turkey Microbiology, Department of Pharmacy Department of Biotechnology , Middle East and BioTechnology (FaBiT) , Technical University , Ankara , University of Bologna , Bologna , Italy Turkey [email protected] [email protected] Jonathan M. Conway José Maria Fernández-Sevilla Department of Chemical and Biomolecular Department of Chemical Engineering , Engineering , North Carolina State University of Almería , University , Raleigh , NC , USA Almería , Spain [email protected] [email protected]

xxxi xxxii

Juan C. Fontecilla-Camps Sergey Kosourov Metalloproteins Unit , Institut de Biologie Institute of Basic Biological Problems , Structurale J.P. Ebel, Commissariat à Russian Academy of Sciences , l’Énergie Atomique, Centre National Pushchino, Moscow Region , de la Recherche Scientifi que, Russia Université Joseph Fourier, UMR 5075 , [email protected] Grenoble , France Pierre-Pol Liebgott [email protected] IRD, Aix-Marseille Université, Dario Frascari CNRS/INSU, MIO, UM 110, Department of Civil, Chemical, Marseille Cedex 09 , France Environmental and Materials Engineering [email protected] (DICAM), University of Bologna , Pin-Ching Maness Bologna , Italy National Renewable Energy Laboratory , [email protected] Golden , CO , USA Maria L. Ghirardi [email protected] National Renewable Energy Laboratory , James B. McKinlay Golden , CO , USA Department of Biology , Indiana University , [email protected] Bloomington , IN , USA Ufuk Gündüz [email protected] Department of Biotechnology , Emilio Molina-Grima Middle East Technical University , Department of Chemical Engineering , Ankara , Turkey University of Almería , Almería , Department of Biology , Middle East Spain Technical University , Ankara , [email protected] Turkey David W. Mulder [email protected] National Renewable Energy Laboratory , Patrick C. Hallenbeck Golden , CO , USA Department of Microbiology and [email protected] Immunology , University of Montreal , William E. Newton Montreal , QC , Canada Department of Biochemistry , Virginia [email protected] Polytechnic Institute and State University , Robert M. Kelly Blacksburg , VA , USA Department of Chemical and Biomolecular [email protected] Engineering , North Carolina State Paulo Oliveira University , Raleigh , NC , USA Bioengineering and Synthetic Microbiology [email protected] Group, IBMC – Instituto de Biologia Paul W. King Molecular e Celular , Universidade do Porto , National Renewable Energy Laboratory , Porto , Portugal Golden , CO , USA [email protected] [email protected] xxxiii

Bernard Ollivier Anatoly Tsygankov Aix-Marseille Université, Université du Institute of Basic Biological Problems , Sud Toulon-Var, CNRS/INSU, IRD, Russian Academy of Sciences , MIO, UM 110, Marseille Cedex 09 , Pushchino, Moscow Region , Russia France [email protected] [email protected] Anne Volbeda Ebru Özgür Metalloproteins Unit , Institut de MEMS Research and Application Center , Biologie Structurale J.P. Ebel, Middle East Technical University , Commissariat à l’Énergie Atomique, Ankara , Turkey Centre National de la Recherche [email protected] Scientifi que, Université Joseph Fourier, UMR 5075 , Grenoble , France Catarina C. Pacheco [email protected] Bioengineering and Synthetic Microbiology Group, IBMC – Instituto de Biologia Hengjing Yan Molecular e Celular , Universidade do Porto , Institute for Collaborative Biotechnologies , Porto , Portugal Department of Chemistry and Biochemistry, [email protected] University of California Santa Barbara , Anne Postec Santa Barbara , CA 93106 , USA Aix-Marseille Université, Université du Sud Jianping Yu Toulon-Var, CNRS/INSU, IRD, MIO, UM National Renewable Energy Laboratory , 110 , Marseille Cedex 09 , France Golden , CO , USA John M. Regan [email protected] Department of Civil and Environmental Meral Yücel Engineering , The Pennsylvania Department of Biotechnology , Middle East State University , University Park , Technical University , Ankara , PA , USA Turkey [email protected] Department of Biology , Middle East Marc Rousset Technical University , Ankara , Turkey CNRS, BIP , Marseille Cedex 20 , France [email protected] [email protected] Davide Zannoni Paula Tamagnini Department of Pharmacy and BioTechnology Bioengineering and Synthetic Microbiology (FaBiT) , University of Bologna , Group, IBMC – Instituto de Biologia Bologna , Italy Molecular e Celular , Universidade do Porto , [email protected] Porto , Portugal Jeffrey V. Zurawski Faculdade de Ciências, Departamento de Department of Chemical and Biomolecular Biologia , Universidade do Porto , Porto , Engineering , North Carolina State University, Portugal Raleigh , NC , USA [email protected] [email protected]

Author Index

Acién-Fernández, F.G. , 291–317 Liebgott, P.-P. , 43–70 Adessi, A. , 269–285 Antonioni, G. , 349–355 Maness, P.-C. , 101–121 McKinlay, J.B. , 155–172 Blumer-Schuette, S.E. , 177–192 Molina-Grima, E. , 291–317 Bothe, H. , 137–149 Mulder, D.W. , 101–121

Cappelletti, M. , 197–219 Newton, W.E. , 137–149 Conway, J.M. , 177–192 Oliveira, P. , 79–94 De Philippis, R. , 269–285, 349–355 Ollivier, B. , 197–219 Dubini, A. , 101–121 Özgür, E. , 237–262

Eckert, C. , 101–121 Pacheco, C.C. , 79–94 Eroglu, E. , 237–262 Postec, A. , 197–219 Eroglu, I. , 237–262 Regan, J.M. , 225–231 Fernández-Sevilla, J.M. , 291–317 Rousset, M. , 43–70 Fontecilla-Camps, J.C. , 23–37 Frascari, D. , 349–355 Tamagnini, P. , 79–94 Tsygankov, A. , 321–342 Ghirardi, M.L. , 101–121 Gündüz, U. , 237–262 Volbeda, A. , 23–37

Hallenbeck, P.C. , 3–19 Yu, J. , 101–121 Hengjing, Y. , 225–231 Yücel, M. , 237–262

Kelly, R.M. , 177–192 Zannoni, D. , 197–219, King, P.W. , 101–121 349–355 Kosourov, S. , 321–342 Zurawski, J.V. , 177–192

xxxv