Research Frontiers in Bioinspired Energy
Report of a Workshop

Committee on Research Frontiers in Bioinspired Energy
Board on Chemical Sciences and Technology
Division on Earth and Life Studies

                   OF THE NATIONAL ACADEMIES

Washington, D.C.

The National Academies of Sciences, Engineering, and Medicine
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Committee on Research Frontiers in Bioinspired Energy Board on Chemical Sciences and Technology Division on Earth and Life Studies

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, N.W. Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Gov- erning Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engi - neering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This study was supported by the U.S. Department of Energy under Award DE-SC0002584 and the National Science Foundation under Grant CBET-0948076. Any opinions, findings, conclusions, or recommendations expressed in this mate - rial are those of the authors and do not necessarily reflect the views of the National Science Foundation or of the U.S. Department of Energy. This report was prepared as an account of work sponsored by an agency of the U.S. government. Neither the U.S. government nor any agency thereof, nor any of their employees, makes any warranty, express or implied, or assumes any legal liability or responsibility for the accuracy, completeness, or usefulness of any information, apparatus, product, or process disclosed, or represents that its use would not infringe privately owned rights. Reference herein to any specific commercial product, process, or service by trade name, trademark, manufacturer, or otherwise does not necessarily constitute or imply its endorsement, recom - mendation, or favoring by the U.S. government or any agency thereof. The views and opinions of authors expressed herein do not necessarily state or reflect those of the U.S. government or any agency thereof. International Standard Book Number-13: 978-0-309-22044-6 International Standard Book Number-10: 0-309-22044-0 Additional copies of this report are available from The National Academies Press, 500 Fifth Street, N.W., Lockbox 285, Washington, DC 20055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, Cover image: Shewanella oneidensis by Rizlan Bencheikh and Bruce Arey, Environ- mental Molecular Sciences Laboratory, U.S. Department of Energy Pacific North - west National Laboratory. Copyright 2012 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal govern - ment on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its mem - bers, sharing with the National Academy of Sciences the responsibility for advis - ing the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in pro - viding services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council.

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COMMITTEE ON RESEARCH FRONTEIRS IN BIOINSPIRED ENERGY Chair GreGory A. Petsko, Brandeis University, Waltham, Massachusetts Members John Golbeck, Pennsylvania State University, University Park Julie MAuPiin-Furlow, University of Florida, Gainesville DouGlAs rAy, Pacific Northwest National Laboratory, Richland, Washington JAMes c. liAo, University of California, Los Angeles National Research Council Staff tinA M. MAsciAnGioli, Study Director erickA McGowAn, Program Officer (until April 2011) sheenA siDDiqui, Senior Program Associate AMAnDA cline, Administrative Assistant rAchel yAncey, Program Assistant Dorothy ZolAnDZ, Board Director v

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BOARD ON CHEMICAL SCIENCES AND TECHNOLOGY Co-chairs PAblo DebeneDetti, Princeton University, Princeton, New Jersey c. DAle Poulter, University of Utah, Salt Lake City Members ZhenAn bAo, Stanford University, Stanford, California robert berGMAn, University of California, Berkeley henry brynDZA, E. I. du Pont de Nemours & Company, Wilmington, Delaware eMily cArter, Princeton University, Princeton, New Jersey DAviD w. christiAnson, University of Pennsylvania, Philadelphia MAry JAne hAGenson, Chevron Phillips Chemical Company, LLC, The Woodlands, Texas cArol J. henry, George Washington University, Washington, D.C. Jill hruby, Sandia National Laboratories, Albuquerque, New Mexico MichAel c. kerby, ExxonMobil Chemical Company, Baytown, Texas chArles e. kolb, Aerodyne Research, Inc., Billerica, Massachusetts JoseF Michl, University of Colorado, Boulder sAnDer Mills, Merck Research Laboratories, Kenilworth, New Jersey DAviD l. Morse, Corning Incorporated, Corning, New York robert e. roberts, Institute for Defense Analyses, Washington, D.C. DArlene J. s. soloMon, Agilent Technologies, Inc., Santa Clara, California JeAn toM, Bristol-Myers Squibb, West Windsor, New Jersey DAviD wAlt, Tufts University, Medford, Massachusetts National Research Council Staff Dorothy ZolAnDZ, Director DouGlAs FrieDMAn, Program Officer kAthryn huGhes, Program Officer tinA M. MAsciAnGioli, Senior Program Officer AMAnDA cline, Administrative Assistant sheenA siDDiqui, Senior Program Associate rAchel yAncey, Program Assistant vi

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Preface In May 2007, the National Academies Chemical Sciences Roundtable held a public workshop on the topic of Bioinspired Chemistry for Energy,1 where government, academic, and industry representatives discussed promising research developments in solar-generated fuels, hydrogen-pro- cessing enzymes, artificial photosynthetic systems, and biological-based fuel cells. Workshop participants identified the need for a follow-up activ- ity that would explore bioinspired energy processes in more depth and involve a wider array of disciplines as speakers and participants. Particu - larly, workshop participants stressed the importance of holding a work - shop that would include more researchers from the biological sciences and engineering, as well as those involved in technological advances that enable progress in understanding these systems. Building upon the 2007 workshop, the National Academies Board on Chemical Sciences and Technology convened the workshop described in this report, titled Research Frontiers in Bioinspired Energy: Molecular-Level Learning from Natural Systems. The workshop featured invited presenta- tions and included discussion of key biological energy capture, storage, and transformation processes, gaps in knowledge and barriers to tran- sitioning the current state of knowledge into applications, and under- developed research opportunities that might exist beyond disciplinary 1 National Research Council. 2008. Bioinspired Chemistry for Energy: A Workshop Summary. Washington, DC: National Academies Press. vii

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viii PREFACE boundaries. Presentations and discussions focused on molecular-level understanding rather than development of large-scale applications. While reading this document, we sincerely hope you will come across a statement, figure, or discussion topic that entices you to collaborate or to interact with researchers in other disciplines or sectors in the area of bio - inspired energy. Although not comprehensive, this report should provide a good overview of some of the exciting and broad ranges of approaches scientists and engineers are exploring at the interfaces of chemistry, biol - ogy, geology, engineering, and energy applications. The Committee on Research Frontiers in Bioinspired Energy: Molecular-Level Learning from Natural Systems

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Acknowledgment of Reviewers This workshop summary has been reviewed in draft form by indi- viduals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the National Research Council’s Report Review Committee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published summary as sound as possible and to ensure that the summary meets institutional standards for clarity, objectivity, and responsiveness to the charge. The review comments and draft manu- script remain confidential to protect the integrity of the process. We wish to thank the following individuals for their review of this workshop summary: Steven Chuang, University of Akron Sharon Haynie, E. I. du Pont de Nemours & Company Charles E. Kolb, Aerodyne Research, Inc. Michael Ladisch, Purdue University Nikolai Lebedev, Naval Research Laboratory Frances S. Ligler (National Academy of Engineering), Naval Research Laboratory Although the reviewers listed above have provided many construc- tive comments and suggestions, they did not see the final draft of the workshop summary before its release. The review of this summary was overseen by Marye Anne Fox (National Academy of Sciences), University ix

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x ACKNOWLEDGMENTS of California, San Diego. Appointed by the National Research Council, she was responsible for making certain that an independent examination of this summary was carried out in accordance with institutional proce - dures and that all review comments were carefully considered. Responsi- bility for the final content of this summary rests entirely with the authors and the institution.

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Contents 1 Introduction 1 Workshop Organization, 2 Online Component, 5 2 Summary of Speaker Presentations 7 Time and Energy Scales in Biology, 7 Leslie Dutton Microbial Discovery, 10 Penelope Boston Synthetic Biology, 12 Steven Benner Bacteriorhodopsin: A Model Proton Ion Pump, 13 Janos Lanyi Novel Mechanisms of Anaerobic Methane Oxidation, 16 Rudolf Thauer Solar Energy Harvesting in the Epicuticle of the Oriental Hornet , 19 Marian Plotkin xi

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xii CONTENTS Energy Production in Biofuel Cells, 22 Kenneth Nealson Microbes and the Four Basic Strategies for Life on Earth, 26 Felisa Wolfe-Simon DNA Nanotechnology, 28 Nadrian C. Seeman 3 Summary of Key Breakout Discussion Topics 33 Defining “Bioinspired”, 34 Microbial Diversity and Setting Priorities, 36 Research and Collaborative Models, 39 Interdisciplinary Education, Training, and Outreach, 41 Synthetic Biology, 43 Microbial Nanowires and Fuel Cells, 45 The Big Picture, 47 Appendixes A Statement of Task 51 B Workshop Agenda 53 C Biographical Information Committee Members, 57 Guest Speakers, 59 Discussion Leaders, 63 D Workshop Attendees 67