INSPIRED BY BIOLOGY

FROM MOLECULES TO MATERIALS TO MACHINES

Committee on Biomolecular Materials and Processes

Solid State Sciences Committee

Board on Physics and Astronomy

Division on Engineering and Physical Sciences

Board on Life Sciences

Division on Earth and Life Studies

NATIONAL RESEARCH COUNCIL OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS

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inspired By Biology F r o m m o l e c u l e s t o m at e r i a l s t o m a c h i n e s Committee on Biomolecular Materials and Processes Solid State Sciences Committee Board on Physics and Astronomy Division on Engineering and Physical Sciences Board on Life Sciences 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 Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, 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 is based on work supported by Contract No. DE-FG02-05ER46197 between the National Academy of Sciences and the Department of Energy and Grant No. DMR-0426181 between the National Academy of Sciences and the National Science Foundation. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the views of the agencies that provided support for the project. Library of Congress Cataloging-in-Publication Data Inspired by biology : from molecules to materials to machines / Committee on Biomolecular Materials and Processes, Board on Physics and Astronomy, Board on Life Sciences, Division on Engineering and Physical Sciences, Division on Earth and Life Studies. p. cm. Includes bibliographical references. ISBN 978-0-309-11704-3 (pbk. book) — ISBN 978-0-309-11705-0 (pdf book) 1. Molecular biology. 2. Biomolecules—Analysis. 3. Materials—Biotechnology. 4. Biomedical materials. 5. Biomedical engineering. I. National Research Council (U.S.). Committee on Biomolecular Materials and Processes. QH506.I4817 2008 570—dc22 2008016751 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, http://www.nap.edu; and the Board on Physics and Astronomy, National Research Council, 500 Fifth Street, N.W., Washington, DC 20001; Internet, http://www.national-academies.org/bpa. Cover: Three images are shown on the cover of this book, one each to represent a molecule (middle), a material (bottom), and a machine (top) in biomolecular materials research. (Top) Myosin V (blue-green), a molecular motor that moves cargo around the cell by walking on actin (red). Courtesy of Paul R. Selvin, University of Illinois at Urbana-Champaign; created by precisiongraphics.com. (Middle) Antimicrobial peptoids are designed to mimic the amphipathic structures of antimicrobial peptides; models of the folded structure of a synthetic peptoid are shown in views both parallel and perpendicular to the helical axis. Residues are color coded: cationic, purple; hydrophobic, orange; all others, gray. Published in N.P. Chongsiriwatana, J.A. Patch, A.M. Czyzewski, M.T. Dohm, A. Ivankin, D. Gidalevitz, R.N. Zuckermann, and A.E. Barron, “Peptoids that mimic the structure, function, and mechanism of helical antimicrobial peptides,” Proceedings of the National Academy of Sciences USA 105(8):2794- 2799 (2008). Copyright 2008 National Academy of Sciences, U.S.A. (Bottom) Array of microlenses on the skeletal plate of a brittlestar Ophiocoma wendtii that functions as a sophisticated optical element. The whole structure is composed of an intricately shaped single calcite crystal. The lens size is approximately 50 microns. Courtesy of J. Aizenberg, Harvard University. Copyright 2008 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 members, sharing with the National Academy of Sciences the responsibility for advising 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 further- ing 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 providing 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. www.national-academies.org

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COMMITTEE ON BIOMOLECULAR MATERIALS AND PROCESSES ARUP K. CHAKRABORTY, Massachusetts Institute of Technology, Chair JOANNA AIZENBERG, Harvard University ANNELISE E. BARRON, Stanford University KEN A. DILL, University of California at San Francisco SHARON C. GLOTZER, University of Michigan YALE E. GOLDMAN, University of Pennsylvania ELIAS GREENBAUM, Oak Ridge National Laboratory W. JOHN KAO, University of Wisconsin at Madison DAVID NEEDHAM, Duke University V. ADRIAN PARSEGIAN, National Institutes of Health ALAN RUDOLPH, Adlyfe Inc. CYRUS R. SAFINYA, University of California at Santa Barbara CHARLES F. STEVENS, Salk Institute for Biological Studies DAVID A. WEITZ, Harvard University Staff DONALD C. SHAPERO, Director, Board on Physics and Astronomy FRANCES E. SHARPLES, Director, Board on Life Sciences ADAM P. FAGEN, Senior Program Officer, Board on Life Sciences NATALIA J. MELCER, Senior Program Officer, Board on Physics and Astronomy BETH MASIMORE, Christine Mirzayan Science and Technology Policy Graduate Fellow CARYN J. KNUTSEN, Senior Program Assistant, Board on Physics and , Astronomy PHILLIP D. LONG, Senior Program Assistant, Board on Physics and Astronomy (until August 2006) VAN AN, Financial Associate, Board on Physics and Astronomy v

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SOLID STATE SCIENCES COMMITTEE PETER F. GREEN, University of Michigan, Chair BARBARA JONES, IBM Almaden Research Center, Vice-Chair DANIEL P. AROVAS, University of California at San Diego COLLIN L. BROHOLM, Johns Hopkins University PAUL M. CHAIKIN, New York University GEORGE W. CRABTREE, Argonne National Laboratory ELBIO DAGOTTO, University of Tennessee and Oak Ridge National Laboratory DUANE DIMOS, Sandia National Laboratories SIDNEY R. NAGEL, University of Chicago MONICA OLVERA DE LA CRUZ, Northwestern University ARTHUR P. RAMIREZ, Alcatel-Lucent MARK D. STILES, National Institute of Standards and Technology ANTOINETTE TAYLOR, Los Alamos National Laboratory DALE J. VAN HARLINGEN, University of Illinois at Urbana-Champaign FRED WUDL, University of California at Santa Barbara Staff DONALD C. SHAPERO, Director, Board on Physics and Astronomy NATALIA J. MELCER, Senior Program Officer MERCEDES M. ILAGAN, Administrative Assistant VAN AN, Financial Associate vi

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BOARD ON PHYSICS AND ASTRONOMY ANNEILA I. SARGENT, California Institute of Technology, Chair MARC A. KASTNER, Massachusetts Institute of Technology, Vice-Chair JOANNA AIZENBERG, Harvard University JONATHAN A. BAGGER, Johns Hopkins University JAMES E. BRAU, University of Oregon PHILIP H. BUCKSBAUM, Stanford University ADAM S. BURROWS, University of Arizona PATRICK L. COLESTOCK, Los Alamos National Laboratory RONALD C. DAVIDSON, Princeton University ANDREA M. GHEZ, University of California at Los Angeles PETER F. GREEN, University of Michigan LAURA H. GREENE, University of Illinois at Urbana-Champaign WICK C. HAXTON, University of Washington JOSEPH HEZIR, EOP Group, Inc. ALLAN H. MacDONALD, University of Texas at Austin HOMER A. NEAL, University of Michigan JOSE N. ONUCHIC, University of California at San Diego WILLIAM D. PHILLIPS, National Institute of Standards and Technology CHARLES E. SHANK, Lawrence Berkeley National Laboratory THOMAS N. THEIS, IBM T.J. Watson Research Center MICHAEL S. TURNER, University of Chicago C. MEGAN URRY, Yale University Staff DONALD C. SHAPERO, Director NATALIA J. MELCER, Senior Program Officer MICHAEL H. MOLONEY, Senior Program Officer ROBERT L. RIEMER, Senior Program Officer DAVID B. LANG, Associate Program Officer CARYN J. KNUTSEN, Senior Program Assistant MERCEDES M. ILAGAN, Administrative Assistant VAN AN, Financial Associate vii

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BOARD ON LIFE SCIENCES KEITH YAMAMOTO, University of California at San Francisco, Chair ANN M. ARVIN, Stanford University School of Medicine RUTH BERKELMAN, Emory University DEBORAH BLUM, University of Wisconsin at Madison VICKI L. CHANDLER, University of Arizona JEFFERY L. DANGL, University of North Carolina at Chapel Hill PAUL R. EHRLICH, Stanford University MARK D. FITZSIMMONS, John D. and Catherine T. MacArthur Foundation JO HANDELSMAN, University of Wisconsin at Madison KENNETH H. KELLER, Johns Hopkins University School of Advanced International Studies, Bologna, Italy JONATHAN D. MORENO, University of Pennsylvania RANDALL MURCH, Virginia Polytechnic Institute and State University MURIEL E. POSTON, Skidmore College JAMES REICHMAN, University of California at Santa Barbara BRUCE W. STILLMAN, Cold Spring Harbor Laboratory MARC T. TESSIER-LAVIGNE, Genentech, Inc. JAMES TIEDJE, Michigan State University CYNTHIA WOLBERGER, Johns Hopkins University School of Medicine Staff FRANCES E. SHARPLES, Director KERRY A. BRENNER, Senior Program Officer ADAM P. FAGEN, Senior Program Officer ANN H. REID, Senior Program Officer MARILEE K. SHELTON-DAVENPORT, Senior Program Officer REBECCA L. WALTER, Senior Program Assistant MERCURY FOX, Program Assistant ANNA FARRAR, Financial Associate viii

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Preface The National Research Council of the National Academies convened the Com- mittee on Biomolecular Materials and Processes (BMAP) to assess current work and future promise at the intersection of biology and materials science. The Solid State Sciences Committee of the Board on Physics and Astronomy developed the charge for this study in consultation with the Board on Life Sciences and the study’s sponsors at the Department of Energy and the National Science Foundation. The Committee on BMAP was charged to identify the most compelling questions and the emerging scientific opportunities at the interface between biology and con- densed matter and materials research, suggest strategies to best meet the identified opportunities, and consider connections to national priorities, including health care, security, the workforce, and economic and societal needs. The committee did not address tissue engineering in this report, because it has been reviewed elsewhere1 and was considered outside the scope of the committee’s charge. The complete charge is reproduced in Appendix A. The Committee on BMAP is composed of experts from many different areas of biomolecular materials research (see Appendix B for biographical sketches of com- mittee members). The full committee met in person three times (see Appendix C) to address its charge. The committee formed subgroups to study areas in further detail and to develop the text of the final report. At its meetings, the committee heard from experts in the field and from the federal agencies that support BMAP 1 National Research Council, Capturing the Full Power of Biomaterials for Military Medicine, Wash- ington, D.C.: The National Academies Press (2004). ix

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Preface x research. Conference calls and e-mail were used to coordinate the work of the com- mittee between meetings. This final report reflects the committee’s enthusiasm and excitement for the research opportunities in BMAP. The report is the product of input from many people. On behalf of the commit- tee, I extend my thanks and appreciation to all who participated in this endeavor. I also thank the speakers who made formal presentations at the committee meetings (Appendix C); those presentations and the ensuing discussions strongly informed the committee’s deliberations. In addition, the committee would like to thank the following people for their insights: Ian Anderson, James R. Baker, Jr., Sergey Bezrukov, Mark S. Humayun, Nicholas A. Kotov, Ronald G. Larson, John Miao, Dean A. Myles, Kevin Plaxco, Rudi Podgornik, Clinton Potter, Roger Pynn, Don Rau, David A. Tirrell, Gregory Voth, Karen Wooley, Wenbing Yun, and Joshua Zimmerberg. In particular, Theresa Reineke is thanked for her insight and contri- bution to the challenges in the area of synthesis. Finally, I also thank the National Research Council staff (Natalia Melcer, Adam Fagen, Don Shapero, Frances Sharples, Phillip Long, and Caryn Knutsen) for their guidance and assistance throughout the development of the report. As chair, I am grateful to the committee members for their wisdom, coopera- tion, and commitment to ensuring the development of a comprehensive report. Arup Chakraborty, Chair Committee on BMAP

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Acknowledgment of Reviewers This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the National Research Council’s (NRC’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 report as sound as possible and to ensure that the report meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process. We wish to thank the following individuals for their review of this report: Robert H. Austin, Princeton University, William F. Carroll, Jr., Occidental Chemical Corporation, Robert J. Full, University of California at Berkeley, Laura L. Kiessling, University of Wisconsin at Madison, Robert S. Langer, Massachusetts Institute of Technology, Monica Olvera de la Cruz, Northwestern University, Jose N. Onuchic, University of California at San Diego, Joel M. Schnur, Naval Research Laboratory, and David A. Tirrell, California Institute of Technology. Although the reviewers listed above have provided many constructive com- ments and suggestions, they were not asked to endorse the conclusions or recom- mendations, nor did they see the final draft of the report before its release. The xi

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acknowledgment reviewers xii of review of this report was overseen by Peter B. Moore, Yale University. Appointed by the NRC, he was responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and the institution.

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Contents SUMMARY 1 1 INTRODUCTION 5 Unifying Concepts, 5 Areas for Research, 6 Alternative and Renewable Energy, 6 Health and Medicine, 7 National Security, 7 Next-Generation Bioinspired Materials, 8 Enabling Tools, 8 2 UNDERSTANDING BIOMOLECULAR PROCESSES: 10 TOWARD PRINCIPLES THAT GOVERN BIOMATERIAL DESIGN Multiple Cooperative Interactions, 11 Cells, 12 Cell-mimetic Materials, 14 Processes Far from Equilibrium, 15 Design Principles for Mechanics, 17 Self-assembly, Directed Assembly, and Spatiotemporal Assembly, 19 Hierarchical Self-assembly, 21 Complex Spatiotemporal Assembly, 23 xiii

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contents xiv Self-replicating, Self-healing, and Evolving Materials, 25 Self-replicating Materials, 26 Self-healing Materials, 27 Materials That Evolve, 27 Opportunities and Challenges, 28 Suggested Reading, 30 3 ADVANCED FUNCTIONAL MATERIALS 31 Alternative and Renewable Energy from Biomolecular Materials and Processes, 32 Biofuels and Processes, 33 Biomimetic Photosynthesis, 36 Biomolecular Motors, 41 Advanced Functional Materials in Health and Medicine, 48 Medical Diagnostics, 49 Targeted Drug Delivery, Targeted Imaging Systems, Targeted Radiation, 51 Neural Prosthetics, 54 Advanced Functional Materials and National Security, 57 Environmental Surveillance and Biosensing, 57 Functional Biomaterials for Decontamination and Protection, 58 Next-Generation Bioinspired Materials, 59 Supermaterials from Biology, 59 Materials That Mimic Proteins and Membranes, 67 Opportunities and Challenges, 71 Alternative and Renewable Energy, 71 Health and Medicine, 72 National Security, 73 Next-Generation Bioinspired Materials, 74 Suggested Reading, 74 4 PROBES AND TOOLS FOR BIOMOLECULAR MATERIALS 76 RESEARCH Three-Dimensional Electron Microscopy, 78 Hyperresolution Optical Microscopy, 81 X-ray Methods, 83 X-ray Tomography, 84 X-ray Diffraction, 85 Small-Angle X-ray Scattering, 86 Neutron Scattering, 87

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contents xv Single-Molecule Probes, 90 Single-Molecule Instrumentation, 92 Theory and Computation, 95 Modeling and Computer Simulation, 97 Access to High-Performance Computing Environments, 101 Informatics and Data Mining, 102 Public Domain Codes, 102 The Need for Theoretical Advances, 102 Synthesis of Biomolecular Materials, 104 Synthetic Methods for Materials Synthesis, 105 Materials Synthesis Using Natural Machinery, 107 Materials Synthesis Using a Natural Toolbox, 108 Macromolecular Assembly Routes, 109 Opportunities and Challenges, 113 Suggested Reading, 115 5 INFRASTRUCTURE AND RESOURCES 116 Education and Training, 117 Mechanisms for Bridging Biological and Materials Sciences, 120 Shared Resources and Essential Facilities, 122 Partnership Among Industry, Academia, and the National Laboratories, 125 Commercialization of Biomolecular Materials, 126 Biomolecular Properties, Processes, and Products, 126 Manufacturability and Production, 127 Specific Biomolecular Material Product Areas, 127 Challenges and Opportunities in Commercialization, 129 6 CONCLUSIONS AND RECOMMENDATIONS 131 Supporting Interdisciplinary Research, 132 Developing and Evaluating Programs for Interdisciplinary Education, 133 Emphasizing Both Fundamental and Applied Sciences, 135 Developing and Evaluating National Facilities Based on Midrange Instruments, 135 APPENDIXES A Statement of Task 139 B Biographies of Committee Members 140 C Committee Meeting Agendas 146 D Glossary 149

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