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Introduction

This report addresses the interdisciplinary emerging field of self-assembling biomolecular materials—its status, the opportunities that face it, and the research and infrastructure developments that are needed to ensure that it achieves its potential. This field is an exciting new area at the frontiers of materials science. It is based on the premise that nature has already done the critical experiments, and it is up to us to better understand them and learn how to profit from them. The focus of this report is the study and generalization of biomolecular self-assembly, as directed toward the development of new or advanced materials of technical importance. The underlying theme is the belief that there are important lessons to be learned from understanding, and perhaps mimicking, biological materials and the ways in which they self-assemble. This report conveys the relationship between materials complexity, materials self-assembly, and lessons learned from biology; it underscores the need to encourage a partnership between physical scientists, engineers, and biologists and medical researchers.

Biomolecular materials are those whose properties are abstracted from biology. They share many of the characteristics of biological materials but are not necessarily of biological origin. For example, they may be inorganic materials that are organized or processed in a biomimetic fashion. A key feature of biological and biomolecular materials is their ability to undergo self-assembly, a process in which supermolecular hierarchical organization is established without external intervention.1

The field of biomolecular materials is an emerging discipline at the intersection of molecular biology, the physical sciences, and materials engineering. In the words of H. Ringsdorf,2 “the field … is now located at the interface between life-science and materials science. It applies the principles of self organization, regulation, replication, communication and cooperativity and has advanced to a promising area of applied science, undermining the borderline between scientific disciplines and offering new routes for the design of materials where the organization precedes the function.” This is schematically demonstrated in Figure 1. The technological promise includes, but extends well beyond, the health applications of biomaterials and biotechnology. The stage has been set by progress in modern molecular biology, the development of powerful microscopic characterization techniques, and advances in theoretical understanding.

We are now ready for the development of a physical understanding of the complex but exquisite behavior manifested by biological systems, including recognition and response, self-assembly, and self-repair. These principles can be extended to the control of modern materials synthesis and will lead to new materials and processes with a broad range of technological impact. The approaches used can be expected to fall into two general categories. The first involves directly mimicking biological systems or processes to produce materials with enhanced properties. An example of this approach is the use of molecular genetic techniques to produce polymers with unprecedentedly uniform molecular length. The second category involves studying how nature accomplishes a task or creates a structure with unusual properties, and then applying similar techniques in a completely different context or using completely different materials. An example of this approach is the study of the laminated structure of clam shells, which has been reverse-engineered to design a metal ceramic composite. This composite has twice the strength of other composites, is an order of magnitude tougher, and is, of course, constructed of more robust materials than its natural analogue. Such reverse engineering, in which lessons learned from a

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Examples of self-assembly include protein folding, the formation of liposomes, and the alignment of liquid crystals. While this type of equilibrium self-assembly is the central focus of this report, it is important to emphasize that much biological assembly is also driven by energy sources such as adenosine triphosphate (ATP), which power biomotors for chemical transduction and other processes. These biomotors are considered to be biomolecular and are discussed in the body of this report, but strictly speaking they do not conform to the panel's definition of self-assembly.

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H. Ringsdorf, Supermolecular Science 1:5 (1994).



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--> 1 Introduction This report addresses the interdisciplinary emerging field of self-assembling biomolecular materials—its status, the opportunities that face it, and the research and infrastructure developments that are needed to ensure that it achieves its potential. This field is an exciting new area at the frontiers of materials science. It is based on the premise that nature has already done the critical experiments, and it is up to us to better understand them and learn how to profit from them. The focus of this report is the study and generalization of biomolecular self-assembly, as directed toward the development of new or advanced materials of technical importance. The underlying theme is the belief that there are important lessons to be learned from understanding, and perhaps mimicking, biological materials and the ways in which they self-assemble. This report conveys the relationship between materials complexity, materials self-assembly, and lessons learned from biology; it underscores the need to encourage a partnership between physical scientists, engineers, and biologists and medical researchers. Biomolecular materials are those whose properties are abstracted from biology. They share many of the characteristics of biological materials but are not necessarily of biological origin. For example, they may be inorganic materials that are organized or processed in a biomimetic fashion. A key feature of biological and biomolecular materials is their ability to undergo self-assembly, a process in which supermolecular hierarchical organization is established without external intervention.1 The field of biomolecular materials is an emerging discipline at the intersection of molecular biology, the physical sciences, and materials engineering. In the words of H. Ringsdorf,2 “the field … is now located at the interface between life-science and materials science. It applies the principles of self organization, regulation, replication, communication and cooperativity and has advanced to a promising area of applied science, undermining the borderline between scientific disciplines and offering new routes for the design of materials where the organization precedes the function.” This is schematically demonstrated in Figure 1. The technological promise includes, but extends well beyond, the health applications of biomaterials and biotechnology. The stage has been set by progress in modern molecular biology, the development of powerful microscopic characterization techniques, and advances in theoretical understanding. We are now ready for the development of a physical understanding of the complex but exquisite behavior manifested by biological systems, including recognition and response, self-assembly, and self-repair. These principles can be extended to the control of modern materials synthesis and will lead to new materials and processes with a broad range of technological impact. The approaches used can be expected to fall into two general categories. The first involves directly mimicking biological systems or processes to produce materials with enhanced properties. An example of this approach is the use of molecular genetic techniques to produce polymers with unprecedentedly uniform molecular length. The second category involves studying how nature accomplishes a task or creates a structure with unusual properties, and then applying similar techniques in a completely different context or using completely different materials. An example of this approach is the study of the laminated structure of clam shells, which has been reverse-engineered to design a metal ceramic composite. This composite has twice the strength of other composites, is an order of magnitude tougher, and is, of course, constructed of more robust materials than its natural analogue. Such reverse engineering, in which lessons learned from a 1   Examples of self-assembly include protein folding, the formation of liposomes, and the alignment of liquid crystals. While this type of equilibrium self-assembly is the central focus of this report, it is important to emphasize that much biological assembly is also driven by energy sources such as adenosine triphosphate (ATP), which power biomotors for chemical transduction and other processes. These biomotors are considered to be biomolecular and are discussed in the body of this report, but strictly speaking they do not conform to the panel's definition of self-assembly. 2   H. Ringsdorf, Supermolecular Science 1:5 (1994).

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--> Figure 1 Illustration of the relationships among various aspects of biomolecular materials and their connections with the life sciences. (Courtesy of H. Ringsdorf, Johannes Gutenberg Universität Mainz.) biological system are applied to a completely different system, is a very important concept, for in many applications the environment (e.g., temperature, pressure, corrosive chemicals) is more severe than the original biological system or material can tolerate. In addition, understanding how nature accomplishes a task or creates an unusual structure may lead to new materials or processes in which the advance is in learning to reverse nature's approach, rather than in learning to copy or modify it, so as to eliminate materials characteristics that are undesirable. Although still in its infancy, the application of biological principles to the development of new materials has already been demonstrated. A nucleus of broad-based research already exists, involving a variety of disciplines including chemistry, physics, biology, materials science, and engineering. The field of biomolecular materials requires substantial additional basic research, however. Many significant applications are to be expected, but they may require a decade of research and development. The results of the research may not necessarily be systems that are strictly analogous or equivalent to those found in nature. It may be that payoffs will come in areas in which no functioning examples or archetypes yet exist. The unique properties of biomolecular materials can be ascribed to certain common characteristics: They are typically composed of molecules that interact by multiple, weak, orientation-dependent forces. Because these molecules interact weakly, thermal fluctuations are important. The materials are often self-assembled into structures on mesoscopic length scales from 100 Å to 10 mm.

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--> These structures may be hierarchical;3 i.e., they may be organized on multiple length scales with multiple functions at each scale. The systems that they form consist of several components. The following specific examples of current research may help to give the reader an idea of the character of this exciting field: Polymer biosynthesis.4 Biosynthetic routes are being explored for the preparation of biobased polymers: natural fibers, modified versions of natural proteins, and synthetic proteins that have no close natural analogues. Self-assembled monolayers and multilayers.5 The phase behavior of self-assembling surfactant monolayers on both fluid and solid substrates is being mapped out. These monolayers are effective in applications such as lithographic masking and high-resolution reaction templating. They also have potential as chemical sensors, as nonlinear optical elements, in neuronal networks, and for environmentally safe metal plating. Stable multilayer films of polymeric systems have been fabricated and their activity demonstrated. This approach is expected to lead to the development of functional organic films. Decorated membranes.6 For many years, lipid bilayer membranes have been investigated as models for cell walls. Current research is focusing on active membranes that mimic natural membrane function by including bound proteins, adsorbed colloidal particles, and so on. Mesoscopic organized structures.7 Biomolecular systems that spontaneously organize into crystalline structures with lattice constants in the mesoscopic range are being studied as molecular sieves (S-layers), 8 electrically active arrays (tubules),9 and long-term controlled-release systems (vesicles).10 Biomineralization.11 Biomolecular templates are being studied as nucleation devices for the synthesis of inorganic compounds with unusual structures and high degrees of perfection. Examples include the epitaxial growth of carbonates induced by molluscan shell protein and the intracellular synthesis of CdSe semiconductors. These specific models of contemporary biomolecular materials research have encouraged the panel to examine more speculative possible long-term goals. Some examples are discussed in Section 3 of this report, “Opportunities.” 3   The materials addressed in this report are organized on the molecular to membrane length scales. A report entitled Hierarchical Structures in Biology As a Guide for New Materials Technology (National Academy Press, Washington, D.C., 1994), prepared under the aegis of the National Materials Advisory Board of the National Research Council, concentrated on more complex cellular or extracellular materials. 4   J.G. Tirrell, M.J. Fournier, T.L. Mason, and D.A. Tirrell, Chemical and Engineering News 72:40 (1994). 5   L.H. Dubois and R.G. Nuzzo, “Synthesis, Structure, and Properties of Model Organic Surfaces,” Annu. Rev. Phys. Chem. 60:437 (1992); A. Ulman, Ultrathin Organic Films (Academic Press, Boston, 1991). 6   N. Unwin and R. Henderson, Scientific American 250(February):78 (1984). 7   National Research Council, Hierarchical Structures in Biology As a Guide for New Materials Technology (National Academy Press, Washington, D.C., 1994). 8   U.B. Sleytr and M. Sara, Appl. Microbiol. Biotechnol. 25:83 (1986); W. Baumeister and G. Lembcke, J. Bioenerg. Biomembr. 24:567 (1992). 9   J.M. Schnur, Science 262:1669 (1993). 10   D.D. Lasic, Liposomes: From Physics to Applications (Elsevier, Amsterdam, 1993). 11   Stephen Mann, John Webb, and Robert J.P. Williams, eds., Biomineralization: Chemical and Biochemical Perspectives (VCH, New York, 1989).