Life As a Nanoscale Phenomenon We Thank Dr. Erik
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Reviews S. Mann DOI: 10.1002/anie.200705538 Artificial Life Life as a Nanoscale Phenomenon** Stephen Mann* Keywords: cells · membranes · miniaturization · nanoscience · proteins Angewandte Chemie 5306 www.angewandte.org 2008 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim Angew. Chem. Int. Ed. 2008, 47, 5306 – 5320 Angewandte Cellular Life Chemie The nanoscale is not just the middle ground between molecular and From the Contents macroscopic but a dimension that is specifically geared to the gath- ering, processing, and transmission of chemical-based information. 1. Introduction—The Significance of Nanoscience 5307 Herein we consider the living cell as an integrated self-regulating complex chemical system run principally by nanoscale miniatur- 2. Limits to Cellular Life 5309 ization, and propose that this specific level of dimensional constraint is critical for the emergence and sustainability of cellular life in its 3. Nanometer-Thin Boundaries 5311 minimal form. We address key aspects of the structure and function of 4. Globular Nanoobjects 5313 the cell interface and internal metabolic processing that are coextensive with the up-scaling of molecular components to globular nanoobjects 5. Modular Assemblyand (integral membrane proteins, enzymes, and receptors, etc) and higher- Nanomotors 5315 order architectures such as microtubules, ribosomes, and molecular 6. Nanoscience and Artificial Life 5316 motors. Future developments in nanoscience could provide the basis for artificial life. 7. Conclusions 5317 1. Introduction—The Significance of Nanoscience direct consequences of the development of nanoscience. Nanoscale miniaturization is of immediate relevance partic- Given that nanoscience has grown exponentially over the ularly to a large and active community concerned with storage last decade, producing important contributions at the inter- density, functional displays and screening protocols, isolation faces between chemistry, physics, biomedicine, and analytical of molecules and their conjugates, and device integration. science, it seems expedient to ask why this research area is so Moreover, collective properties such as super-hydrophobic- scientifically distinguished. It is now over twenty years since ity,[17] plasmonic coupling,[18] and magnetic/electronic behav- certain semiconductors[1,2] and iron oxides[3, 4] were shown to ior of devices[19,20] can be modulated by miniaturization of exhibit markedly different electronic and magnetic proper- structural components and fabrication of superlattice assem- ties, respectively, compared with corresponding bulk materi- blies. And from a bottom-up perspective, the ability to als when confined to length scales of a few nanometers. This synthesize complex nanoscale objects with hybrid structure was followed some years later by innovations in scanning and composition is seen as a major challenge and opportunity tunneling microscopy that enabled individual atoms to be in the chemistry of organized matter.[21] manipulated and positioned into quantum structures,[5,6] and The very large scope of the above activities indicates how the discovery of nanotubular forms of carbon.[7] Together, nanoscience has shifted in significance in recent years from an these important advances justify the commonly held raison initial focus on the confinement-induced modification of detre of nanoscience that confinement is of key importance intrinsic properties towards the exploration of extrinsic in determining the intrinsic properties of structured matter. properties associated with miniaturization. This transition But size alone is not the defining parameter of many brings nanoscience close to biology, although the engineering nanoscale-derived effects. More generally, these phenomena challenges associated with reduction in length scale are very are determined by the surface area to volume ratio, with the different from the problems involved with the amplification consequence that particles with constant volume but variable of molecular-based architectures. It is self-evident that nano- shape can differ significantly in their confinement properties. scale miniaturization is a principle attribute of biochemistry, Thus, much work continues to be undertaken on the synthesis and it follows that the evolution of life was contingent on the of nanoparticles in the form of rods,[8] plates,[9] and multipodal emergence and integration of multiple forms of nanostruc- structures,[10,11] which have high shape anisotropy. Similarly, tured objects (Figure 1, Table 1). These remarkable architec- structure as well as size, plays a key role in determining the tures serve as miniaturized components of complex process- metallic/semiconducting properties of carbon nanotubes,[12] ing systems, and given the molecular basis of metabolism it is and the depletion of crystal defects, moderation of surface pertinent to ask why these structures are as large as they are; roughness, and selected expression of crystal faces[13–16] are that is, what key properties are associated with nanoscale additional parameters that contribute significantly to the objects that are absence in small molecules, and which continuing surge of activity in nanoscience today. Taking into account the above considerations, it remains nevertheless true that only a limited number of materials [*] Prof. S. Mann Centre for Organized Matter Chemistry exhibit significant and useful changes in their intrinsic School of Chemistry, University of Bristol properties as a function of scale. Yet nanoscience remains Bristol BS8 1TS (UK) wide ranging and eclectic. This is because natural progres- Fax : (+ 44)117-929-0509 sions in the science and engineering of miniaturization, as well E-mail: [email protected] as structural amplification in supramolecular chemistry, are [**] We thank Dr. Erik Dujardin, Toulouse, for designing the frontispiece. Angew. Chem. Int. Ed. 2008, 47, 5306 – 5320 2008 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim 5307 Reviews S. Mann Figure 1. Examples of biological nanoobjects (see Table 1 for details and other examples): a–c) nanoparticles (a, globular (myoglobin); b, hollow/ core–shell (ferritin); c, wrapped (nucleosome)); d–f) helical nanofilaments (d, triple coiled-coil (collagen); e, nanoparticle chain (F-actin);f, double-strand (DNA); g) nanotube (membrane protein (porin)); h,i) nanopods (h, l-shaped (tRNA)), i, Y-shaped (IgG)); j) nanobarrel (chaperonin groEL/ES complex); k) nanocage (clathrin); l) bacterial S-layer. Figures adapted from: c) ref. [28]; d) http:///www.med.unibs.it/ ~ marchesi/pps97/ course/section11/assembli.html; e) ref. [79]; f) http://www.nmr.cabm.rutgers.edu/photogallery/proteins/htm/page26; g) http://www.palaeos. com/Eukarya/Images/BetaBarrels.jpg; h) http://www.biochem.umd.edu/biochem/kahn/teach_res; i) http://www.sci.sdsu.edu/TFrey/Chem365/ Proteins/AntibodyStructCh365.htm; j) http://www.rbvi.ucsf.edu/Outreach/Workshops/UCSF-Fall-2005/07-VolumeData/tutorial/chaperonin.html; k) ref. [73]; l) ref. [60]. ultimately lead to sustainable chemical systems capable of self-renewal and replication? Stephen Mann is Professor of Chemistry and Director of the Centre for Organized Matter In this Review, we propose that the correlation between Chemistry in the School of Chemistry at the biology and nanoscience is of deeper significance than University of Bristol, UK. He is interested in generally acknowledged, and that the long-standing legacy the self-assembly, biomimetic synthesis, and of nanoscale phenomena lies in the emergence of sustainable chemical emergence of complex forms of systems of chemical complexity. We consider the living cell as organized matter across extended length an integrated self-regulating machine run by nanoscale scales, and has published over 350 papers and a book entitled Biomineralization: Prin- miniaturization, and propose that this specific level of ciples and Concepts in Bioinorganic Materi- miniaturization is critical for the emergence and sustainability als Chemistry. He has obtained numerous of the cell. We base this notion on the grounds that the awards, including most recently the RSC J. regulation and optimization of systems based primarily on the Chatt Medal and Lectureship (2007). He is input and reactivity of small molecules necessitate nanoscale a Fellow of the Royal Society and a member of the editorial and advisory operations and transformations to specifically facilitate the boards of several journals including Advanced Materials and Angewandte gathering, processing, and transmission of chemical informa- Chemie. tion. Given the molecular nature of chemical systems, this 5308 www.angewandte.org 2008 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim Angew. Chem. Int. Ed. 2008, 47, 5306 – 5320 Angewandte Cellular Life Chemie Table 1: Biological nanoobjects. 2. Limits to Cellular Life Type Examples Size [nm] The living cell can be considered as a spatially enclosed nanoparticles complex chemical system that is self-maintained and self- globular (many proteins) > 2.5 hollow apoferritins 12 generated internally by metabolic processes acting under the lumazine synthase 15 flow of genetic information. Cellular components are pro- cowpea chlorotic mottle 28 duced, transformed, and arranged within the system, and this virus process—often referred to as autopoiesis[22]—is considered a core–shell lipoproteins (LDL) 20 necessary, and possibly sufficient, condition of life.[23] The cell ferritins 8 (core) + 4 (shell) is organized not only in the form of physically ordered wrapped nucleosomes 11 structures