Proc. Natl. Acad. Sci. USA Vol. 96, pp. 3479–3485, March 1999 Colloquium Paper

This paper was presented at the National Academy of Sciences colloquium ‘‘Geology, Mineralogy, and Human Welfare,’’ held November 8–9, 1998 at the Arnold and Mabel Beckman Center in Irvine, CA.

Biochemical evolution III: Polymerization on organophilic silica-rich surfaces, crystal–chemical modeling, formation of first cells, and geological clues (biological evolution͞silica͞feldspar͞zeolite͞first cell walls)

JOSEPH V. SMITH*†,FREDERICK P. ARNOLD,JR.‡,IAN PARSONS§, AND MARTIN R. LEE§

*Department of Geophysical Sciences and Center for Advanced Radiation Sources, 5734 South Ellis Avenue, The University of Chicago, Chicago, IL 60637; ‡Advanced Research Systems, 5640 South Ellis Avenue, The University of Chicago, Chicago, IL 60637; and §Department of Geology and Geophysics, University of Edinburgh, Edinburgh EH9 3JW, United Kingdom

ABSTRACT Catalysis at organophilic silica-rich surfaces tides and RNAs, must be protected from photochemical of zeolites and feldspars might generate replicating biopoly- destruction by solar radiation and must not be overly heated. mers from simple chemicals supplied by meteorites, volcanic A stable cell wall is needed to protect the first primitive gases, and other geological sources. Crystal–chemical mod- organism. eling yielded packings for amino acids neatly encapsulated in Part I (1) pointed out that certain inorganic materials have 10-ring channels of the molecular sieve silicalite-ZSM-5- internal surfaces that are both organophilic and catalytic, (mutinaite). Calculation of binding and activation energies for allowing efficient capture of organic species for catalytic catalytic assembly into polymers is progressing for a chemical assembly into polymers in a protective environment. These composition with one catalytic Al–OH site per 25 neutral Si physicochemical features are related to the state of the art for tetrahedral sites. Internal channel intersections and external zeolite catalysts in the chemical industry, the observed prop- terminations provide special stereochemical features suitable erties of zeolite, feldspar (2), and silica minerals, and a for complex organic species. Polymer migration along nano͞ plausible framework for the accretion and early history of the micrometer channels of ancient weathered feldspars, plus Earth’s crust and atmosphere (1). Various materials from the exploitation of phosphorus and various transition metals in zeolite, feldspar, and silica mineral groups were listed as entrapped apatite and other microminerals, might have gen- having surfaces with the capacity to adsorb organic species erated complexes of replicating catalytic biomolecules, leading preferentially over water molecules and catalyze them into to primitive cellular organisms. The first cell wall might have polymers. We focus here on mutinaite, a zeolite mineral been an internal mineral surface, from which the cell devel- recently discovered in Antarctica, which is the natural analog oped a protective biological cap emerging into a nutrient-rich of the ZSM-5/silicalite series of synthetic microporous mate- ‘‘soup.’’ Ultimately, the biological cap might have expanded rials (Note: Microporous does not imply that the pores are of into a complete cell wall, allowing mobility and colonization of micrometer size; indeed the pores in zeolites are generally less energy-rich challenging environments. Electron microscopy than a nanometer across). This type of molecular sieve is based of honeycomb channels inside weathered feldspars of the Shap on a tetrahedral framework containing a three-dimensional granite (northwest England) has revealed modern bacteria, channel system spanned by rings of 10 oxygen atoms (Fig. 1 perhaps indicative of Archean ones. All known early rocks Upper Left and Upper Right). The silica-rich end-member of the were metamorphosed too highly during geologic time to ZSM-5 series, silicalite, is very organophilic, and Al-substituted permit simple survival of large-pore zeolites, honeycombed synthetic relatives catalyze organic reactions at Al–OH re- feldspar, and encapsulated species. Possible microscopic clues ͞ gions. Silicalite provides a useful basis for modeling adsorp- to the proposed mineral adsorbents catalysts are discussed tion͞catalytic processes that would apply in principle, but not for planning of systematic study of black cherts from weakly in detail, to other materials in paper I (1). metamorphosed Archaean sediments. Nonexperts in computer modeling of crystal structures might note the conventions in Fig. 1 Upper Left and Upper Introduction and Summary of Biochemical Evolution: Part Right. Three-dimensional imaging must be idealized and trun- ͞ ͞ ͞ ͞ I. Darwin Oparin Haldane Watson Crick biological evolu- cated. Fig. 1 Upper Left displays 10 oxygen atoms as spheres tion provides a plausible framework for integrating the patchy half the conventional atomic radius of 1.4 Å. All other atoms paleontological record with the complex biochemical zoo of are shown merely by the intersection of spokes. Each tetrahe- the present Earth (literature review: ref. 1). But how could the drally coordinated (T) atom lies at the intersection of four first replicating and energy-supplying molecules have been yellow spokes and each O atom at the intersection of two assembled from simpler materials that were undoubtedly maroon spokes. Fig. 1 Upper Right shows all the O atoms as available on the early protocontinents? Bernal preferred ‘‘life’’ half-size spheres, and the Si and Al types, respectively, of T to begin by catalytic assembly on the surface of a mineral, but atoms as yellow and pink spheres joined by thin grey spokes. all pre-1998 attempts using clays and other minerals to assem- Only four 10-rings are shown lying in the wall of the channel, ble an integrated scheme of physicochemical processes had and you, the reader, must imagine the channel extending up significant weaknesses. Catalysis of organic compounds dis- and down to the surface of the crystal where some adjustment persed in aqueous ‘‘soup’’ requires a mechanism for concen- of chemical bonding is needed. Fig. 1 Upper Right is deliber- trating the organic species next to each other on a catalytic ately tilted slightly with respect to Fig. 1 Upper Left. The substrate. Biochemically significant polymers, such as polypep-

†To whom reprint requests should be addressed. e-mail: smith@geo1. PNAS is available online at www.pnas.org. uchicago.edu.

3479 Downloaded by guest on September 29, 2021 3480 Colloquium Paper: Smith et al. Proc. Natl. Acad. Sci. USA 96 (1999)

FIG. 1. Computer graphics of part of the atomic framework of silicalite͞ZSM-5 with amino acids encapsulated in energetically favored positions. (Upper Left) Tetrahedral framework of silicalite͞ZSM-5 showing a 10-ring channel down the y-axis. Most of the figure consists of spokes linking atom positions. One 10-ring of O atoms is shown by spheres displayed at half the formal atomic radii. See text for explanation: oxygen atoms, maroon spheres and intersection of maroon spokes; tetrahedral (T) atoms, intersection of yellow spokes. Only four 10-rings are shown, whereas a perfect crystal would have an infinite number defining the channel. Also shown are the tilted five-rings. Ten-ring channels present in the plane of the paper are difficult to see without rotation on the video display. (Upper Right) Four glycine molecules in the zwitterion configuration encapsulated in Ϫ ϩ silicalite͞ZSM-5. Glycine consists of a central C atom bonded to two H, one carboxyl COO , and one amine NH3 . The cluster of three molecules near the middle of the near-vertical channel has been optimized to interact mutually by way of hydrogen bonding and to be suspended by van der Waals bonding from the O atoms of the 10-ring channel. The fourth molecule is oriented along a horizontal 10-ring channel. All the framework O atoms are represented by half-size maroon spheres. The tetrahedrally coordinated atoms are represented by small spheres differentiated by color: Si, yellow, Al, pink. The glycine molecule is represented by a stick model with conventional color code: O, red; C, grey; N, blue; H, white. The orientation of the channel system is rotated slightly from that in Upper Left.(Lower Left) Three glycine molecules within a 10-ring channel of silicalite, viewed down the y- axis. Coloring as in Upper Left; silicalite͞ZSM-5 framework shown as tetrahedra (Si, Al) and balls (O); glycine shown as tubes. Note the alignment of the amino acids parallel to the channel and restricted lateral positions within the channel. (Lower Right) Two of the glycine molecules from Lower Left, viewed along the z-axis. Note the ‘head-to-tail’ alignment of the carboxylate group of an amino acid with the amino group of the next amino acid. Once again, the positional constraints on the amino acids in the channel, as well as their parallel alignment with the channel, are emphasized.

conventions for amino acids are given in the Fig. 1 Upper Right Introduction to New Unpublished Studies. This third part legend. integrates the current state of research on biochemical evolu- Downloaded by guest on September 29, 2021 Colloquium Paper: Smith et al. Proc. Natl. Acad. Sci. USA 96 (1999) 3481

tion that will be presented at the Colloquium on Geology, thermodynamic calculation of amino acid synthesis in hot Mineralogy, and Human Welfare. [The second part on weath- water and application to hydrothermal vents (black smok- ered honeycombed feldspars and associated bacteria in a ers) on ocean floor (26); polymerization of various amino modern granite was under preparation as this third part was acids on hydroxylamine and illite mica, with increasing being completed and will be published (57) in the regular part adsorption affinity of oligomers longer than 7-mer (27–29).] of the Proceedings before this paper. Its key contents are given briefly in this paper and are illustrated in Fig. 3.] We begin with Figs. 1 Upper Right, Lower Left, and Lower Right and 2 Upper crystal–chemical modeling of amino acids inside 10-ring chan- and Lower illustrate the current state of chemical modeling of nels of the chosen zeolite, silicalite (Figs. 1 Upper Right, Lower amino acids encapsulated in a silicalite containing one Al substitution for 25 tetrahedral Si. Simulations were carried out Left, and Lower Right and 2 Upper and Lower). The channel ͞ walls are electrically neutral except for arbitrary replacement using the Sorption module within the MSI Cerius 2 program of 4% of the silicon–oxygen tetrahedra by aluminum-oxygen- system (issued by Pharmacopeia, Princeton, NJ). The Consis- hydroxyl catalytic centers. This 1 in 25 replacement yields nice tent Valence Force Field was used for all atoms. graphics and has no particular scientific significance. More- Figs. 1 Lower Left and Lower Right and 2 Upper illustrate the over, this ratio can be varied to increase or decrease the spacing results of packing simulations based on Monte Carlo tech- of catalytic centers along the 10-ring channels and to vary the niques for glycine and histidine molecules encapsulated within electrical forces on adsorbed molecules and the repeat dis- the 10-ring channels of silicalite. It is possible at low pressure tances of the polymers generated by catalytic condensation. to pack 28 glycine molecules per unit cell or eight histidine. Fig. We end with new ideas for generating primitive protocells 1 Lower Left, and its rotated version in Fig. 1 Lower Right, inside the honeycombed weathered surfaces of feldspars [Part demonstrate how the restriction of lateral motion by the II (57)]. Fig. 3 shows scanning-electron micrographs of the channel system, coupled with charge effects at the amino and crystallographically controlled channels in feldspars from the carboxyl ends of the amino acids, assists in orienting them Shap granite, northwest England, together with associated correctly for the production of polypeptides. It can also be seen modern bacteria, as models for speculation on the develop- from these illustrations that one of the chief difficulties of the ment of the first primitive cells. Now to details. standard model for the formation of life, that of achieving Preliminary Simulations of Encapsulation of Amino Acids sufficient concentration of reactants while excluding or min- in Silicalite͞ZSM-5 and Catalytic Generation of Biopolymers. imizing environmental degradation, is overcome. Not only are The crystal–chemical reviews in refs. 1 and 2 are updated by the growing biopolymers protected from outside interference papers in the following areas: and concentrated in the channels, but the limited degrees of freedom in molecular movements assist in orienting them Y crystal chemistry of high-silica materials: Fourier Transform- optimally for polymerization. Raman studies of single-component and binary adsorption Simple molecular mechanics simulations within the SPAR- in silicalite-1 (3); vapor adsorption in thin silicalite-1 films TAN computer package (Wavefunction, Irvine, CA) of various studied by spectroscopic ellipsometry (4); adsorption͞de- model complexes are shown in Fig. 2 Upper and Lower. Fig. 2 sorption of n-alkanes on silicalite crystals (5); adsorption Upper (stereoview) illustrates an adenine hydrogen bound to equilibria of C1 to C4 alkanes, CO2, and SF6 on silicalite (6); the hydroxyl site of the 10-ring channel, with the carboxyl end adsorption of linear and branched alkanes in zeolite sili- of a glycine residue bound to the amino group of the adenine. calite-1 (7); combined quantum mechanical͞molecular me- This complex is correctly oriented for protonation of the chanics ab initio modeling, demonstrating that the most hydroxyl group of the amino acid, followed by the elimination stable Brønsted sites occur in high-silica zeolites (8); simu- of water and the formation of an amide bond between the base lation of adsorption and diffusion of hydrocarbons in sili- and the amino acid. Such a reaction would be facilitated by a calite, demonstrating that a linear hydrocarbon moves more second metal site in the region, and provides one possibility for freely than a branched one, whose CH group becomes a precursor to the autocatalytic biopolymers of the ‘pre-RNA’ locked at a channel intersection (9); adsorption isotherms of world. Electrostatic potential calculations on the system, using linear alkanes in ferrierite— smaller ones, C1–C5, fill the the PM3 semiempirical Hamiltonian within the MOPAC mo- entire pore system, whereas C6 and C7 fit only in a 10-ring lecular orbital package, indicate that this orientation is favor- channel unless forced into an eight-ring channel by pressure able for the proposed reaction. (10, 11); nuclear magnetic resonance of 1H in water ad- Fig. 2 Lower illustrates one possibility of the bonding of an sorbed on silicalite (12); heterogeneity of Brønsted acid sites amino acid to the hydroxyl site of a zeolite-type material. It is in Al-substituted faujasites (13); nuclear magnetic resonance obvious that the nitrogen functionalities of the histidine ring of 17O in silica, albite glasses, and stilbite (14, 15); simulation could form hydrogen bonds. Furthermore, it is also possible to of alkane adsorption in aluminophosphate-5, and calorim- bind the hydroxyl group of the carboxyl functionality to the etry of alkane absorption in high-silica zeolites (16, 17); acid site within the zeolite framework, then dehydrate and hydrophobic properties of all-silica beta zeolite (18); struc- form a covalent bond between the surface and the amino acid. tural location of sorbed p-nitroaniline in silicalite͞MFI This process is analogous to the functionalized glass or plastic molecular sieves from x-ray powder diffraction and 29Si beads used in commercial DNA or protein synthesis, where the Magic Angle Spinning–NMR (19); nature, structure, and polymer chain grows away from the supported terminus. composition of hydrocarbon species obtained by oligomer- Reaction with hydronium ion, presuming mildly acidic media, ization of ethylene on acidic H-ZSM-5 molecular sieve (20): would enable cleavage of the chain and would release the Y surface chemistry of various minerals: coordination models peptide into solution. In passing, it should also be noted that for simple surfaces of oxide and silicate minerals (21); the the amino terminus of the amino acid, which is facing away role of intragranular microtextures and microstructures in from the viewer, is oriented along the axis of the channel and chemical and mechanical weathering, direct comparisons of hence, in analogy to Fig. 1 Lower Right, is oriented optimally experimentally and naturally weathered alkali feldspars for further reaction. (22); Speculations on Biochemical Evolution Currently Under Y synthesis: RNA-catalyzed nucleotide synthesis of a pyrimi- Evaluation. These illustrative results give confidence for spec- dine (23); conversion of amino acids into peptides at 373 K ulations that a microporous aluminum-substituted silica ma- and pH 7–10 on (Ni, Fe)S surfaces (24), synthesis of terial with mainly hydrophobic channels and widely spaced glycylglycine dipeptide in the presence of kaolin clay and Al–OH catalytic centers might act as a sausage machine for zeolites of Linde Type A, faujasite, and beta types (25); production of biopolymers that became assembled into pro- Downloaded by guest on September 29, 2021 3482 Colloquium Paper: Smith et al. Proc. Natl. Acad. Sci. USA 96 (1999)

FIG. 2. Computer graphics of part of the atomic framework of silicalite͞ZSM-5 with amino acids encapsulated in energetically favored positions. (Upper) Stereopair of 10-ring channel of silicalite, showing a hydrogen-bound adenine–glycine complex itself hydrogen-bound to an acid site of the framework. Some framework atoms removed for clarity. This stereopair illustrates the ability of the zeolitic material both to accommodate large biopolymer precursors and to provide sites at which reactions may occur. (Some students initially have difficulty viewing stereopairs. If you have this problem, try putting a bright spot at the red atoms at the extreme top right and bottom left. Your brain should then be able to make your eyes swivel to achieve stereo with the left eye seeing the left dot. This contrasts with the cross-eye technique used in some biological modeling.) (Lower) Histidine and water molecules in silicalite. Histidine was chosen for modeling because its imidazole ring can switch electronic states readily to catalyze Downloaded by guest on September 29, 2021 Colloquium Paper: Smith et al. Proc. Natl. Acad. Sci. USA 96 (1999) 3483

tocells in protected honeycombs in weathered feldspars. Var- logic time into granitic metamorphic rocks. Hence, we are ious new matters are being evaluated currently from the comfortable in proposing that zeolites and feldspars would viewpoint of physical and chemical processes and are modeled have coexisted on the early Earth, for which only the resultant in detail for later publication: granitic metamorphic rocks have been seen so far. Hence we ͞ ͞ Y can suggest for discussion purposes that a zeolite silica First, channel intersections may prove important for stere- altered feldspar sausage machine fed a range of biological ochemical control of larger functional groups, especially at polymers into feldspar honeycombs. As discussed above, in- the end of a biopolymer. The intersection of an internal termingling of polymers, generation of P-bearing energy- channel with the outer surface should be even more impor- transporting species from apatite, and hydrogen-bond cou- tant and indeed might be considered as an anchor for a pling between organic species and silica-rich walls, would have polymer that projects outwards into a ‘soup.’ Y generated primitive protocells. To conclude the evolution into Second, after outward migration from an internal channel, the first organisms, a cap between the dangerous outer regime the first biopolymers would begin to coil up like a snake and of ‘soup’ and the inner protected world might have expanded in certain places, such as a tapered tube in a honeycombed to completely enclose the protocell so that it could swim into feldspar approximately 5 to 100 nanometers across, would the future. Part IV, under preparation, will show graphics begin to interact closely with the aluminosilicate surface. Y illustrating the scientific factors underlying these flights of Third, various biopolymers of different types might begin to fancy about cell formation. interact and begin the evolution toward a protobacterium. Y Conclusion. We conclude with matters of specific geological Particularly important would be the first generations of import. From the humanistic viewpoint, it would be extremely persistent energy-generating species containing phosphorus significant if the early forms of life had left behind some and electron-transferable transition metals. Very important physicochemical evidence of their existence. The current is that K-rich feldspars from granites contain micrometer ͞ carbon-isotope evidence of bulk samples is indicative of some inclusions of the calcium—phosphate–hydroxide halide kind of early biological evolution, but has no particular import mineral apatite and transition-metal oxides, including ilmen- for the atomic-level ideas presented above. A review of the ite, spinel, and hematite, which might well be the primary geological evidence indicates that at least most and perhaps all reservoirs of these key elements. Y of the early Archean rocks have been metamorphosed to a high At some stage, a protocell lining inside an aluminosilicate enough level that all volcanic rocks have recrystallized. There tube might develop a bilipid lining that would extend into a can be little doubt that volcanoes would have been pumping cap, ultimately allowing detachment from the silicate and out ash containing crystals of K-feldspar and silica minerals. free motion through a soup. Again, one might imagine a By analogy with modern conditions, much of the ash would sausage machine popping off a free cell as the remaining have been converted into zeolite beds, and there might well protocell reconstituted itself ready for generation of the next have been zoned beds of zeolite minerals interacting with salty free cell. Schematic graphics are being envisaged along with lakes sloshed by tides and impacts. Some K-feldspar and zeolite ideas for chemical bonding schemes. crystals would have been exposed to an acidic rain, and Y All these processes would involve subtle effects related to ͞ honeycombed and grooved faces should have occurred (1, 2). diurnal and annual temperature cycles and wet dry cycling Primitive molecules would certainly have been available dis- driven both by solar radiation and lunar tides that would persed in ‘soups’, as envisaged by many writers (1). change the spatial distribution of chemical forces across Here are some ideas for testing whether minerals produced mineral surfaces. Ideas are not developed enough so far to by metamorphic recrystallization of earlier igneous origin warrant further description here. might have retained some specific signature indicative of subtle Mineralogical Observations and Speculations: Electron biological processes involving feldspar, zeolite and silica min- Microscopy of Honeycombed Weathered Feldspars—Bacteria erals: and Protocells. Turning now to mineralogical information, Fig. Y Ancient cherts (silica–hydroxyl-rich aggregates) range in 3 contains four scanning-electron micrographs of the crystal- color at least from black to brown, red, and orange-yellow. lographically controlled honeycomb weathering on a modern At least some of the color variation must result from surface of a K-feldspar from the Shap granite (30). Particularly transition metals, especially Fe and Mn, at different redox important are the micrometer-scale sausage shapes inter- states. Might some carbonaceous species have survived in preted as electron scattering from bacteria, somewhat the black cherts? If so, would careful analysis reveal organic shrunken from interaction with the electron beam. Many have breakdown products specific to primary biocatalytic precur- no particular orientation with respect to the feldspar, but the sors? bacterium in Lower Right is interpreted as sitting neatly in a Y Because early organisms would have needed P and various crevice. The near correspondence between the segmentation transition metals, would their absence or low abundance in of the proposed bacterium and the spacing of the feldspar the metamorphosed siliceous rocks be indicative of early honeycomb is intriguing. Perhaps it may ultimately be possible biological scavenging by organisms that escaped into the to quantify the original chemical linkages between the inor- ‘soup’? ganic substrate and the unshrunken bacterium and to use them Y Particularly challenging, because of the possibility of com- for modeling the above ideas. plete failure, would be a hunt for x-ray diffraction evidence Coupling the catalytic production of polymers at the nano- of surviving Si-rich molecular sieves. Silicalite and other meter scale with bacteria at the micrometer scale is plausible large-pore zeolites have strong low-angle diffractions that in the geologic context, but requires many flights of imagina- would stand out in low-background patterns obtained with tion and a lot of faith. On the present Earth, volcanic glass synchrotron x-rays, even at a concentration below 1%. transforms to zeolites in continental basins and ocean floors; the zeolites become metamorphosed to feldspars; and the Since the review in ref. 1, the following geological͞biological whole mineralogical assemblage becomes converted over geo- publications have been added:

the making and breaking of bonds, as well as to provide several potential sites for binding and reactivity. The histidine molecules are shown by a ball-and-stick arrangement and are colored as in Upper. The water molecules are represented by a bent bicolor rod with two white ends representing H, and the red center represents O. The framework is represented by tetrahedra whose shared vertices are at O positions. A further reason for choosing histidine is its prevalence as a metal-binding site in modern proteins, undoubtedly an important function in the prebiotic world. Downloaded by guest on September 29, 2021 3484 Colloquium Paper: Smith et al. Proc. Natl. Acad. Sci. USA 96 (1999)

FIG. 3. Four scanning-electron micrographs of weathered feldspar from the Shap granite. (Upper Left) Resin cast of honeycomb texture. The cast is somewhat flexible, so that some of the etched dislocations appear to be curved, although they were almost straight in the original feldspar, which has been dissolved away in HF. (Upper Right) A near-planar surface close to bar601 with a trace of etched dislocations running horizontally and vertically across the image with ellipsoidal bacteria, some in strings like sausages hanging in a U.K. butcher’s shop. (Lower Left) More deeply weathered surface showing occasional traces of etched dislocations, with sausage-shaped bacteria. (Lower Right) Detail of honeycomb on the 001 surface of a feldspar honeycomb. The holes are etch pits formed on paired outcrops of dislocations that formed on exsolution lamellae. The bacterium, although perhaps partly shrunken by the instrument vacuum, is segmented on a scale remarkably similar to the spacing of the etch pits. Details of the feldspar weathering are given in Part II (57).

Y stardust and meteorites: Photochemical evolution of inter- biogeochemical cycles͞prebiotic Earth and mineral cycles͞ stellar͞precometary organic material (31); silica-rich micro- theoretical perspectives on the origins of life (Oparin– meter objects in a carbonaceous chondrite (32); Haldane theory, Cairns–Smith ideas on clays and life, pyrite, Y planetary impact processes: Survival of amino acid in large and the origins of life, ‘‘thioester world’’) (43); intracellular comet impacts (33); bacteria in protozoa (44); plant cell wall proteins (45); gene Y early geologic events on Earth: Nitrogen fixation by volcanic molecular sequences of Archea and details of thermophiles lightning (34); redox state of upper-mantle peridotites under and cold-dwelling types (46); hydrogen consumption by the ancient cratons, and possible equilibrium of diamonds methanogens on the early Earth (47); genome sequences with methane-nitrogen-rich fluids (35); new revised Pb-ages from a dozen bacteria and a yeast fit with a three-kingdom of Greenland gneisses at 3.65–3.70 instead of earlier 3.85 world (48); ‘Eukaryotes are suggested to have arisen through gigayear-before-present (36); interpretation of geologic ev- symbiotic association of an anaerobic strictly hydrogen- idence in favor of plate-tectonic processes in the Archean dependent strictly autotrophic archaebacterium (the host) era (37); interpretation of Archean magmatism and defor- with a eubacterium (the symbiont) that was able to respire, mation in nonplate tectonics terms (38); details of Precam- but generated molecular hydrogen as a waste product of brian clastic sedimentation that partly match and partly anaerobic heterotrophic metabolism,’ (49); bacteria in sed- differ from recent processes (39); evidence from mature iments (50); quartz arenites in various Archean shields of stable conti- Y chert: The following papers about the siliceous nodules nental crust containing quartz-rich granitoid rocks (40); known as chert and about related siliceous materials should microbiological evidence for Fe(III) reduction to Fe(II) on be useful in thinking about how to characterize ancient early Earth, and support for earlier idea that Fe(III) was a chert: Evidence of volcanic origin of chert in the Permo- more likely electron acceptor than S in microbial metabo- Triassic Sydney Basin (51); growth of chalcedony by assem- lism (41), birth of the Earth’s atmosphere, and the behavior bly of short linear polymers with silica monomers (52); and fate of its major elements (42); growth fault control of Ϸ3.5 Gybp Early Archaean cherts, Y bacteria, cell walls, various matters: Text on bacterial bio- barite mounds, and chert-barite veins, North Pole Dome, geochemistry, with final chapter on origins and evolution of Eastern Pilbara, Western Australia, carbonaceous aggre- Downloaded by guest on September 29, 2021 Colloquium Paper: Smith et al. Proc. Natl. Acad. Sci. USA 96 (1999) 3485

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