A New Molecular Window on Early Life

Andrew H. Knoll [HN14] *

For generations, the PrecambrianCambrian boundary [about 544 million years ago (Ma)] formed paleontology's Great Divide, separating the tractable record of a familiar biology from an earlier Terra Incognita populated mostly out of the imagination [HN1]. Although this boundary persists as an important benchmark for animal evolution (1), the discovery and elucidation of the Precambrian fossil record [HN2] have shown it to be a Maginot line (2) for the history of life as a whole. The line of paleontological frustration didn't disappear--it merely receded by nearly 2 billion years to the boundary between the Archean and Proterozoic eons [HN3]. Proterozoic (2500 to 544 Ma) sedimentary rocks are relatively widespread, usually little altered, and occasionally replete with morphological and chemical remnants of a familiar, if largely microscopic, biota. In contrast, the Archean (>2500 Ma) world has remained a shadow land in which "probably" and "maybe" qualify nearly all paleobiological interpretations until now, that is. On page 1033 of this issue, Brocks et al. [HN4] (3) report molecular fossils that bring unprecedented clarity to the late Archean biosphere, dramatically lengthening both the geological record of eukaryotic biology and the list of questions we need to ask about early evolution.

A mountain of iron. The discovery of cyanobacterial biomarker molecules in late Archean rocks in the Hamersley Range, Western Australia, bolsters the hypothesis that photosynthesis provided the oxidizing power to precipitate the ~2500 Ma Hamersley iron formation.

CREDIT: (TOP) A. H. KNOLL

Biomarker compounds are geologically stable molecules, mostly lipids, of known biosynthetic origin [HN5]. Biomarker geochemistry is a standard tool in petroleum exploration (4), but until now, biomolecules older than 1700 Ma (5) were unknown. Nor did conventional wisdom encourage prospects of finding earlier biomolecules, because the average Archean sedimentary rock has been heated to temperatures thought to destroy biomarkers. Brocks et al. wisely ignored average rocks and focused instead on exceptionally preserved 2700 Ma shales from northwestern Australia [HN6] that are renowned for their high organic content (see image above). Consequently, Brocks et al. have extended the molecular fossil record by 1 billion years.

In molecular paleontology, contamination is an issue to be taken seriously, and so Brocks and colleagues painstakingly executed laboratory procedures designed to eliminate the possibility that younger biomarkers migrated into their Archean rocks. Room for doubt has, accordingly, been markedly reduced, and at a minimum, naysayers must go beyond curmudgeonliness to explain the complex pattern of biomarker abundance and distribution identified by Brocks and co-workers, which cannot easily be explained by fluid migration or drilling contamination.

Accepting an Archean age for the biomarkers, what do they tell us about early biology? First, they confirm that cyanobacteria lived in Archean environments. Cyanobacteria [HN7] are the microscopic heroes of Earth history--primary producers, life's great ecological liberators, and source of the oxygen that transformed our planetary surface. Archean microfossils, stromatolites, and carbon isotopes [HN8] have all been interpreted in terms of cyanobacterial biology (6), but although all of these features are consistent with a cyanobacterial origin, none requires that cyanobacteria existed in the Archean. In a recent paper in Nature, Summons et al. (7) show that the 2-methylhopanes found in sediments derive from 2-Me-bacteriohopanepolyols, membrane lipids synthesized in large quantities only by cyanobacteria. Therefore, the extraction of 2-methylhopanes from 2700 Ma rocks by Brocks et al. provides independent geochemical evidence for the antiquity of cyanobacteria and points the way toward tests of a still earlier origin. Morphological fossils show that even the shallowest branches of the cyanobacterial tree had diverged by 2100 Ma (8). Thus, cyanobacteria stand as prime targets for studies of molecular evolution.

Remarkably, the late Archean biomarkers also include steranes, sedimentary molecules derived from sterols [HN9]. A few bacteria incorporate sterols into their membranes, and a subset of these are capable of de novo sterol biosynthesis (9). But no prokaryotes [HN10] are known to form the more elaborate sterols that were precursors of the C28-C30 steranes extracted by Brocks et al. Archeae also have distinctly different membrane systems from Eucaryotes [HN11] and are not known to synthesize sterols. In phylogenies based on ribosomal RNA genes, a very long branch connects eukaryotes to the Archeae (see the figure below) (10), and a host of phenotypic characters separate the domains. Thus, although the discovery of Brocks et al. indicates that a key attribute of eukaryotic physiology had evolved by 2700 Ma, we can make only limited inferences about the overall biology of the organism that synthesized the sterols. Nonetheless, the early appearance of eukaryotic attributes directs new attention to the immense interval between the divergence of the Eucarya and their rise to ecological and taxonomic prominence 1200 to 1000 Ma (see diagram) (11). Explanations based on biological innovation ("just add sex") have been favored in recent years, but these require careful rethinking, with more attention paid to possible environmental facilitation.

Trimming the tree. The Universal Tree depicts the phylogenetic relationships of extant organisms, as inferred from sequence comparisons of ribosomal RNA genes (10). The boxed dates indicate the minimum age of selected branches, based on paleontological and biogeochemical data. New biogeochemical constraints reported by Brocks et al. (3) are shown in orange [HN13].

In a now classic model of atmospheric evolution, geochemists have postulated that oxygen concentrations grew from extremely low to nearly modern levels about 2200 to 2300 Ma (12). But molecular oxygen is required for sterol synthesis, and independent isotopic evidence connects methanotrophic bacteria that depend on oxygen to late Archean ecosystems (13). Thus, regardless of the circumstances of early Archean Earth, biogeochemical observations suggest that by the late Archean, oxygen had begun to accumulate in the atmosphere, perhaps reaching levels sufficient for aerobic respiration by single cells (about 1% of present-day values), although probably not much more (12, 14). Recent models of Proterozoic ocean chemistry also suggest that the partial pressure of oxygen, PO2, approached modern levels only near the end of the Archean (1, 15), further emphasizing the need to consider a protracted, multistage history of atmospheric chemistry [HN12].

Knowledge of Archean life and environments remains sketchy, but the discoveries of Brocks et al. bolster confidence that, like the Precambrian-Cambrian boundary before it, the paleontological barrier at the Proterozoic-Archean boundary is destined to fall. This time the advance will be driven by innovative biogeochemistry tied to careful field studies of Archean sedimentary rocks (16).

References and Notes

  1. A. H. Knoll and S. B. Carroll, Science 284, 2129 (1999).
  2. The Maginot line was the line of defense built before World War II to keep the Germans from invading France. Claimed to be impenetrable, it quickly proved ineffectual when invasion began.
  3. J. J. Brocks, G. A. Logan, R. Buick, R. E. Summons, Science 285, 1033 (1999).
  4. K. E. Peters and J. M. Moldowan, The Biomarker Guide (Prentice-Hall, Englewood Cliffs, NJ, 1993).
  5. R. E. Summons, T. G. Powell, C. J. Boreham, Geochim. Cosmochim. Acta 52, 1747 (1988) [GEOREF].
  6. J. W. Schopf, in Early Life on Earth, S. Bengtson, Ed. (Columbia Univ. Press, New York, 1994), pp. 193-206 [publisher's information].
  7. R. E. Summons, L. L. Janke, J. M. Hope, G. A. Logan, Nature 400, 554 (1999).
  8. S. Golubic, V. N. Sergeev, A. H. Knoll, Lethaia 28, 285 (1995) [GEOREF].
  9. G. Ourisson, M. Rohmer, K. Poralla, Annu. Rev. Microbiol. 41, 301 (1987) [Medline].
  10. C. R. Woese, O. Kandler, M. Wheeler, Proc. Natl. Acad. Sci. U.S.A. 87, 4576 (1990) [Medline].
  11. A. H. Knoll, Science 256, 622 (1992) [Medline].
  12. R. Rye and H. D. Holland, Am. J. Sci. 298, 621 (1998) [GEOREF]. For a contrasting view, see H. Ohmoto [Geology 24, 1135 (1996)] [abstract].
  13. J. M. Hayes, in Early Life on Earth, S. Bengtson, Ed. (Columbia Univ. Press, New York, 1994), pp. 220-236 [publisher's information].
  14. B. Rasmussen and R. Buick, Geology 27, 115 (1999) [abstract].
  15. D. E. Canfield, Nature 396, 450 (1998) [GEOREF].
  16. R. Buick, B. Rasmussen, B. Krapez, Am. Assoc. Petrol. Geol. Bull. 82, 50 (1998) [GEOREF].

The author is at the Botanical Museum, Harvard University, Cambridge, MA 02138, USA. E-mail: aknoll@oeb.harvard.edu

HyperNotes
Related Resources on the World Wide Web

General Hypernotes

 
The University of California Museum of Paleontology (UCMP) presents extensive Web exhibits about the phylogeny of living and fossil organisms, geology and geologic time, and evolutionary theory.
The Internet Resource Guide for Zoology from the Zoological Record includes links to Web resources on phylogeny and evolution and paleontology.
The U.S. Geological Survey Paleontology Web site provides an introduction to fossil groups, a glossary, and a selection of Internet resources on paleontology and related disciplines.
The Department of Geology and Geophysics, University of Calgary, presents a geologic time scale. K. Magruder, Oklahoma Baptist University Planetarium, Shawnee, provides a detailed geological column for an Earth sciences course.
The Royal Tyrrell Museum, Midland Provincial Park, Alberta, Canada, presents the fossil encyclopedia and other paleontological resources.
The Dawn of Animal Life is an online exhibit presented by the Miller Museum of Geology, Queen's University, Kingston, Ontario, Canada.
P. Gore, Georgia Perimeter College, Clarkston, presents lecture notes and links to Internet resources for a historical geology course.
Lecture notes and other resources are presented for a course on the history of life offered by the Department of Geosciences, San Francisco State University. A geologic time scale Web page provides links to Internet resources for each period.
B. Walsh, Department of Ecology and Evolutionary Biology, University of Arizona, provides an overview of the origins of life in lecture notes for a biology course for nonmajors.
P. Olsen, Lamont-Doherty Earth Observatory of Columbia University, provides lecture notes on the origin and early evolution of life for a course on dinosaurs and the history of life.
For a course on evolutionary biology, D. Rand, Department of Biology, Brown University, Providence, RI, provides lecture notes on the origin of life and the fossil record.
The September-October 1995 issue of American Scientist had an article by C. de Duve titled "The beginnings of life on Earth."
The 25 June 1999 issue of Science was a special issue on evolution. It included a news article by Richard Kerr titled "Early life thrived despite earthly travails."
Palaeontologia Electronica is a peer-reviewed online journal of paleontology. The principal objective of the journal is to provide instant, free, and global access to the latest developments in paleontology and related fields. The journal has several mirror sites.

 

Numbered Hypernotes

  1. The online Funk and Wagnalls Encyclopedia provides overviews of the Precambrian and the Cambrian, as well as a general introduction to paleontology. R. Freeman-Lynde, Department of Geology, University of Georgia, presents lecture notes on the Precambrian-Paleozoic boundary for a course on historical geology. J. Werner, Department of Geology, University of Illinois, presents lecture notes on the early history of life and Precambrian and Cambrian life for a geology course on the history of life. J. B. Bennington, Department of Geology, Hofstra University, Hempstead, NY, provides lecture notes on the Precambrian-Cambrian transition for a course on historical geology. The Hooper Virtual Natural History Museum, Ottawa-Carleton Geoscience Centre, presents an online exhibit on the Cambrian explosion of life. The International Subcommission on Cambrian Stratigraphy presents a Virtual Visit to the Cambrian World. The March-April 1997 issue of American Scientist had an article by D. Erwin, J. Valentine, and D. Jablonski titled "The origin of animal body plans" that includes sections on Neoproterozoic and Cambrian life.
  2. H. Hoffmann, Department of Geology, McGill University, provides a geologic time scale of the Precambrian. P. Gore presents lecture notes on the Precambrian for a historical geology course. W. Huff, Department of Geology, University of Cincinnati, provides lecture notes on Precambrian geology and life for a geology course. L. McKenna, Department of Geology, University of Kansas, provides lecture notes on Precambrian life for an Earth history course. The Miller Museum of Geology offers a presentation on the Precambrian Ediacaran biota.
  3. UCMP presents introductions to the Archean era and the Proterozoic era. R. Gastaldo, Department of Geology, Colby College, Waterville, ME, presents an overview of Archean paleobiology in lecture notes for a historical geology course. D. Haywick, Department of Geology and Geography, University of South Alabama, Mobile, offers lecture notes on Archean geology for an Earth history course. J. B. Bennington presents lecture notes on the Archean eon and the Proterozoic eon for a course on historical geology. R. Freeman-Lynde presents lecture noes on Archean and Proterozoic tectonics and Archean and Proterozoic life for a course on historical geology.
  4. J. Brocks, G. Logan, and R. Summons are at the Australian Geological Survey Organisation, Canberra. Brocks and R. Buick are in the School of Geosciences, University of Sydney, Australia.
  5. A definition of biomarkers is provided by the DGSI Total Quality Geochemistry Web site. UCMP offers a presentation on molecular fossils. The Biomarker Handbook, made available by Pattern Recognition Associates, offers an introduction to biological markers in petroleum products. A description of a research project on biomarkers is provided by the Newcastle Research Group, University of Newcastle upon Tyne, UK.
  6. Geological and tectonic maps of western Australia are provided by the Geological Survey of Western Australia; the samples studied by Brocks et al. were taken from the Pilbara Craton region near Wittenoom in northwestern Australia. The Mining Technology Web site provides a presentation on the Hamersley Iron Province in the Pilbara Region of western Australia. A conference paper titled "Geophysical architecture of the Australian continent" by B. Drummond, R. Shaw, and S. Cox is made available by the Australian Geodynamics Cooperative Research Centre.
  7. S. Jansen's Filamentous Marine Cyanobacteria Web site provides an introduction to cyanobacteria. D. Krempels, Department of Biology, University of Miami, provides an introduction to the cyanobacteria. UCMP presents information on the cyanobacteria and their fossil record.
  8. The Hooper Virtual Natural History Museum offers a presentation on stromatolites. R. Arculus, Geology Department, Australian National University, Canberra, discusses stromatolites in lecture notes on the evolution of life for an Earth systems course. D. Sumner, Division of Geological and Planetary Sciences, California Institute of Technology, offers a presentation on Archean microbialites. UCMP provides an introduction to microfossils and information about the fossil record of bacteria. The 29 Jan 1999 issue of Science had a report by M. Rosing titled "13C-depleted carbon microparticles in >3700-Ma sea-floor sedimentary rocks from west Greenland" about sedimentological and geochemical evidence indicating a biogenic origin of the carbon forming the graphite globules. The ABC News Web site offers an article about Rosing's research.
  9. Steranes and sterols are defined in the glossary provided by Pattern Recognition Associates. The section on types of biomarkers in the Biomarker Handbook discusses steranes and related products.
  10. D. Krempels provides an introduction to the prokaryotes. K. Todar, Department of Bacteriology, University of Wisconsin, presents an introduction to the biological identity of prokaryotes for a bacteriology course. Neactica, an Internet natural history guide, provides an introduction to the Archaea and links to relevant Internet resources.
  11. The Tree of Life from the University of Arizona provides an introduction to the eukaryotes. UCMP provides an introduction to the Eukaryota. K. Miller, Department of Geological Sciences, University of Texas at El Paso, discusses prokaryotes and eukaryotes and the evolution of Precambrian life in lecture notes for a historical geology course.
  12. UCMP discusses atmospheric oxygen levels in a presentation on the stratigraphy of the Proterozoic era. K. Miller provides lecture notes on Precambrian atmosphere, oceans, and life for a course on historical geology. M. Palmer provides lecture notes on the first oceans and atmosphere for an environmental geoscience course at Bristol University, UK. For a course on global change, T. Killeen, Department of Atmospheric, Oceanic and Space Sciences, University of Michigan, provides lecture notes titled "From chemical to biological evolution: The impact of life on Earth systems" and lecture notes titled "Evolution of the atmosphere: Structure and composition." G. Shields makes available on the Web an article titled "Oxygen pulse and the evolutionary expansion of the metazoans."
  13. The UCMP Phylogeny of Life Exhibit provides an introduction to the three domains of life: Bacteria, Archaea, and Eukaryota.
  14. A. H. Knoll is at the Botanical Museum and the Department of Organismic and Evolutionary Biology, Harvard University.
Volume 285, Number 5430 Issue of 13 Aug 1999, pp. 1025 - 1026
©1999 by The American Association for the Advancement of Science.