Rich feast on stony ground

On a sunny day in late July, "I am off to the North Pole", writes the palaeontologist Andrew Knoll, to examine vestiges of life's beginnings, 3.5 billion years ago. He goes on to explain, in an unusual mixture of accessible prose and serious science, how only at the North Pole and a few other places worldwide has "tectonic grace" protected ancient rocks from metamorphic destruction by the heat and pressure found in the earth's interior that together tend to obliterate the evidence for past life in sedimentary rocks.

In this wonderful book, the protected oases that have avoided the metamorphic fate become our cherished destinations. The main sites of tectonic grace we visit include Knoll's big six. They are the Gunflint iron formation of the Lake Superior region (especially in Ontario), the Great Wall of China, the Bil'yakh formation in Siberia, the Akademekerbreen in Spitsbergen (a desolate Arctic island in the Svalberg archipelago), the Doushentuo in China, and the Nama of the Namibian desert.

All the sites are Proterozoic, which means the rocks were laid down as sediments between 2,500 and 540 million years ago. To this we may add the Kotuikan rocks of Siberia, which are the youngest of the sites. They extend from the latest Proterozoic until well into the modern eon. Modern here means the Phanerozoic, which begins with the shelly animal fossils of the Cambrian era fewer than 541 million years ago and extends through the age of dinosaurs to the present.

The Kotuikan rocks straddle the period of most interest to Knoll: the stretch of time when sediments underlain by a relative paucity of fossil predecessors give rise to those replete with abundant and diverse animal remains. Knoll's extensive field experience and eagerness to share data and ideas with colleagues enable him to reconstruct responsibly the broad evolutionary scenario yet to remain close to the evidence.

Readers unfamiliar with the revolution in evolution still divide the living world into animals and plants. They may at first be confused when Knoll explains that the ancient fossiliferous rocks contain neither. Indeed, many of the large fossils illustrated here, some in beautiful colour, are neither animal nor plant. So what are they? Knoll answers this by describing the great domain of aquatic life that includes the plasmodial slime moulds, ciliates, red seaweeds, labyrinthulan slime nets, green algae, diatoms, shelled foraminifera and their naked relatives, the reticulomyxids. They comprise more than 50 inclusive groups (phyla). He approaches their evolution from prehistory and raises our consciousness of the extraordinary diversity of non-animal and non-plant life. These groups do not belong to the kingdom Monera - archaebacteria and eubacteria - or the kingdom Fungi - moulds, yeasts, mushrooms - but to the kingdom Protoctista.

Extrapolation from general palaeontological principles reveals that most protoctista, whether or not they form hard parts, are extinct. Among them lived the earliest cellular ancestors of all animals, plants and fungi.

Modern and ancient protoctista are composed of cells with nuclei whose descendants include ourselves. Fossil counterparts of live ones are surprisingly abundant.

Knoll's book provides a fascinating entry into the first appearance of these unruly beings on the stage of planet earth.

A genuine news item in Knoll's account concerns the marine environment of early life. His Proterozoic rock and fossil experience, coupled with his vast knowledge of scientific literature and his lively communication with geochemists and geophysicists, lead him to conclude that Proterozoic oceans were far less oxygenated and far more sulphide-rich at depth than previously realised.

The earliest nucleated organisms probably coped with fluctuating concentrations of both hydrogen sulphide and free oxygen. Knoll describes research by Don Canfield, an imaginative and industrious isotope geochemist now at the University of Odense in Denmark. Canfield and Knoll posit that, until the late Proterozoic, deep ocean basins resembled today's Black Sea.

An "intermediate ocean" separated the Archaean-eon anoxia (no oxygen) from the modern Phanerozoic-eon oxygen-rich oceans. Knoll argues that the early Proterozoic oxygen revolution did not directly usher in the fully oxygenated modern world but "rather an alien intermediate marked by moderate oxygen in the atmosphere and surface sea and hydrogen sulphide in deep water".

This newly conceived Proterozoic sulphide-rich ocean delights me and two colleagues of mine (Michael F. Dolan and Dennis G. Searcy) at the University of Massachusetts. Unaware of the Knoll-Canfield work, we hypothesised a sulphur-rich backdrop to the origin of the first nucleated cells.

Knoll and Canfield, who conclude that the transition to the oxidising atmosphere was neither sudden nor gradual, unwittingly bolster Searcy's discovery. Searcy measured continuous cytoplasmic production of significant quantities of hydrogen sulphide in all of a half a dozen representatives of the major groups of nucleated organisms: protoctista, fungi, animals and plants. Research that leads to similar conclusions from two very different fields (geochemistry and cell biology) should inspire closer collaboration to reconstruct environmental and cell evolution on the young earth.

Life on a Young Planet must surely be destined for a long-lasting paperback student edition. May I therefore suggest that Knoll updates his references to our papers on symbiosis in evolution - all highly positive I should say - with a summary of our recent work on the origin of the nucleus, whose conclusions are complementary to his own.

Lynn Margulis is distinguished university professor, department of geosciences, University of Massachusetts, Amherst, US.