Sea change in sediments

Earth's oxygen levels increased slowly over a long and ill-defined transitional period around two billion years ago. A microbial ‘footprint’ from this era provides biological evidence to complement existing geological data.

The microorganisms that were the sole forms of life on the early Earth survived billions of years of profound environmental change. Their modern counterparts exhibit a broad range of metabolic capabilities, exploiting diverse energy sources and so thriving in many different environments. But how did this remarkable adaptability develop? And have microorganisms preserved a record of past environmental changes? In the absence of complex body fossils laid down by microorganisms, Brocks and colleagues (page 866 of this issue)1 explore the early biosphere by analysing the chemical ‘footprint’ left by microorganisms on an ocean floor some 1.6 billion years ago, and compare it with how such a footprint would look today. In doing so, they confirm geochemical evidence of changes in the composition of Earth's oceans and atmosphere that occurred over a long period around two billion years ago.

In the primordial Archaean era, Earth's oceans and atmosphere contained little or no free oxygen. In this anoxic era, reduced compounds (the chemical opposites of oxidized compounds, containing species with an increased number of electrons), such as sulphides and ferrous-iron compounds, persisted for longer than they do in today's well-oxygenated marine and land environments2,3. Anaerobic photosynthesizing microorganisms used these reduced inorganic compounds to harvest energy for the synthesis of their cellular constituents. This situation began to change with the emergence of oxygen-producing photosynthetic cyanobacteria around 2.7 billion years ago, perhaps earlier (Fig. 1).

Figure 1: Life on Earth through the ages.

The ages of earliest known evidence of various biota (shown here) are probably determined by the quality of preservation of such ancient evidence. Bacteria capable of photosynthesis developed sometime before 2.7 billion years ago. The oxygen-producing cyanobacteria started the prolonged process of oxygenation of Earth's atmosphere and oceans that ultimately allowed more complex aerobic organisms to develop. Brocks and colleagues' analyses1 of biomarkers for microorganisms in marine sediments 1.6 billion years old provide a snapshot of an ocean in an intermediate stage of oxygenation: despite the presence of cyanobacteria, the waters were largely anoxic and sulphidic, with no evidence for the aerobic, planktonic eukaryotes characteristic of the modern ocean.

Photosynthesis is used by at least five phototrophic bacterial groups. In four of these groups — green sulphur bacteria, green non-sulphur bacteria, heliobacteria and proteobacteria — the process is anoxygenic (no oxygen is produced). These microbiota also require a reduced chemical substrate to provide electrons for organic biosynthesis4. Cyanobacteria, which form the fifth group, are unique in harnessing light directly to split water molecules, releasing molecular oxygen as a by-product. Oxygenic photosynthesis liberated emergent microbial life from its total dependence on hydrothermal fluids and other sources of reduced inorganic compounds; cyanobacteria could then spread across the planet.

A significant initial effect of oxygenic photosynthesis on the oceans was the oxidation of reduced compounds containing ferrous iron and sulphides — at least in surface waters. Gradually, oxygen levels increased until the oceans resembled the well-oxygenated seas we know today. Evidence that this transition was slow has previously been garnered from geological and geochemical features, such as the large bodies of iron-rich sedimentary rocks known as banded iron formations. Ferrous iron supplied through weathering and hydrothermal activity was deposited in these layers for hundreds of millions of years until the process came to an abrupt halt2 around 1.7 billion years ago, when the presence of sufficient photosynthetic oxygen oxidized ferrous iron in sea water. Sometime later, sulphides became rapidly oxidized during weathering, and sulphates, their oxidized products, accumulated in sea water5.

Brocks and colleagues1 pursue the crucial question of exactly when marine oxygen levels approached modern values — and when, for example, communities of the aerobic planktonic, eukaryotic (nucleus-containing) cellular organisms characteristic of today's oceans became established. They investigated fossilized hydrocarbons in siltstones and shales in a former marine sedimentary basin in northern Australia dating from the mid-Proterozoic era, 1.64 billion years ago. The synthesis of certain hydrocarbons is specific to certain groups of microorganisms6, so the fossilized hydrocarbons present in the rocks act as ‘biomarkers’ for the bacteria active at the time of their deposition.

By comparing these biomarkers with those from analogous modern environments1, a portrait can be painted of a global environment 1.64 billion years ago that was at a degree of oxidation intermediate between those of the Archaean and modern worlds. The presence of β-carotane in the record, for example, probably signals that cyanobacteria supplying reduced carbon were present. Aerobic methane-oxidizing bacteria, which flourish in environments where methane and oxygen are available but oxygen levels are low, were seemingly also abundant. This methane was produced by a group of microorganisms known as archaea that must have competed successfully with sulphate-reducing bacteria for reduced chemical substrates; this indicates that sulphate levels were substantially lower than in modern sea water. On the other hand, the sulphate supply to sulphate-reducing bacteria was at least sufficient for these microorganisms to produce some sulphides.

The carotenoids found by Brocks and colleagues1 in their rock samples speak for the presence of non-oxygenic photosynthetic bacteria of the type that typically requires both reduced sulphur compounds and sunlight for growth — so indicating the presence of shallow, sunlit sulphidic waters lacking oxygen. The abundances of pyrite (iron sulphide, FeS2) and stable sulphur isotopes in mid-Proterozoic sediments5,7 support the inference that sulphate levels were substantially lower than those today, and that sulphide was pervasive in the water column. Finally, the conspicuous absence of eukaryotic biomarkers in the samples seems to indicate that the pervasive planktonic populations so characteristic of later marine environments were not to be found.

So why did atmospheric and marine oxygen fail to attain near-modern levels during the mid-Proterozoic? A possible answer is that biologically important metals such as iron and molybdenum were stripped from sea water to form highly insoluble sulphides8. Sulphidic waters are toxic to planktonic eukaryotes and therefore possibly suppressed their populations. This mid-Proterozoic period of deep- sea anoxia and restricted productivity probably ended when increased rates of oxidative weathering of sulphides accelerated sulphate production and caused the sulphidic waters to retreat5.

Brocks and colleagues' study1 greatly extends the known antiquity of key biomarkers and is a significant contribution to charting the evolution of the mid-Proterozoic biosphere. But it is also just a first step. Now these microbial biomarkers should be analysed for their carbon-isotopic compositions to help confirm the microorganisms' identities and clarify their relationships within their communities9. Biomarkers should be characterized in mid-Proterozoic sedimentary rocks along an onshore–offshore axis to reconstruct the coastal palaeogeography more completely. Further analyses of biomarkers in rocks of similar age from other localities should help to provide a more global perspective. And sediments of various ages should be examined to determine, among other things, how the distribution of eukaryotic biomarkers might be related to changes in the biogeochemical sulphur cycle. Such studies will indeed add pieces to the puzzle of the microbial populations and processes that eventually led to the modern oxygenated biosphere.


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Marais, D. Sea change in sediments. Nature 437, 826–827 (2005).

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