Special Viewpoints

Life and the Evolution of Earth's Atmosphere

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Science  10 May 2002:
Vol. 296, Issue 5570, pp. 1066-1068
DOI: 10.1126/science.1071184

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Harvesting light to produce energy and oxygen (photosynthesis) is the signature of all land plants. This ability was co-opted from a precocious and ancient form of life known as cyanobacteria. Today these bacteria, as well as microscopic algae, supply oxygen to the atmosphere and churn out fixed nitrogen in Earth's vast oceans. Microorganisms may also have played a major role in atmosphere evolution before the rise of oxygen. Under the more dim light of a young sun cooler than today's, certain groups of anaerobic bacteria may have been pumping out large amounts of methane, thereby keeping the early climate warm and inviting. The evolution of Earth's atmosphere is linked tightly to the evolution of its biota.

Microorganisms are important for many reasons, not the least of which is their responsibility, direct or indirect, for the production of nearly all of the oxygen we breathe. Oxygen is produced during photosynthesis by a reaction that can be written as CO2 + H2O → CH2O + O2. Here, “CH2O” is a geochemist's shorthand for more complex forms of organic matter. Most photosynthesis on land is carried out by higher plants, not microorganisms; but terrestrial photosynthesis has little effect on atmospheric O2 because it is nearly balanced by the reverse processes of respiration and decay. By contrast, marine photosynthesis is a net source of O2because a small fraction (∼0.1%) of the organic matter synthesized in the oceans is buried in sediments. This small leak in the marine organic carbon cycle is responsible for most of our atmospheric O2.

Although higher plants (e.g., kelp) are found in the oceans, most marine photosynthesis is performed by single-celled organisms. The most abundant of these are eukaryotic algae, such as diatoms and coccolithophorids (Fig. 1). Roughly 99% of primary production can be attributed to such organisms (1). Prokaryotic bacteria are also important for another reason. Though they make up only ∼1% of marine biomass, cyanobacteria (or blue-green algae) are the main organisms responsible for fixing nitrogen (1). This capability is quite remarkable because the enzyme responsible for reducing N2, nitrogenase, is poisoned by O2. Thus, cyanobacteria have had to evolve complex mechanisms for protecting their nitrogenase. Some, such as the filamentous Anabaena spp., do so by fixing nitrogen only in specialized cells called heterocysts. Other cyanobacteria fix nitrogen at night and photosynthesize by day. Still others, such asTrichodesmium spp. (very abundant in tropical waters), fix nitrogen in the morning and photosynthesize in the afternoon (2). Such specificity shows that these are highly evolved pieces of biological machinery.

Figure 1

Examples of photosynthesizing marine microorganisms (phytoplankton), including diatoms (A), coccolithophorids (B), and the cyanobacteria Trichodesmium (C),Prochlorococcus (D), and Anabaena(E). [(A) and (B) from (23), (C) from (2), (D) courtesy of S. Chisholm and C. Ting, and (E) copyright Dennis Kunkle Microscopy, Inc.]

In some sense, when it comes to producing oxygen, cyanobacteria are the entire story. Because cyanobacteria can live anaerobically and aerobically, they are universally believed to have been responsible for the initial rise of atmospheric O2 around 2.3 billion years ago (Ga) (3, 4). Comparison of ribosomal RNA from cyanobacteria with portions of the DNA inside chloroplasts implies that all eukaryotes, including algae and higher plants, derived their photosynthetic capabilities from cyanobacteria by way of endosymbiosis (5). The Prochlorococcus spp., an important component of today's marine ecosystem, may be the living ancestor of the cyanobacterium involved in this event (6). It appears that oxygenic photosynthesis—an extremely complex biochemical process—was “invented” only once, and a primitive cyanobacterium was the organism responsible.

Though the production of O2 is the most notable effect of organisms on the atmosphere, it is by no means their only one. Our modern atmosphere contains numerous trace gases (e.g., CH4, N2O, CH3Cl, COS, dimethyl sulfide) whose sources are almost entirely biological. Some of these gases influence climate today by contributing to the atmospheric greenhouse effect. Concentrations of CH4 (methane) and N2O (nitrous oxide) have been increasing in recent years as a consequence of agricultural activities, and this is of some concern with respect to the problem of human-induced global warming.

More interesting from a long-term perspective, however, is the effect that such reduced biogenic gases might have had before the rise of O2. Some of them, like N2O, should have been rapidly photolyzed in the absence of an ozone shield (7), but others—CH4 in particular—could have been quite abundant in an anoxic atmosphere. CH4 has only a 10-year residence time today because it reacts with the hydroxyl radical, OH. In an anoxic atmosphere, OH would have been much less abundant and CH4would have been destroyed mainly by photolysis at Ly α wavelengths (121.6 nm). Under such conditions, its residence time should have been more like 10,000 years (8). A biogenic CH4source comparable to the modern flux of 535 Tg CH4/year (9), which produces an atmospheric CH4concentration of 1.6 ppm (parts per million) today, could have generated over 1000 ppm of CH4 in the distant past. This is enough to have had a major warming effect on climate (10). The Sun was considerably dimmer at that time, so the added greenhouse effect of CH4 was precisely what was needed to keep the Archean Earth from freezing. The rise in atmospheric O2corresponds precisely with Earth's first well-documented glaciation (11), suggesting that the glaciation was triggered by the accompanying decrease in atmospheric CH4.

Methane is of such potential importance on the primitive Earth that we should say more about the organisms that produce it. The methanogenic bacteria, or methanogens, are members of the Euryarchaeota branch of the Archaea, one of the three major kingdoms of life identified by sequencing ribosomal RNA. They have several characteristics, including a strictly anaerobic lifestyle and a tendency toward thermophily, that suggest they are evolutionarily ancient (12, 13). Today, methanogens are confined to restricted, oxygen-free environments such as the intestines of cows and the soils beneath flooded rice paddies. They make their metabolic living by converting the by-products of fermentation (e.g., formate, acetate, lactate) into methane. The overall reaction (fermentation plus methanogenesis) can be written as: 2CH2O → CO2 + CH4. This process would have assumed greater importance on the early Earth (14) because low concentrations of dissolved O2 and sulfate (15) would have meant less recycling of organic matter by aerobic respiration or biological sulfate reduction.

On the anoxic primitive Earth, methanogens may also have been primary producers of organic matter. All methanogens can use hydrogen as a substrate, described by the reaction CO2 + 4H2 → CH4 + 2H2O. Predicted H2 concentrations in an anoxic early atmosphere are of the order of 1000 ppm (16), which is well above the threshold for methanogenesis, even at today's relatively low CO2 level (17). H2concentrations would have dropped once methanogens proliferated (18, 19); however, other gases, such as CO (carbon monoxide), could have served as biological substrates as well. CO hydrolyzes to HCOO (formate ion), which in turn converts to hydrogen via the reaction HCOO + H2O → HCO3 + H2. This latter reaction is catalyzed by enzymes released by methanogens (20).

All of this suggests that, before the rise of O2, CH4 could have been produced at rates that exceeded today's rate by factors of 10 to 100. But this leads to a conundrum: the modern solar Ly α flux is only ∼5 × 1011photons cm-2 s-1, which corresponds to a methane destruction rate of 2140 Tg CH4/year, or about fourfold the modern methane flux. Even if the solar EUV (extreme ultraviolet) flux was several times higher back then (21), it appears that CH4 should have accumulated to very high concentrations in the atmosphere. The factor that limited the CH4 abundance was likely the production of organic haze, which is predicted to form when the atmospheric CH4/CO2 ratio exceeds unity (8). This haze would have created an “anti–greenhouse effect,” which would have lowered surface temperatures and made life less comfortable for the predominately thermophilic methanogens (22).

Thus, microorganisms have probably determined the basic composition of Earth's atmosphere since the origin of life. During the first half of Earth's history, this may have resulted in a planet that looked much like Saturn's moon Titan (Fig. 2). During the latter half of Earth's history, microorganisms created the breathable, O2-rich air and clear blue skies that we enjoy today. Atmospheric evolution on an inhabited planet is determined largely by its microbial populations.

Figure 2

This photograph of Saturn's moon, Titan, shows the orange-tinted haze that is thought to be formed by photolysis and charged-particle bombardment of methane in Titan's upper atmosphere. The Cassini mission, now on its way to Saturn, will test this model by dropping a probe into Titan's atmosphere. [Photo courtesy of NASA:http://photojournal.jpl.nasa.gov/]

  • * To whom correspondence should be addressed. E-mail: kasting{at}essc.psu.edu


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