Universal chlorophyll

At first sight the problem of addressing the question of evolutionary alternatives seems almost intractable. How can we begin to compare something of which we know nothing with that with which we are familiar? Self-evidently, but also trivially, the history of life is unique,3 and perhaps the absence of extraterrestrial communication4 is simply because intelligence is just another evolutionary quirk. Yet constraints on the alternative possibilities and trajectories through time, at least in evolution, can be demonstrated by at least three avenues. These are respectively: (a) to make a genuine attempt to consider the alternatives, (b) to devise experiments that at least in a restricted way rerun evolution, and (c) to look again at the history of life and enquire whether the ubiquity of convergence, be it in the anatomy, behaviour, or molecules, is anything more than a biological curiosity.

In the first chapter I mentioned the very surprising degree of efficiency of the genetic code. In principle the combinatorial immensity of the 'code hyperspace' means that there may be many other equally effective genetic codes, but as also explained one can impose a number of additional restrictions that suggest that the code adopted on Earth really is not just adequate, but quite remarkably good. There are, moreover, a number of other ways in which we can consider biological alternatives. An appropriate place to start is at the base of the planet's life-support system: that is, photosynthesis, and specifically the molecule that serves to trap the energy of the sunlight: chlorophyll. Chlorophyll must be a very ancient invention,5 because it occurs not only in the familiar plants but also in various bacteria. Of these, one group, usually referred to as the cyanobacteria (or sometimes blue-green algae), is of particular note. This is because, unlike the other photosynthetic bacteria, the oxygen it produces, as a by-product of the photosynthetic process, was (and, of course, still is) released into the surrounding water and thence to the atmosphere. Green land plants and eukaryotic algae, the latter most familiar as the various sorts of seaweed, also release free oxygen. This is, however, a consequence of the photosynthetic organelles within the cell, known as the chloroplasts. They were once free-living gram-positive bacteria, similar to the living cyanobacteria, but which merged symbi-otically with eukaryotic cells, ultimately to lose all independence.6 In this way, billions of years ago, the atmosphere of the Earth, originally free of oxygen, slowly became oxygenated, and as a result increasingly corrosive. Thus, the planet started to rust.7 The principal episode of oxygenation is usually identified as occurring at about 1.9 Ga ago. This is inferred principally on sedimentary evidence, notably the disappearance of mineral grains susceptible to oxidation, notably those of pyrite and uranium oxide (uraninite), and the development of red beds, whose colour signifies the onset of atmospheric oxygenation.

As oxygen levels climbed, so organisms had to adapt to this toxic and reactive molecule. But the process of oxygenation started much earlier. Just how geologically ancient photosynthesis is likely to be is hinted at in the oldest known well-preserved sedimentary rocks. These are from west Greenland (Chapter 5, p. 72) and as already noted contain carbon. The carbon has, however, been heated by temperature and pressure within the Earth and is now in the form of graphite,8 but it may still retain a signature of very ancient photosynthesis. To understand how this is possible, one needs first to recall that photosynthesis is a process whereby carbon in the atmosphere, in the form of carbon dioxide, is combined with water and ultimately transmuted to sugars, using sunlight as the source of energy. The carbon itself occurs in the form of two isotopes, one slightly heavier than the other: carbon-13 and carbon-12.9 The processes of photosynthesis 'prefer' to use the slightly lighter carbon-12, and hence the carbon stored in the plant tissue is slightly enriched in the lighter isotope. Photosynthesis thus imprints an isotopic signature, and provided that the carbon survives in the sedimentary record one can infer the ancient activity of chlorophyll, even if no other evidence for photosynthesis survives.10 And although altered to graphite, the carbon in the most ancient sediments, dated at about 3.8 Ga, looks as if it, too, might once have passed through the photosynthetic process.

The chemical processes of photosynthesis are very complex. Exactly how the Sun's photons are captured to yield the necessary energy within the photosynthetic 'factory', located within the chloroplasts of the green leaf, is still not completely understood. Despite the apparent miracle of sunlight pouring down on orchards and lagoons to produce apples and sea grass, it is clear that the process of photosynthesis is far from perfect. There are many chemical steps, and if an engineer had been in charge of the design process, the accountants and administrators would by now have been asking awkward questions. In particular, the activity of one key enzyme (known as d-ribulose-1,5-bisphosphate carboxylase, or RuBisCO for short) is severely hampered in the presence of oxygen, which ironically it also produces by catalysing another chemical reaction that accordingly competes with the process of photosynthesis. The net result is that valuable energy is consumed in an unavoidable metabolic process known as photorespiration.11 It is as if the crew on a sinking ship are ordered into the hold to stem the flood, and are all issued with sieves.

Nor is this the only problem the photosynthesizers face. An essential prerequisite of the process, of course, is carbon dioxide. Suppose, however, that the amount of this gas in the atmosphere were to plummet drastically. This might be due to a number of natural processes, such as episodes of massive mountain-building that expose vast areas of rock and scree where the carbon dioxide can be 'soaked' up by the enhanced rates of rock weathering. Plants would be faced with an extremely serious problem, and it was one that actually started about 15 million years ago. At this time the levels of atmospheric carbon dioxide began to decline precipitously, in part probably because of the uplift of a series of huge mountain belts, most notably the Himalayas. The plants' solution was to modify the steps in the photosynthetic process, leading to a transition from so-called C3 photosynthesis to a C4 mode (the numbers refer to the number of carbon atoms in the first compound to be formed). The details of this C4 photosynthesis are considered in Chapter 10, but what is worth noting here is that its evolution is rampantly convergent.

The processes of photosynthesis are, therefore, hedged in with many constraints, but even so chlorophyll is a remarkable molecule that effectively underpins the entire biosphere. It is thus rather surprising to learn that not only does chlorophyll fall short in such matters as the effectiveness of its RuBisCO, but it also seems to suffer from rather more general difficulties. George Wald, in particular, has pointed out that if one compares the absorption spectra of the various types of chlorophyll to the available visible light spectrum of our Sun the match is, to put it mildly, disappointing (Fig. 6.1). Clearly the chlorophyll has to absorb some sunlight or it simply would not work. In addition, different types of chlorophyll vary somewhat in their absorption spectra: chlorophyll d, for example, shows a rather remarkable shift towards absorption of red light.12 Accordingly chlorophyll has some latitude in the wavelengths of light it is best adapted to absorb, but it is all the more remarkable that the lion's share of the Sun's radiant energy remains largely untapped. And from this apparent anomaly Wald draws a very interesting inference. He argues that, however desirable a 'perfect' chlorophyll might be, it is simply not attainable: as the initial supplies of prebiotic 'soup' run out, so life must move to the situation where it can synthesize its own food

figure 6.1 A comparison between the spectrum of the Sun and the absorption spectra of three types of chlorophyll. Note how the spectra of the chlorophylls differ, but none is able to intercept the maximum output of the Sun. An 'ideal' chlorophyll would mirror the outline of the Sun's spectral profile, leading George Wald to suggest that not only is terrestrial chlorophyll the best available, but anywhere else in the Universe on a planet the same chlorophyll will occur. (Redrawn from figure by Emai Kasai on p. 96 of G. Wald's article 'Life and light', Scientific American, vol. 201 (4), pp. 92-108. Copyright © 1959 by Scientific American, Inc. All rights reserved.)

figure 6.1 A comparison between the spectrum of the Sun and the absorption spectra of three types of chlorophyll. Note how the spectra of the chlorophylls differ, but none is able to intercept the maximum output of the Sun. An 'ideal' chlorophyll would mirror the outline of the Sun's spectral profile, leading George Wald to suggest that not only is terrestrial chlorophyll the best available, but anywhere else in the Universe on a planet the same chlorophyll will occur. (Redrawn from figure by Emai Kasai on p. 96 of G. Wald's article 'Life and light', Scientific American, vol. 201 (4), pp. 92-108. Copyright © 1959 by Scientific American, Inc. All rights reserved.)

from the light of its sun. Accordingly the necessary machinery, including chlorophyll, must evolve. On this basis Wald draws a bold conclusion, remarking that 'When that time comes, it seems to me likely that the same factors that governed the exclusive choice of the chlorophylls for photosynthesis on the Earth might prove equally compelling elsewhere.'13

We have already seen that the chances of encountering habitable planets may be much lower than is generally supposed, but what if we do locate an alien biosphere? Wald's arguments suggest that however many light years we may be from the Earth, if we discover a planet and wander along its remote shores with their entanglements of seaweeds or explore its immense forests, sure enough there will be the same and all-too-familiar chlorophyll soaking up the light of an alien star.14

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