Rubisco and the tendency towards perfection

The effects of scala naturae in the way we think about the evolutionary process are profound and harmful. As a shameful example, it comes to my mind the ludicrous concept that “man came from monkey”. No evolutionary biologist would assert such a thing, neither using the strict and monophyletic sense of the word “monkey” (only the old world monkeys) nor in its most broad, paraphyletic and incorrect sense (all primates but man). Using the word “monkey” in its strict sense, I always like to say to my students that man did not come from monkey, and that the reverse is also incorrect, i. e., monkey did not come from man: we can only say that man and monkey share a common ancestor.

Understanding the evolutionary process in the correct way, one can easily see that humans and their ancestors took one path, while monkeys and their ancestors took another path in their evolutionary histories. But there is a lot late XIX and early XX century’s ideas about evolution in which scala naturae not only played a major theoretical role but was sadly the very cornerstone of the evolutionary thought, and this biased way of thinking leads to a very different conclusion. For instance, let’s put the monkeys aside and think about a species much more closely related to the humans, the chimpanzee. It is quite common (I am always aware of these lapses in books, documentaries etc …) hearing that “chimps don’t walk bipedally yet”, or that “chimps did not develop spoken language yet” among others nonsensical things. What does that “yet” mean? The chimpanzee is not the man’s ancestor, the chimpanzee is not a less evolved man (another statement that, by the way, means nothing). Chimpanzees and humans descended from a common ancestor, that’s all. While the lineage that led to humans developed spoken language, for its own needs and vicissitudes, the lineage that gave rise to chimpanzees was worried with other evolutionary problems (and solutions). Chimpanzees do not had or have to develop spoken language, and probably never will. I emphasize again that chimps are not the ancestors of humans, and that neither humans are the ancestors of chimpanzees.

In the scala naturae way of thinking, the man, placed (by himself) in the topmost position of the great chain of being, defines the parameters to the other creatures, all of them compared to us in the light of those parameters and, inevitably, labelled as less evolved creatures. The fishes have not legs yet, the frogs have not amnion yet, the lizards have not endothermic thermoregulation yet, the chimps have not language yet (this last sentence is, by the way, a behavioural canard). Whenever I’m watching a show on Discovery Channel or National Geographic Channel, watching a film, reading a biology book or just chatting with folks, I try to keep myself aware of the effects (some of them quite subtle, almost imperceptible) of scala naturae in our way of understanding the life on Earth.

The next example is somewhat more complex, but it brings out the same classic notion associated with the scala naturae we just discussed, which is the tendency to perfection. It is the dual catalytic activity of the enzyme Ribulose-1,5-bisphosphate-carboxylase-oxidase, or simply Rubisco. Rubisco is one of the most important enzyme in the planet, because it catalyzes the addition of carbon dioxide to ribulose-1,5-bisphosphate in the Calvin cycle, producing 3-phosphoglycerate. For those who do not remember, we are talking about the enzyme that initially fix carbon dioxide in photosynthesis. It turns out that, depending on the concentration of molecular oxygen and carbon dioxide, Rubisco can add either the former or the latter to ribulose; the reaction with molecular oxygen, undesirable, leads to production of 3-phosphoglycerate and phosphoglycolate. In short, this is a process (called photorespiration) energetically harmful for the photosynthetic organism.

3D structure of Rubisco.

3D structure of Rubisco (source: Protein Data Bank).

The classic explanation for this strange property of Rubisco is that the enzyme would have appeared at a time when there was practically no free molecular oxygen in the atmosphere. According to this view, Rubisco was selectively shaped to an environment very different from today, when concentration of carbon dioxide were much higher and therefore the oxygenase activity of Rubisco did not have metabolic or evolutionary importance. Thus, according this explanation, all the physiological framework of plants depends on an enzyme that, ever since the carboniferous, is no more in its ideal medium, and now carries out a stressful oxidative activity.

This explanation is clearly inappropriate. First, we know today that there are several different forms of Rubisco, each one with different oxidative activities. There are variants of Rubisco found in microorganisms far more sensitive to molecular oxygen than Rubisco found in plants, showing that the latter would already be very effective in using carbon dioxide as a substrate. Second, 300 or 350 million years (from carboniferous to the present) is a huge time evolutionarily speaking: in this time span evolution was able to bring up the highly complex CAM and C4 metabolism for preventing photorespiration, for example. So, time is not the culprit for evolution having not brought up a variant of Rubisco with its oxidative activity reduced.

Moreover, there is currently a tendency to think about photorespiration as an important activity for the plant! Thus, in this process, the consumption of reduced NADP and ATP would be an escape valve to prevent photooxidation. According to this line of analysis, Rubisco does not have a lower oxidative activity because, to the plant, the oxidative activity itself, which we generally regard as a “imperfection” of Rubisco, would be selectively advantageous.

Regardless of which point of view is the correct one, I think that a key explanation can be found in Lodish’s Molecular Cell Biology  (5th edition, page 345):

“Photorespiration is wasteful to the energy economy of the plant: it consumes ATP and O2, and it generates CO2. It is surprising, therefore, that all known rubiscos catalyze photorespiration. Probably the necessary structure of the active site of rubisco precluded evolution of an enzyme that does not catalyze photorespiration.”

This interpretation is supported by Douglas Futuyma, who kindly answered me after I emailed him asking about this property of Rubisco. He wrote: “Usually there are trade-offs, so that a characteristic (whether it be an enzyme or an anatomical feature) is not ideally suited for the one function we are aware of – often because it must perform several functions, or a single function under different conditions that would require differrent optimal properties.”

However, it is common to hear that the extant form of Rubisco (supposing there is only one) is an “imperfect” form of the enzyme, and that probably we are witnessing the evolutionary process, which should lead us to a enzyme that shows no oxidative activity, thus avoiding the occurrence of photorespiration. I have heard this interpretation quite often.

I think this is an inappropriate thought in evolutionary biology. First, let’s see: the catalytic activity of Rubisco is such that both carbon dioxide and oxygen can act as molecular reagents, and possibly changes in the three-dimensional structure of its active site could circumvent the problem, eliminating the oxidative activity of Rubisco. But why, even after millions of years of existence of this enzyme in more than 400,000 species, this variant never showed up? I’m only dealing the question statistically, since this hypothetical variant has no obligation to arise. So, the chances are enormous, given the time and number of populations and species involved. Why it never showed up?

Second, why have the plants developed the whole complex mechanism of C4 photosynthesis, with Kranz anatomy, or even the carbon sequestration mechanism in CAM, both much more complex evolutionarily speaking, when it would be much simpler to develop a Rubisco without oxidative activity?

My point is that we cannot ascribe a tendency to perfection in evolutionary biology, especially when faced with a structure that “might” be better. In fact, such structures can be modified (evolutionarily speaking), but this is not an obligation, much less the result of an internal mystical force.

Finally, there is one last point I wish to talk about: what does it mean when someone speaks of Rubisco being an intermediate form for a future variant, and that “we’re watching the evolutionary process”? After all, are not we watching the evolutionary process in all existing beings, all the time? Are not all current structures, even those we consider most perfect and finished, just a snapshot of the evolutionary process, an intermediate step between what has being and what will be?

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