Tuesday, July 12, 2016

A Chimeric Origin: Complexity, Sex, Life and Death


“If life is nothing but an electron looking for a place to rest, death is nothing but that electron come to rest.”

That’s the last sentence of the penultimate paragraph to Nick Lane’s The Vital Question. In Sections III and IV of his book, Lane tackles the origin of eukaryotes. (For my thoughts on the earlier sections, see part 1 and part 2.) Evidence is marshaled suggesting (but not proving) that a one-time endosymbiosis between a bacterium and an archaean cousin is the ancestor to all eukaryotic life on earth. This would be LECA, the Last Eukaryotic Common Ancestor. But reconstructing how this chimera came about is very difficult, and there seems to be a quantum leap in complexity.

After going through issues of genome size, circular versus straight chromosomes, phylogenetic considerations, and other potential structural constraints, Lane writes: “[LECA] was a complex cell that already had straight chromosomes, a membrane-bound nucleus, mitochondria, various specialized organelles and other membrane structures, a dynamic cytoskeleton, and traits like sex. It was recognizably a ‘modern’ eukaryotic cell. None of these traits exist in bacteria in anything resembling the eukaryotic state.”

To underscore the strangeness of this situation, he uses the following analogy. “It’s as if every single invention of modern society – houses, hygiene, roads, division of labour, farming, courts of law, standing armies, universities, governments, you name it – all these inventions could be traced back to ancient Rome; but before Rome, there was nothing but primitive hunter-gatherer societies. No remains of ancient Greece, China, Egypt, the Levant, Persia, or any other civilization; just abundant traces of hunter-gatherers everywhere you look. Here’s the rub. Imagine that experts have spent decades scrutinizing the archaeology of the world to unearth the remains of earlier cities, civilisations that pre-dated the Romans, which would give insight into how Rome was built. Hundreds of examples were discovered, yet each one, on closer inspection, turned out to post-date Rome. All these outwardly ancient and primitive cities were actually founded in the ‘dark ages’ by progenitors who could trace their own ancestors back to ancient Rome. In effect, all roads lead to Rome, and Rome really was built in a day.”

What drove the appearance of the eukaryote and cellular complexity? Energy per gene and chemical food sources. Lane surveys a range of bacteria comparing physical size, genome size and metabolic rate. There turns out to be a significant barrier to scale-up. Endosymbiosis between prokaryotes is uncommon although there are a couple of examples. Lane weaves a narrative starring mitochondria, the energy powerhouses of eukaryotes, that seem to fit the odd structure of our genes – piecemeal, messy and full of introns. The similarity between self-splicing introns and the eukaryotic spliceosome suggests that introns originated from the bacterial endosymbiont, subsequently evolving into genome-reduced mitochondria focused on bioenergetics needs.

Having two genomic sources can cause a variety of problems. Lane outlines the issues and uses them to construct an argument for the origins of sex (and two sexes in particular), the division between germline and somatic cells, and cell death via apoptosis. These are marshaled as evidence for the two-fold origin of eukaryotes. I can’t easily summarize the details here (you’ll have to read the book) but I will say that although speculative, his arguments are very intriguing. For example, why should cytochrome c, a respiratory protein, be so important in apoptosis? I suspect Lane is on to something here, but I do not have enough of a background in cell biology, genetics and biochemistry to properly evaluate his argument.

Lane’s book is the molecular biology counterpart to Brownlee and Ward’s Rare Earth: Why Complex Life is Uncommon in the Universe (written from the perspective of an astronomer and a paleontologist). Lane’s central story, however, is energy transduction. In his concluding paragraph, Lane summarizes: “Living needs an unceasing flux of energy. It’s hardly surprising that energy flux puts major constraints on the path of evolution, defining what is possible. It’s not surprising that bacteria keep doing what bacteria do, unable to tinker in any serious way with the flame that keeps them growing, dividing, conquering. It’s not surprising that the one accident that did work out, that singular endosymbiosis between prokaryotes, did not tinker with the flame, but ignited it in many copies in each and every eukaryotic cell, finally giving rise to complex life. It’s not surprising that keeping this flame alive is vital to our physiology and evolution, explaining many quirks of our past and our lives today.”

I beg to differ on terminology. I think this story is surprising. Being able to ‘explain’ something or at least string together a logical narrative with scientific arguments, does not make it any less surprising. The story is wonder-ful and awe-some. An excellent writer such as Lane evokes in the reader this sense of wonder.

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