Nick Lane 2015. The Vital Question. Why is life the way it is? London: Profile Books, 360 pp.

An original, exciting discussion of what life is, and how it may have evolved. ‘Origin of Life’ is a crowded field where it is difficult to be original, but The Vital Question certainly qualifies.

Flow of energy, not information, is central to Nick Lane’s account, DNA is rarely discussed. The overriding principle seems to be, when seeking to reveal phylogenetic relationships, that parsimony of energy metabolic mechanisms in cells is more informative (at least at basal branches) than molecular phylogeny based on genetic data (which cannot be trusted because lateral gene transfer is rife among bacteria et al. and is only good for gene trees). Instead, Nick Lane would map genes onto a tree based on characteristics related to energy metabolism. An interesting reversal from the very many molecular phylogenies of eukaryote taxa, in which lateral gene transfer is much less common.

In the Introduction, Nick Lane dismisses the “serial symbiosis” model championed by Lyn Margulis because it predicts there should be many kinds of eukaryotes formed from many different combinations of bacterial/archaeal symbionts. Instead we find that all cells are virtually identical in their component organelles in all eukaryote organisms (including “… you (and ewe and yew)” - E. Yonge, 2014). All eukaryotes are thus derived from a single symbiotic event, somewhere between 1.5-2 billion years ago.

What is life? and What lives? present the current views on what molecular phylogenetics concludes about evolutionary relationships (3 monophyletic groups: bacteria, archaea, eukaryota) and also a thrilling description of the molecular power plant of the mitochondrion, which is a semi-permeable membrane that functions as a proton pump. A large respiratory complex (comprised of proteins) uses a redox reaction to pump protons across the membrane and a complex protein called ATP synthase sits in the membrane and uses the protons gradient through the membrane to allow protons to pass back through the protein, rotating the proteins complex head like a motor. This converts ADP to ATP and powers the cell. This mechanism was discovered by Peter Mitchell who termed it chemiosmotic coupling. I had to re-read this section (pp. 63-77 and the beautiful drawing of ATP synthase on p. 74) several times, both to be sure I sort of understood it, but also for pure pleasure. It is not easy to describe biochemical reactions in a way that is not only interesting but downright exciting.

But how did it arise?

A good case is made for alkaline deep sea vents being a likely model environment for the appearance of life (not black smokers, which have the wrong chemical constituents and are too short-lived). Alkaline vents are not volcanic, are warm but not hot, are micro-porous towers (not hollow chimneys) and persist for thousands of years (the first-discovered, the Lost City, is over 100,000 years old). Lane argues convincingly that, if imagined in an ancient oxygen-poor ocean, an alkaline vent would be an environment where a lipid membrane with the necessary properties would occur spontaneously to become LUCA (the last universal common ancestor), possessing properties still common to both bacteria and archaea: similar DNA transcription and translation, ribosomes, protein synthesis etc. From LUCA, subpopulations then diverged into archaea and bacteria, which differ in basic traits including the structure of the membrane and the pump, the cell wall, DNA replication and others, these differences being conserved within bacteria and archaea.

Most of the second half of the book is devoted to eukaryotes. in a way that is not only interesting but downright exciting.

But how did it arise?

A good case is made for alkaline deep sea vents being a likely model environment for the appearance of life (not black smokers, which have the wrong chemical constituents and are too short-lived). Alkaline vents are not volcanic, are warm but not hot, are micro-porous towers (not hollow chimneys) and persist for thousands of years (the first-discovered, the Lost City, is over 100,000 years old). Lane argues convincingly that, if imagined in an ancient oxygen-poor ocean, an alkaline vent would be an environment where a lipid membrane with the necessary properties would occur spontaneously to become LUCA (the last universal common ancestor), possessing properties still common to both bacteria and archaea: similar DNA transcription and translation, ribosomes, protein synthesis etc. From LUCA, subpopulations then diverged into archaea and bacteria, which differ in basic traits including the structure of the membrane and the pump, the cell wall, DNA replication and others, these differences being conserved within bacteria and archaea.

Most of the second half of the book is devoted to eukaryotes.

Lane concludes that eukaryotes were formed from a bacterial symbiont and an archaeal host. (Of eukaryote genes with identifiable prokaryote homologues, ~75% are from bacteria and 25% from archaea.) Another point well made is that while morphological diversity is with the eukaryotes, metabolic diversity and versatility is overwhelmingly with the bacteria and archaea (prokaryotes). ‘Energy per gene’ is Nick Lane’s insightful way of thinking about this: eukaryotes have 200,000 times more energy per gene than prokaryotes, mainly because mitochondria safely contained within a eukaryote cell operate vastly more efficiently than ‘wild’ bacteria and other prokaryotes. Thus, eukaryotes have many thousands of times the amount of energy per gene available to make protein, which they can thus produce in greater variety or quantity, or (usually) both. So eukaryotes are able to make an albatross or a blue whale or a conifer while bacteria are restricted to microscopic sizes.

Introns are probably leftover DNA fragments from failed endosymbionts and they are enclosed in the nucleus to isolate them. Introns are numerous in eukaryotes but few in prokaryotes, which are able to eliminate them through some as yet unknown mechanism. The positions of introns in the eukaryote genome is conserved across diverse groups, indicating a likely ancient origin.

Sex (recombination) increases the genetic variation and also exposes mutations to selection. In organisms such as sponges and corals selection can continue to operate throughout life. But in organisms with differentiated somatic cells (tissues and organs), health of the organism depends on health of organs so decreasing genetic variation in adult tissues is necessary. Large eggs with lots of mitochondria achieve this but this strategy is not so good for gametes since they also reduce variance and deleterious mutations are not exposed to selection. Hence sperm are small and lack mitochondria thus both needs are met. (This is work in progress; the above assumes low rates of mitochondrial mutation which is not true in vertebrates. Models for other scenarious are currently being developed and tested.)

A lot of the remainder of the discussion are corollaries and predictions based on the observation that coding for most proteins vital to mitochondrial function have been transferred to the nucleus (historically there were mitochondrial and nuclear copies but to make mitochondria more efficient their genes were largely lost). Even the vital respiratory protein complex is coded by both nuclear genes and a few from the mitochondrial genome. This has all sorts of consequences. Mitochondrial and nuclear genes must be coadapted. A mechanism for cell death (apoptosis; pp. ~243-248) allows enzymes to kill of and clear up dodgy cells where mitochondrial and nuclear genes are no longer coadapted, as indicated by accumulating free radicals and other molecular signals. Speciation is also promoted because hybrids in many cases will also have mitochondrial and nuclear code mismatched. Nevertheless, the anti-oxidant theory of aging is (largely) shown to be false, although Lane promotes a more qualified version. And aerobic exercise is still beneficial to mitochondria, and thus to us with some predictable patterns in the animal world (for example aerobic pigeons live to be 30 while sedentary rodents to 3).

There is an intriguing epilogue about an enigmatic organism, Parakaryon myojinensis, recently described from the deep sea (from a single cell if you please!) Yamaguchi M, Mori Y, Kozuka Y, Okada H, Uematsu K, Tame A, Furukawa H, Maruyama T, Worman CO, Yokoyama K (2012). “Prokaryote or eukaryote? A unique microorganism from the deep sea.”. J Electron Microsc (Tokyo). 61 (6): 423–431.. And, it was collected from a polychaete (yay! haven’t found out what kind yet). Lane makes a convincing case that this is a prokaryote in which endosymbiosis is just starting up anew, and several predictions about genome size etc are put forward. These remain untested.

Seemingly Nick Lane is aiming as much at a cross-disciplinary academic audience as a general one. As befits a book with this goal, originality and ambition, the text is supported by a 30 page bibliography including much original literature, conveniently organised under headings that correspond with the text.