The origin of complex life – it was all about energy

By Ed Yong
Oct 20, 2010 6:00 PMApr 12, 2023 2:17 PM


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The 21st century is all about conserving energy. The push towards energy-efficient buildings, vehicles and lifestyles is both fashionable and necessary, but it’s also ironic. Our pattern of ever-increasing energy consumption is deeply rooted in our history, not just since the Industrial Revolution, but since the origin of all complex life on Earth.

According to a new hypothesis, put forward by Nick Lane and Bill Martin, we are all natural-born gas-guzzlers. Our very existence, and that of every animal, plant and fungus, depended on an ancient partnership, forged a few billion years ago, which gave our ancestors access to unparalleled supplies of energy and allowed them to escape from the shackles of simplicity.

To Lane and Martin, energy supply is the key factor that separates the two major types of cells on the planet. The first group – the simple prokaryotes, such as bacteria and archaea – are small, consist entirely of single cells (or at most, simple colonies), and have little in the way of internal structure. They are very different to the eukaryotes, the group that includes all complex life on the planet, including every animal, plant, fungus and alga. Their cells are large, structured, and filled with many internal compartments. These include the nucleus, where DNA is stored, and the mitochondria, which act as tiny powerhouses (more on these later).

Prokaryotes can do many incredible things. They can eat food as unappetising as oiland live in places where literally not a single other living thing can thrive. But despite their boundless innovations, they have always remained simple. While eukaryotic cells have evolved into large and complex forms like animals and plants on at least six separate occasions, prokaryotes have always remained simple. Some have nudged into more complex territory – for example, by becoming incredibly big– but all of these pioneers have stopped short. Only once in history have simple prokaryotes made the transition to complex eukaryotes. Why?

Lane and Martin think that the answer lies within the mitochondria. They were once prokaryotes themselves. In the depths of history, a free-living bacterium was engulfed by a larger cell and was neither digested nor destroyed. Instead, it was domesticated. It forged a unique and fateful partnership with its host, eventually becoming the mitochondria of today. All of this happened just once in life’s history and all of today’s eukaryotes are descended from that fused cell. Indeed, many scientists view the origin of mitochondria as the origin of the eukaryotes themselves.

Mitochondria are the power centres of eukaryotic cells. Within their walls, proteins carry out chemical reactions that combine food with oxygen to produce ATP, the molecule that acts as a cell’s energetic currency. These proteins sit inside the mitochondrion’s inner membrane, which is repeatedly folded like ruched fabric. These folds provide a greater surface area for energy-producing reactions to occur, allowing the mitochondria to produce a substantial supply to its host. That gives eukaryotes a major advantage over their prokaryotic peers: with more available energy, they can afford to have more genes.

The transition from a simple prokaryotic cell to a complex eukaryotic one was accompanied by a large rise in the number of genes. The average bacterium only has around 5,000 genes but even the smallest eukaryotes have an average of 20,000. But having more genes comes at a cost. The simple act of reading the gene and translating it into a protein (biologists would say “expressing” it) requires energy. This process takes up a whopping 75% of a cell’s energy budget.

In the same way that a gadget-hoarding human would ramp up a sizeable electricity bill, a cell with a larger genome would face a substantial energy burden. And just like the gadget fanatic has a limited budget to spend on their escalating bills, a bacterium has only so much energy to devote to expressing its genes. Every extra gene reduces the amount of available energy per gene. Its only option would be to produce fewer proteins, which would put it at a disadvantage compared to its peers.

So prokaryotes are stuck in an energetic rut. They sit at the bottom of a deep evolutionary canyon, surrounded by steep walls that require a massive influx of energy to scale. Unable to surmount these barriers, they are stuck with small genomes and simple structures. Indeed, evolution tends to push bacteria towards ever more compact genomes, mercilessly pruning away superfluous genes. Today, in a million ‘letters’ of DNA, eukaryotes have around 12 genes while the average bacterium has around 1,000!

Eukaryotes, however, are not so constrained. Thanks to their mitochondria, they have energy to spare. The average eukaryote can support a genome that’s 200,000 times larger than that of a bacterium, and still devote a similar amount of energy to each of its genes. As Lane and Martin say, “Put another way, a eukaryotic gene commands some 200,000 times more energy than a prokaryotic gene.”

The eukaryotic genome is like a gas-guzzling monster truck, compared to the sleek, sports-car genomes of prokaryotes. The benefits of this lumbering size can’t be overstated. By having enough energy to support more genes, they have room to experiment. It’s no surprise that the diversity of eukaryotic genes vastly outstrips that of prokaryotic ones. The last common ancestor of all eukaryotes had already evolved at least 3,000 entire families of genes that the prokaryotes lack, and it had complex ways of controlling and regulating these newcomers.

But why haven’t prokaryotes evolved a workaround that produces the same benefits as mitochondria? If all it takes is an internal, intensely-folded compartment, then bacteria should have been able to evolve that. Indeed, some have evolved internal folds like those of mitochondria. Why are they still stuck in their energetic canyon?

The answer, according to Lane and Martin, is that mitochondria give eukaryotic cells something special that bacteria will never have, no matter how many folds they develop – an extra set of DNA. Having evolved from free-living bacteria, mitochondria have a tiny genome of their own. Most of the genes from the original bacteria have emigrated to the host cell’s main genome but those that remained in the mitochondria include those that are responsible for liberating energy from food and oxygen.

Having these energy-production genes close at hand means that mitochondria can react very quickly to any changes in their folded membrane that would hamper their abilities to fuel their host cell. Put simply, eukaryotes cells need the tiny amounts of DNA in their mitochondria in order to get a steady energy supply. Lose that DNA, and catastrophic blackouts ensue. Without this close association between extra membranes and energy-producing genes, prokaryotes cannot hope to achieve the huge and stable supplies necessary to become bigger and more complex.

In some ways, the exceptions here prove the rule. Epulopiscium fishelsoni is a giant bacterium that’s about as big as the full stop at the end of this sentence, and certainly a match for many eukaryotes in size. It has solved the problems posed by giant size by having as many as 600,000 copies of its full genome in every cell, dotted around its edges. Even this giant prokaryote needs to have genes in close proximity to its membrane.

But this strategy would never allow prokaryotes to achieve eukaryote-style complexity. It’s a false economy. The problem with Epulopiscium’s strategy is that it had hundreds of thousands of copies of its entire genome and every time the bacterium divides, all of that DNA needs to be copied. That is a massive energy drain that leads to the exact same problem that smaller bacteria face – the amount of available energy per gene is tiny. Faced with the same supply problem, Epulopiscium will remain a prokaryote.

By contrast, mitochondria have jettisoned the vast majority of their genes, so that copying their tiny remaining genomes is a cinch. They give a lot, but require little in return. They provided the first eukaryote with the equivalent of thousands of tiny batteries, giving them the extra power they needed to expand, evolve and experiment with new genes and proteins. Indeed, the rise of the eukaryotes was the greatest period of genetic innovation since the origin of life itself. As Lane and Martin write, “If evolution works like a tinkerer, evolution with mitochondria works like a corps of engineers.”

If Lane and Martin are correct, then their ideas on the importance of mitochondria have big implications for the evolution of eukaryotes. There are two general schools of thought on this (which I covered in greater depth in a previous post). One says that eukaryotes are descended from bacterial ancestors, and that they were well on the way towards evolving a complex structure before one of them engulfed the bacterium that would eventually become a mitochondrion.

But if mitochondria were the key the eukaryotic complexity, as Lane and Martin argue, then that model can’t be right. Instead, it’s the second model that is more plausible: that the first eukaryote was forged from a chance encounter between two prokaryotes. One swallowed the other and it was at this very moment that the first eukaryote came into being. Only then, with a surge of power, did all the characteristic features of eukaryotes start to evolve. It was a singular evolutionary step, when prokaryotes leapt out of their energetic canyon into the plateaus of complexity lying beyond, literally in a single bound.

Reference: Nature:

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