My direct experience with prokaryotes is sadly limited — while our entire lives and environment are profoundly shaped by the activity of bacteria, we rarely actually see the little guys. The closest I've come was some years ago, when I was doing work on grasshopper embryos, and sterile technique was a pressing concern. The work was done under a hood that we regularly hosed down with 95% alcohol, we'd extract embryos from their eggs, and we'd keep them alive for hours to days in tissue culture medium — a rich soup of nutrients that was also a ripe environment for bacterial growth. I was looking at the development of neurons, so I'd put the embryo under a high-powered lens of a microscope equipped with differential interference contrast optics, and the sheet of grasshopper neurons would look like a giant's causeway, a field of tightly packed rounded boulders. I was watching processes emerging and growing from the cells, so I needed good crisp optics and a specimen that would thrive healthily for a good long period of time.
It was a bad sign when bacteria would begin to grow in the embryo. They were visible like grains of rice among the ripe watermelons of the cells I was interested in, and when I spotted them I knew my viewing time was limited: they didn't obscure much directly, but soon enough the medium would be getting cloudy and worse, grasshopper hemocytes (their immune cells) would emerge and do their amoeboid oozing all over the field, engulfing the nasty bacteria but also obscuring my view.
What was striking, though, was the disparity in size. Prokaryotic bacteria are tiny, so small they nestled in the little nooks between the hopper cells; it was like the opening to Star Wars, with the tiny little rebel corvette dwarfed by the massive eukaryotic embryonic cells that loomed vastly in the microscope, like the imperial star destroyer that just kept coming and totally overbearing the smaller targets. And the totality of the embryo itself — that's no moon. It's a multicellular organism.
I had to wonder: why have eukaryotes grown so large relative to their prokaryotic cousins, and why haven't any prokaryotes followed the strategy of multicellularity to build even bigger assemblages? There is a pat answer, of course: it's because prokaryotes already have the most successful evolutionary strategy of them all and are busily being the best microorganisms they can be. Evolving into a worm would be a step down for them.
That answer doesn't work, though. Prokaryotes are the most numerous, most diverse, most widely successful organisms on the planet: in all those teeming swarms and multitudinous opportunities, none have exploited this path? I can understand that they'd be rare, but nonexistent? The only big multicellular organisms are all eukaryotic? Why?
Another issue is that it's not as if eukaryotes carry around fundamentally different processes: every key innovation that allowed multicellularity to occur was first pioneered in prokaryotes. Cell signaling? Prokaryotes have it. Gene regulation? Prokaryotes have that covered. Functional partitioning of specialized regions of the cell? Common in prokaryotes. Introns, exons, endocytosis, cytoskeletons…yep, prokaryotes had it first, eukaryotes have simply elaborated upon them. It's like finding a remote tribe that has mastered all the individual skills of carpentry — nails and hammers, screws and screwdrivers, saws and lumber — as well as plumbing and electricity, but no one has ever managed to bring all the skills together to build a house.
Nick Lane and William Martin have a hypothesis, and it's an interesting one that I hadn't considered before: it's the horsepower. Eukaryotes have a key innovation that permits the expansion of genome complexity, and it's the mitochondrion. Without that big powerplant, and most importantly, a dedicated control mechanism, prokaryotes can't afford to become more complex, so they've instead evolved to dominate the small, fast, efficient niche, leaving the eukaryotes to occupy the grandly inefficient, elaborate sloppy niche.
Lane and Martin make their case with numbers. What is the energy budget for cells? Somewhat surprisingly, even during periods of rapid growth, bacteria sink only about 20% of their metabolic activity into DNA replication; the costly process is protein synthesis, which eats up about 75% of the energy budget. It's not so much having a lot of genes in the genome that is expensive, it's translating those genes into useful protein products that costs. And if a bacterium with 4400 genes is spending that much making them work, it doesn't have a lot of latitude to expand the number of genes — double them and the cell goes bankrupt. Yet eukaryotic cells can have ten times that number of genes.
Another way to look at it is to calculate the metabolic output of the typical cell. A culture of bacteria may have a mean metabolic rate of 0.2 watts/gram; each cell is tiny, with a mass of 2.6 x 10-12g, which means each cell is producing about 0.5 picowatts. A eukaryotic protist has about the same power output per unit weight, 0.06 watts/gram, but each cell is so much larger, about 40,000 x 10-12g, that a single cell has about 2300 picowatts available to it. So, more energy!
Now the question is how that relates to genome size. If the prokaryote has a genome that's about 6 megabases long, that means it has about 0.08 picowatts/megabase to spare. If the eukaryote genome is 3,000 megabytes long, that translates into about 0.8 picowatts of power per megabase (that's a tenfold increase, but keep in mind that there is wide variation in size in both prokaryotes and eukaryotes, so the ranges overlap and we can't actually consider this a significant difference — they're in the same ballpark).
Now you should be thinking…this is just a consequence of scaling. Eukaryotic power production per gram isn't any better than what prokaryotes do, all they've done is made their cells bigger, and there's nothing to stop prokaryotes from growing large and doing the same thing. In fact, they do: the largest known bacterium, Thiomargarita, can reach a diameter of a half-millimeter. It gets more metabolic power in a similar way to how eukaryotes do it: we eukaryotes carry a population of mitochondria with convoluted membranes and a dedicated strand of DNA, all to produce energy, and the larger the cell, the more mitochondria are present. Thiomargarita doesn't have mitochondria, but it instead duplicates its own genome many times over, with 6,000-17,000 nucleoids distributed around the cell, each regulating its own patch of energy-producing membrane. It's functionally equivalent to the eukaryotic mitochondrial array then, right?
Wrong. There's a catch. Mitochondria have grossly stripped down genomes, carrying just a small cluster of genes essential for ATP production. One hypothesis for why this mitochondrial genome is maintained is that it acts as a local control module, rapidly responding to changes in the local membrane to regulate the structure. In Thiomargarita, in order to get this fine-tuned local control, the whole genome is replicated, dragging along all the baggage, and metabolic expense, of all of those non-metabolic genes.
Because it is amplifying the entire genomic package instead of just an essential metabolic subset, Thiomargarita's energy output per gene plummets in comparison. That difference is highlighted in this illustration which compares an 'average' prokaryote, Escherichia, to a giant prokaryote, Thiomargarita, to an 'average' eukaryotic protist, Euglena.
(Click for larger image)
The cellular power struggle. a-c, Schematic representations of a medium sized prokaryote (Escherichia), a very large prokaryote (Thiomargarita), and a medium-sized eukaryote (Euglena). Bioenergetic membranes across which chemiosmotic potential is generated and harnessed are drawn in red and indicated with a black arrow; DNA is indicated in blue. In c, the mitochondrion is enlarged in the inset, mitochondrial DNA and nuclear DNA are indicated with open arrows. d-f, Power production of the cells shown in relation to fresh weight (d), per haploid gene (e) and per haploid genome (power per haploid gene times haploid gene number) (f). Note that the presence or absence of a nuclear membrane in eukaryotes, although arguably a consequence of mitochondrial origin70, has no impact on energetics, but that the energy per gene provided by mitochondria underpins the origin of the genomic complexity required to evolve such eukaryote-specific traits.
Notice that the prokaryotes are at no disadvantage in terms of raw power output; eukaryotes have not evolved bigger, better engines. Where they differ greatly is in the amount of power produced per gene or per genome. Eukaryotes are profligate in pouring energy into their genomes, which is how they can afford to be so disgracefully inefficient, with numerous genes with only subtle differences between them, and with large quantities of junk DNA (which is also not so costly anyway; remember, the bulk of the expense is in translating, not replicating, the genome, and junk DNA is mostly untranscribed).
So, what Lane and Martin argue is that the segregation of energy production into functional modules with an independent and minimal genetic control mechanism, mitochondria with mitochondrial DNA, was the essential precursor to the evolution of multicellular complexity — it's what gave the cell the energy surplus to expand the genome and explore large-scale innovation.
As they explain it…
Our considerations reveal why the exploration of protein sequence space en route to eukaryotic complexity required mitochondria. Without mitochondria, prokaryotes—even giant polyploids—cannot pay the energetic price of complexity; the lack of true intermediates in the prokaryote-to-eukaryote transition has a bioenergetic cause. The conversion from endosymbiont to mitochondrion provided a freely expandable surface area of internal bioenergetic membranes, serviced by thousands of tiny specialized genomes that permitted their host to evolve, explore and express massive numbers of new proteins in combinations and at levels energetically unattainable for its prokaryotic contemporaries. If evolution works like a tinkerer, evolution with mitochondria works like a corps of engineers.
That last word is unfortunate, because they really aren't saying that mitochondria engineer evolutionary change at all. What they are is permissive: they generate the extra energy that allows the nuclear genome the luxury of exploring a wider space of complexity and possible solutions to novel problems. Prokaryotes are all about efficiency and refinement, while eukaryotes are all about flamboyant experimentation by chance, not design.
Lane N, Martin W. (2010) The energetics of genome complexity. Nature 467(7318):929-34.
31 Comments
bigjohn756 · 28 December 2010
Unfortunately I didn't understand any of this, but I attribute that to the sauzamargaritas I was drinking.
PZ Myers · 28 December 2010
Every time someone says they don't understand something I wrote, I cry a little deep down inside. Why do you hate me so?
mrg · 28 December 2010
Ah, it's esoteric, but not that bad. I'm not a biologist but I could half-follow it. I'll come back later and pick up the other half.
Rugosa · 28 December 2010
Cheer up, PZ. I understood the gist of it. Your science writing is terrific - you help the reader follow the more technical details.
Chris Caprette · 28 December 2010
Mike Elzinga · 28 December 2010
There are some physics perspectives that fall into the “consider a spherical cow” category of explanations.
Whenever a condensed matter system grows in complexity, any energy-driven organization and coordination emerges within that system depends not only on the influx of energy through the surface of the system, but the flow of energy into the interior of the system as well as any outflow necessary to maintain a flux of energy (and matter) within the interior.
And it is the flow of energy that maintains any coordination and organization. If there are large differences within the system (diffusive and conductive pathways are heavily dependent on structure and coupling among the constituent parts of the system) then one would expect to see completely different processes capable of being sustained in different parts of such a system, and the system begins to look more like a composite system.
Now that’s ok provided that such differences contribute to an over all system that survives selection within a larger environment. And that is the cool thing about this because whatever falls out has not been planned ahead; it is just one of the composite systems that keep functioning in the given environment.
So we can almost begin to see the bridge between abiogenesis and living systems sorted by natural selection.
Gary Hurd · 28 December 2010
Interesting idea. Thanks for the summary. I also enjoyed your "fisking" of Oklahoma's latest elected moron, Mr. Breechen. I have been pounding on him in his hometown newspaper.
Ironoically, it is called the The Durant Daily Democrat.
Doc Bill · 28 December 2010
I'm not even a biologist but I understood the whole thing!
Bacteria are like rice, right?
(Sort of puts me off my sushi, I must say.)
ckc (not kc) · 28 December 2010
...made sense to me (but a megabyte has stolen into your megabases)
Mike Elzinga · 29 December 2010
Wheels · 29 December 2010
Hope that's clear enough to be heard in Margaritaville.
Ichthyic · 29 December 2010
I have been pounding on him in his hometown newspaper.
I just read that article by Bleached-brain.
holy.
crap.
I can't recall seeing anything quite that stupid coming out of the mouth of an actual elected senator before.
I've seen similar, incoherent, garbage coming from the mouths of 12 year old creationists (and I can provide the link)!
jaw droppingly inane.
Glad you did such a thorough job there, but sweet plastic bobbleheaded JESUS!!
that guy will probably only understand about 10% of the words you wrote, let alone the content, even IF he reads it.
wow.
That guy makes IBIGGY look SMART!
IanW · 29 December 2010
Hey! Leave PZ alone - he's blogging science for a change and he needs to be encouraged in that!
jkc · 29 December 2010
Gary Hurd · 29 December 2010
PS: If you of you guys happens to be "knethrea" you should really chill with the ""Holy Book" of Stupid" which only alienates Christians like "scrappymom" who would otherwise be an ally.
mrg · 29 December 2010
Gary Hurd · 29 December 2010
Dale Husband · 29 December 2010
mrg · 29 December 2010
harold · 29 December 2010
On the subject of multicellularity...
Nucleated human cells tend to have diameters of between 10 and 100 microns. The range of sizes of metazoan cells is greater. Bacteria that live in the human body have various shspes, but cocci tend to be be around 2 microns in diameter, and except for some smaller obligate intracellular pathogens, they're all in the same ballpark. Infection causing free living amoebae are eukaryotes and are in the same size range as human cells.
Being mainly familiar with human cells and pathogens, I tend to think that there is a "size gap" between eukaryotic, or at least metazoan, cells and prokaryotic cells. The typical "pond water" unicellular harmless eukaryotic microbes tend to be in that range, too.
However, in fact, a fair number of eukaryotic single celled algae are in the 2-3 micron diameter range.
As far as I know, though, there are no multicellular organisms that are composed of very small individual cells. Being a eukaryote may not be as strongly associated with "large" cells as I once mistakenly thought, but multicellularity seems to be.
william e emba · 29 December 2010
Nick Lane has written three popular science books, all highly recommended. His most recent Life Ascending identifies the ten biggest evolutionary innovations. Along the way, he includes a less technical explanation of the Lane-Wilson hypothesis, so for those who found PZ's description too hard to follow, Lane himself is probably more accessible.
Shorter summary: just read his three books.
James Downard · 29 December 2010
Fine commentary on the Lane/Martin hypothesis, PZ ... and thanks too for the link to the Brecheen articles. It does illustrate the pitfalls of Tortucans elected to public office, doesn't it?
Besides Valentine's fine book on the phyla origin issue, I might toss in the case Conway Morris & Caron (2007) Science 315:1255-1258 make for linking up no less than three phyla with one common early Cambrian ancestor. Like all secondary citation addicts, though, Brecheen is unlikely to venture into reading primary work even when prodded.
Eric Means · 29 December 2010
I'm a lurker on this blog, an electronics engineer with a late-in-life-to-awaken fascination for evolutionary biology. Very happy to see Nick Lane's books cited here. I've gobbled up most of the popular science books on evolution in recent years, and Lane is hands-down my favorite author.
PZ Myers does an excellent job of summarizing Lane's idea here. I'd be interested to read others' opinions of Lane's musings on the origin of life from deep sea vents. The biochemistry, the geology, etc. Do his ideas hold water?
mrg · 29 December 2010
Rich Blinne · 31 December 2010
DS · 31 December 2010
amphiox · 31 December 2010
Lane addresses the issue of genome size/speed of cell division with respect to this question in his books.
Rich Blinne · 1 January 2011
harold · 5 January 2011
Is this thread still alive? I'm sure PZ is 200 posts beyond this on Pharyngula.
Modern prokaryotes seem to experience or be descended from lineages that experienced very high negative selection for large genomes, and in particular, for non-coding DNA.
I say this because, for the most part, they don't have any significant amount of non-coding DNA. In fact, they're more likely to have overlapping genes.
They are also all haploid.
They also have mechanisms for extensive lateral genetic transfer, such as plasmids. Plasmids don't really seem to be parasitic or infectious to speak of. Lateral transfer occurs in eukaryotes, but often due to viruses.
Eukaryotes are fundamentally diploid. There are polyploid forms and there are haploid forms in some lifecycles but they aren't fundamentally haploid.
Diploidy may be as much of an issue as anything else here. With a "backup" copy of every gene, a lot more variance is tolerable.
Michael · 6 January 2011
I was always afraid of something like this happening: it turning out that a proper understanding of what the frell is going on in biology requiring economic reasoning.
Mark R · 22 January 2011