Chapter 7
A Concise History of Life on Earth
In 1969, Carl Woese (1928–2012), then a young professor at the University of Illinois, came up with an unusual way to investigate phylogeny, the study of the interrelatedness of organisms, and in doing so uncovered a rather surprising result. For the preceding century, biologists had categorized life into five kingdoms: four eukaryotic (cells with nuclei) kingdoms comprising animals, plants, fungi, and single-celled protists, and a single prokaryotic (cells lacking a nucleus) kingdom, the bacteria. This classification, which was based on gross cellular features, came about in part because it seemed a natural assumption from our perspective as big, lumbering eukaryotes that the major divisions of life on Earth would be weighted heavily toward us and our close cousins. Woese’s ambition was to probe the relatedness of these kingdoms in more detail and to settle the question, once and for all, as to how bacteria fit into the bigger picture.
Because bacteria don’t have gross structural features, such as hair or scales, that can be easily compared, Woese realized that he would have to study phylogeny at the molecular rather than the cellular or organismal level. Even as late as the late 1960s, though, biologists had depressingly few molecules with which to perform such comparative molecular biology; at the time, the atomic-resolution structures of only about 10 proteins were known,* along with the amino acid sequences of a few dozen more. Even simply establishing the sequence of a small protein took years of effort, and there were no viable methods for sequencing genes, much less entire genomes. How, then, could one compare organisms on a molecular level and work out their evolutionary relationships beyond those that are obvious from outward appearance?
To start, Woese needed a molecule that is present in, and thus could be compared across, all living things. As all cellular organisms employ ribosomes to make their proteins, he chose the RNA strand of the small ribosomal subunit, known as the 16S RNA in bacteria. Reading the nucleotide sequence of the molecule was well beyond the technology of the day, so he shredded the molecule instead. More specifically, he digested the ribosomal RNA with an enzyme that cuts after guanosine (G), and only after guanosine. The resulting fragments, short enough to be sequenced with available methods, would all constitute “words” ending with G (and only containing that one G): AUG, CG, ACACACUUG, and so on.
After sorting the fragments by their length (using gel electrophoresis, a well-established method of separating molecules according to size), sequencing some of them, and thinking about the results, Woese found that the most useful words were those of six letters or more—shorter words were too common to provide clues as to who was related to whom. There are 35 = 243 different six-letter words ending in G, and a typical 16S RNA contains around 25 of them. These short words thus provided good enough statistics to allow Woese to “fingerprint” organisms by their 16S RNA and to use these fingerprints to map out which organisms are most closely related.
Over many years, Woese and his graduate students compiled the “dictionaries” of 16S RNA words from different bacterial species and constructed family trees based on the degree of identity between the content of the dictionaries. To their surprise, a subset of the bacteria they studied—those that produce methane—turned out to be just as distantly related to other bacteria as they are to elephants, guinea pigs, or ourselves. Woese proposed that these microbes represented a new branch on the tree of life, equal in stature to the Eukarya and Bacteria, and he called this third branch the Archaebacteria (later shortened to Archaea, with an individual member of the group called an archaeon) because it seemed to represent an “ancient” form of life.
As mentioned in chapter 6, we now regard the domains of Archaea and Bacteria as the direct offspring of LUCA and the more complex eukaryotic cells as a later recombination of representatives of these two ancestral domains. But, back in the 1970s, the idea was heretical. After all, Woese’s new-fangled “molecular fingerprinting” aside, archaea and bacteria look very similar from the perspective of us big, multicellular organisms, so, naturally, Woese’s arguments were rejected more or less out of hand by many microbiologists. Only the small and initially marginal community of researchers exploring life under extreme physical conditions (see chapter 8), including the German biologists Holger Jannasch (1927–1998) and Karl-Otto Stetter, embraced the new order. It was not until the late 1990s, when the first archaeal genomes were sequenced, that Woese’s claim that Archaea was a separate realm of its own and that life is better divided into two prokaryotic and one eukaryotic “domain” rather than four eukaryotic and one prokaryotic “kingdom” finally prevailed over the earlier, more traditional view. With literally thousands of gene sequences available, comparative molecular studies demonstrated quite compellingly that Woese was correct, and the archaea are, if anything, more distant from bacteria than they are from us. The wheels of science sometimes turn slowly, but turn they do.*
The Emergence of Life on Earth
On the one hand, the history of life on Earth is a bit of a parochial topic for wide-ranging types like us astrobiologists. Clearly, for example, the division of Terrestrial life into three domains would hardly be of relevance to the study of, say, life (if there is any) on Jupiter’s moon Europa. On the other hand, the history of how the story unfolded here on Earth is the only example we have so far, so if we’re careful not to be complacent and fall into thinking that how it occurred on Earth is the only way it could have occurred here or anywhere else, the topic seems worthy of serious consideration.
How and when did the history of life on Earth unfold? Although the Earth formed some 4.56 billion years ago and its crust solidified a few tens of millions of years later, after the formation of the Moon (see chapter 3), it was effectively uninhabitable for a long time after that. It was not until some 3.8 billion years ago that the late heavy bombardment and its planet-sterilizing impacts came to an end. The question, then, is, how quickly after the end of the late heavy bombardment did life arise on our planet?
The answer to this question is obscured, at least in part, by our lack of detailed knowledge of the Earth’s early history. Even after the end of its turbulent formative years, the Earth remained (and remains) a highly dynamic planet, and few records of its early days have survived intact. Due to the incessant erosion brought on by the Earth’s hydrological cycle and plate tectonics constantly recycling crust into the mantle, typical rocks on the surface of our planet are estimated to have a half-life of only a few hundred million years. The chances of the Earth’s first rocks, those dating from the so-called Hadean eon, surviving this gauntlet and remaining unscathed from their formation up to the present approach zero. Despite significant effort on the part of geologists, only one or two rock outcrops have been reported to be much older than 4 billion years, with the oldest reported (the validity of this is debated) clocking in at 4.28 billion years. It is really only from the Archaean eon, which started 4 billion years ago, that any significant geological record has been preserved. (See table 7.1 for a time line of the geological intervals in relation to the history of life on Earth.)
The oldest known Earth rocks come from several locations in the far north of North America, with the oldest, well-accepted age being associated with the Acasta gneisses (metamorphosed igneous rocks, i.e., rocks that originated from molten material and were later altered) found near Great Slave Lake in northern Canada. Unfortunately, though, during the 4.03 billion years since these rocks solidified, they have been modified by heat and pressure to such an extent that they provide little information on what the Earth was like that early in its youth. More critical to our story are the somewhat younger, apparently supracrustal rocks of Isua and Akilia, West Greenland. The “supracrustal” tag denotes that these metamorphosed rocks were deposited as sediments or volcanic flows in shallow water when they were formed, some 3.7 to 3.8 billion years ago. If this mineralogical assignment is correct, these rocks confirm that liquid water (viewed, of course, as critical for the formation of life) existed on Earth at that time. But was there life in this water?
Sediments are formed from a steady rain of material—both organic and inorganic—that settles out of the water, so they provide an ideal place to look for signs of past life. Perhaps consistent with this, the Isua and Akilia rocks contain small globules of graphite, the pure carbon form used in pencil “lead.” Is this evidence that life was flourishing more than 3.7 billion years ago? As it contains only carbon and none of the other chemical elements necessary for life, graphite is not usually associated with biology. On the other hand, this graphite might be. The reason is that the Isua and Akilia rocks are also significantly metamorphosed; had they originally contained life, the organic carbon would have been dehydrogenated to form graphite when the rocks became buried and “cooked” deep within the Earth. Based on this argument, the German geologist Manfred Schidlowski (1933–2012), and later the American geochemist Stephen Mojzsis, suggested that the carbon extracted from these rocks might have been derived from living things. Mojzsis, then a graduate student at the Scripps Institution of Oceanography working under Gustaf Arrhenius (grandson of Svante Arrhenius of panspermia fame; see chapter 5), characterized the ratio of the carbon isotopes 12C and 13C in these ancient materials by heating the rock and analyzing the carbon compounds that were driven off. What he found was carbon depleted in the heavier isotope as is observed today in the organic molecules produced by photosynthesis! (The more rapidly moving, lighter carbon isotope is preferentially “fixed” in the photosynthetic reaction.) Thus, Mojzsis suggested, not only had life arisen at the time the original rock was deposited—just a few hundred million years after the crust cooled and smack at the end of the late heavy bombardment—but it had evolved to such a high degree of complexity that photosynthesis was already a common form of metabolism.
Table 7.1
A chronology of life on Earth
Geological eon/era/period (starting age, years ago) |
|
Time (years ago) |
What was happening? |
|
Hadean eon (4.56 billion) |
|
|
4.56 billion |
Accretion of the Earth |
|
|
4.53 billion |
Formation of the Moon |
|
|
|
4.28 billion |
Oldest claimed Earth rocks still in existence (not widely accepted) |
|
|
|
4.03 billion |
Oldest Earth rocks still in existence (widely accepted) |
|
Archaean eon (4 billion) |
|
|
~3.8 billion |
End of late heavy bombardment; oldest claimed evidence for life on Earth (not widely accepted) |
|
|
>3.77 billion |
Oldest claimed microfossils (not widely accepted) |
|
|
|
~3.6 billion |
Formation of first continents |
|
|
|
~3.4 to 3.5 billion |
Reasonably accepted evidence for life (stromatolites, microfossils, isotopic signatures) |
|
|
|
3.2 billion |
Fully accepted evidence for life (microfossils, stromatolites) |
|
Proterozoic eon (2.5 billion) |
|
|
~2.4 billion |
Great oxygenation event |
|
|
1.65 to 2.2 billion |
First recognizably eukaryotic fossils |
|
|
|
~1.1 to 1.7 billion |
Divergence of major eukaryotic lineages |
|
|
|
>1 billion |
Invention of sex |
|
|
|
1.05 billion |
Oldest multicellular eukaryotic algae fossil |
|
|
|
560 million |
Oldest widely accepted animal fossils |
|
Phanerozoic eon (541 million) |
Paleozoic era (541 million) |
Cambrian (541 million) |
|
Atmospheric oxygen reaches about half of current level; Cambrian “explosion” |
Ordovician (485 million) |
|
Cephalopods and jawless fishes rule the oceans; fossilized arthropod footprints |
||
Silurian (444 million) |
|
Diversification of the bony fish; land plants; spiders and scorpions |
||
Devonian (420 million) |
|
First land vertebrates (amphibians) |
||
Carboniferous (359 million) |
|
Forests of tree ferns; first reptiles |
||
Permian (299 million) |
|
Period ends with largest recorded mass extinction |
||
Mesozoic era (252 million) |
Triassic (252 million) |
|
Origin of dinosaurs (and mammals) |
|
Jurassic (201 million) |
|
Beginning of the age of dinosaurs; first birds (which are a dinosaur lineage) |
||
Cretaceous (145 million) |
|
Origin of flowering plants |
||
Cenozoic era (66 million) |
Paleogene (66 million) |
66 to 20 million |
Mammals diversify after dinosaur extinction event |
|
Neogene (23 million) |
20 to 3 million |
Climate cools; grasslands expand |
||
~6 million |
Human-chimp divergence |
|||
Quaternary (2.58 million) |
2.1 million |
Rise of Homo erectus |
||
0 million |
You’re reading this |
|||
But are these putative indications of life, and possibly even photosynthesis, on a firm footing? Within only a few years of the publication of Mojzsis’s investigations, other researchers began to question the evidence on many grounds. First, the seemingly telling graphite occurs in veins of carbonate rock that were probably formed by the injection of hot fluids when the older host rocks were buried deep within the Earth, perhaps long after they were initially formed. Second, the isotopically odd carbon was released at a temperature far too low to be from the graphite (which has the highest vapor point of any element) and thus could well be a more recent contaminant. Third, known abiological chemical processes can produce carbon similarly depleted in the element’s lighter isotope. Finally, even the age of the relevant rocks has been questioned (see sidebar 7.1)—in fact, by members of Mojzsis’s original research team—as has the original identification of the Isua and Akilia rocks as sedimentary (sediments are a great place to collect fossils; other rocks are not). It’s probably safe to say that, at best, the jury is very much still out regarding the evidence for life in these 3.8-billion-year-old rocks.
Similar, if still debatable, evidence for life is claimed in studies of the Nuvvuagittuq supracrustal belt in northeastern Canada, a geological formation consisting of layers of basalt that, as described above, are debatably dated to around 4.28 billion years, and sediments dated to at least 3.77 billion years. The group of Dominic Papineau at University College London, UK, and others have analyzed the putative sediments, which, with the basalt, they believe formed the floor of an ancient ocean, and found chemistry that they argue is consistent with the rocks having formed in a hydrothermal vent environment. Looking closely, the researchers identified tubes and filaments of the iron oxide mineral hematite that exhibit the characteristic branching seen for filamentous, iron-oxidizing bacteria found near hydrothermal vents today, suggesting that these might be microfossils. The researchers also identified isotopically light carbon (as Mojzsis reported for the Greenland rocks) in both carbonates and in graphite. Anticipating the usual criticism that abiotic processes might be responsible for these structures, the authors rather bluntly argue that, “Collectively, our observations cannot be explained by a single or combined abiogenic pathway, and therefore we reject the null hypothesis.”* Their confidence notwithstanding, the paleontological community remains far from consensus regarding the merits of their claims.
If the evidence for life at 3.8 billion years ago is contentious, how much more recently do we have to go before the evidence becomes firmer? Perhaps not much. In 1993, William Schopf, a professor of paleobiology at the University of California, Los Angeles, described 3.46-billion-year-old specimens from Western Australia (near a fiercely hot mining center, ironically named North Pole) that seemed to contain microscopic, tar-colored fossils of bacteria. The tiny organisms were encased in chert, an extremely fine-grained rock composed of silica that can preserve the smallest of details. Schopf sorted the bacteria into 11 taxa, or distinct groupings, based on the shapes of the fossils and claimed that, in terms of their shape, seven appeared to be early relatives of cyanobacteria. Raman spectroscopy of the samples, which crudely identifies molecular components, indicated that the tar-like substance defining the fossils was kerogen, a complex mixture of hydrocarbons that is typically produced when biological material is subjected to heat and pressure beneath the Earth’s surface. Taken together, Schopf claimed, this provided incontrovertible evidence that complex ecosystems, likely to consist of multiple species of photosynthetic cyanobacteria, existed as early as about 300 million years after the end of the late heavy bombardment.
Following up on Schopf’s claims, Donald Canfield and coworkers at Odense University in Denmark studied sulfur isotopic fractionation in the same rocks and found possible biogenic signatures in the sulfur-containing mineral barite. If their identification proves correct, it would both confirm the existence of life at 3.46 billion years ago and identify one of its key metabolic reactions: namely, the use of the electrons in sulfate (SO4−2) to oxidize hydrogen or hydrocarbons to produce sulfide (S−2) and water or carbon dioxide.
Schopf’s claims, however, have also found critics. One criticism, raised by Martin Brasier (1947–2014) of Oxford University, takes aim at the ambiguous shapes of the putative fossils; of the thousands of inclusions in the rocks, only a tiny fraction of them look like cyanobacteria or, indeed, any contemporary bacteria. Of course, although they fossilize better than other bacteria, cyanobacteria do not fossilize well, especially if they degrade between death and fossilization. A second criticism, also raised by Brasier, is that Schopf misunderstood the geology of the supposed microfossils, which were preserved not in marine sediments, which would have collected fossils, but rather in a hydrothermal vent or even in volcanic glass, in which fossils are much less likely to form. Once again, it seems that the jury is out on whether these are real microfossils, and if so, whether they are cyanobacteria, although the case in favor of life’s remnants in these rocks seems significantly better established than the case for earlier life described above.
If even the evidence for life at 3.46 billion years is contested, when does the evidence for life on Earth become incontrovertible? That’s not such an easy question to answer. As we move forward in the geological record, we see only slowly mounting evidence, without ever finding any single, incontrovertible “smoking gun.” For example, 3.43-billion-year-old sedimentary layers in Strelley Pool, Western Australia, a few tens of kilometers away from the North Pole site, contain abundant, stromatolite-like formations (we discuss stromatolites—fossilized bacterial colonies—in more detail below) that look very similar to stromatolites frequently found in more recent geological settings and are thought to have formed in shallow marine environments. Given their abundance and preservation, there appears to be a reasonable degree of consensus among paleontologists that these strata are convincing evidence of life. They lack, however, any identifiable microfossils, which would help clinch the argument. In contrast, as we move still further forward in the rock record, we see more and more of what looks like microfossils, although this perhaps is not so much because the putative organisms had become more plentiful but rather because the rocks themselves becomes more plentiful. There are fine-grained, 3.40-billion-year-old cherts from South Africa, for example, that preserve many bacteria-sized spheres, some of which seem to have been caught in the process of dividing. And in early 2000, the Australian geologist Birger Rasmussen, now at Curtin University, Bentley, Western Australia, reported convincingly lifelike microfilaments in 3.2-billion-year-old Australian hydrothermal deposits.
The First Complex Ecosystems
Cyanobacteria seem to have invented the first organized supracellular structures and, with them, the oldest widely accepted fossils: the stromatolites we mentioned above (fig. 7.1). Stromatolites, dome-shaped or conical sediments of very finely layered sedimentary rock that can reach heights of decimeters to meters, are a dominant feature of many Precambrian sedimentary rocks. Today, however, living examples are rare and are limited to select niches, such as waters that are too saline to allow animals to eat or otherwise disrupt them. With the rise of animals, it turns out that growing as a delicate and defenseless (and perhaps tasty) mat of bacterial cells is not as successful a lifestyle as it once was.
Figure 7.1 The edge of an author’s shoe (left) on top of some billion-year-old stromatolite fossils in Glacier National Park in America’s Rocky Mountains.
Hamelin’s Pool, in Shark Bay on the coast of Western Australia, is just such a niche. In this hypersaline bay, which is twice as salty as seawater, stromatolites thrive, providing an opportunity to see in detail how their ancient brethren might have formed. Here, complex communities of microorganisms, usually cyanobacteria along with other bacteria and some microbial eukaryotes, spread out in coherent mats across the surface of sediments or rocks. The cells produce a thick, mucus-like material that glues them to one another and affixes them to the substrate. The mucus also traps fine sediments carried in the waves and currents. As this layer of sediment accumulates, the cells grow or migrate upward in order to continue photosynthesis. Cells remaining behind are cut off from the light and die. Other organisms consume the organic material from the dying cyanobacteria, in turn liberating carbon dioxide. The carbon dioxide reacts with water to form carbonic acid, which binds calcium and precipitates out as a layer of limestone.
The oldest putative stromatolite fossils are those found in the 3.43-billion-year-old rocks of Strelley Pool, a site that, ironically, is just 800 km northwest of the stromatolites living today in Hamlin’s Pool. And while the biological interpretation of these formations remains at least a bit contentious, it is hard to see how nonbiological processes, such as sedimentation or precipitation, could create such steeply sloping, conical layers. Thus, as we noted above, there is a fair degree of consensus regarding the biological origins of the Strelley Pool stromatolites despite their lack any clear microfossils. In contrast, the stromatolite fossils that become increasingly common over the early part of the Proterozoic eon, from about 2.5 to 1.6 billion years ago, often contain fairly convincing microfossils. These dominate the fossil record until some 600 million years ago, just before the end of the Proterozoic and the start of the Cambrian explosion, during which, as we describe below, animals proliferated and presumably began to graze on the stromatolites or, at the very least, disturb them by crawling over them and disrupting their fragile organization.
Photosynthesis Changes the World
Sunlight interacts with living organisms in a wide variety of ways. On the simplest level, the sunlight that hits the dayside of our planet delivers an energy flow of more than 170,000 TW (a terawatt equals a trillion watts), corresponding to the electricity output of 200 million nuclear power stations. Even though nearly one-third of this energy is reflected straight back into space, the other two-thirds stays with us and keeps us warm. It is the biggest contribution to our planetary energy balance by more than three orders of magnitude (followed by geological heating, human activity, and tidal friction). All life-forms, including the earliest and most primitive ones, must have benefited from this heat supply as it raised the surface temperature of our planet into the range that allowed water to remain liquid and life to originate and evolve.
At the most sophisticated level, light reflected from objects around us allows us to perceive our environment with our eyes. Although it is a relatively recent development compared with the evolutionary timescale dominated by bacteria, it appears that evolution is reasonably efficient at discovering and rediscovering vision. Enough so that the ability has arisen independently many times over the course of animal evolution. Octopus eyes, for example, look remarkably like our own despite the fact that the last common ancestor we shared with our excessively armed friends is thought to have been sightless.
Between these two uses of light—one very general, the other highly specific—evolution developed a third, equally important way of making use of light, thereby starting a revolution that arguably changed the nature of life on Earth more than any other single event since its origins. At some point, a group of bacteria, probably most closely related to today’s cyanobacteria, came up with the two-step photosynthetic method that uses the energy of light to pull electrons from water, creating oxygen in the process.
The selective pressures in favor of photosynthesis are clear: quite simply, as LUCA and her offspring consumed the various reduced materials that were available in the environment, eventually a new source of energy had to be found. Less clear is how the modern photosynthetic apparatus might have arisen in the first place. As any student who has tried to memorize it will remember, the standard photosynthetic apparatus is incredibly complex. It must have evolved in a stepwise fashion from simpler mechanisms that already harvested sunlight without necessarily producing oxygen. Fortunately, some of the simpler (and presumably older) versions of bacterial photosynthesis are still around today and can help us understand how life came up with this new technology.
The simplest and best understood light-harvesting system is that of the extremely halophilic (salt-loving) archaea from the genus Halobacterium. The membranes of these cells contain characteristically colored patches known as the purple membrane. Its main component is a remarkably robust protein, bacteriorhodopsin, which uses light to pump protons out of the cell. With this activity, it creates a proton gradient across the membrane, which is a primitive means of storing the energy in an electrochemical form. Another membrane protein, called the F-ATPase, uses this proton gradient to drive the synthesis of the energy currency ATP (adenosine triphosphate). This mechanism constitutes a relatively inefficient, “hand-to-mouth” use of solar energy as it creates chemical fuel but no permanent chemical bonds, so it doesn’t count as full-fledged photosynthesis.
In contrast, five major groups of bacteria have learned how to use the energy of sunlight to obtain the reducing potential (again, high-energy electrons) needed to synthesize carbon-containing molecules. Four of these do so without producing oxygen in the process. These are the Chlorobiaceae (green sulfur bacteria), Thiorhodaceae (purple sulfur bacteria), Chloroflexaceae (green nonsulfur bacteria), and Athiorhodaceae (purple nonsulfur bacteria, including Rhodopseudomonas viridis, which provided the first ever atomic-resolution structure of a photosynthetic reaction center). Like green algae and the higher (eukaryotic) plants, these non-oxygen-producing photosynthetic bacteria use light to drive a redox reaction that reduces carbon dioxide (carbon at oxidation state +4) to carbohydrates (carbon at oxidation state 0).* In green algae and the higher plants, the ultimate source of the electrons is water (oxygen at oxidation state −2), which is oxidized to molecular oxygen (O2 at oxidation state 0). By contrast, the sulfur bacteria use sulfides as the electron source (leaving elemental sulfur as waste), and the nonsulfur photosynthetic bacteria employ hydrogen and small, reduced carbon compounds such as isopropanol. These materials are so easily oxidized that the energy of a single photon is sufficient to extract electrons from them, and thus only a single copy of the photosynthetic machinery (called a “photosystem”) is required to exploit them.
Although sulfides and hydrogen are easy to oxidize and were probably abundant in the relatively reduced environments available on the young Earth, they were ultimately in limited supply, and, when they ran out, photosynthetic organisms found themselves in need of a new source of electrons with which to reduce carbon dioxide. A promising, if rather ambitious, solution to this problem was to use water as the reductant since its relatively unfavorable oxidation potential is balanced by its extremely favorable abundance. But there was a hurdle to overcome: oxygen, the second most electronegative element, has a very high affinity for electrons, and thus water holds its electrons so tightly that the energy in a single photon of visible light cannot wrest them free. Cyanobacteria—the fifth, final, and most successful group of photosynthetic microbes—came up with the solution to this by linking two photosystems in series, each of which can trap one photon and convert its energy into chemical energy (fig. 7.2). This allows the energy in two photons to be summed in order to achieve the oxidation of water to oxygen and the efficient exploitation of the liberated electrons and protons.
The resulting light-driven “two-stroke engine” is one of the most complicated molecular machines we know. Essentially, the light energy captured by the chlorophyll molecule of photosystem II (PSII) lifts an electron to a higher energy level. In a slower reaction, the resulting “hole” is filled with an electron pulled from water (ultimately, after four electrons have been sequentially removed from two water molecules, releasing O2). A pair of high-energy electrons flows from PSII down a cascade of reactions with the overall effect that the electrons are ultimately transferred to photosystem I (PSI), with the net production of one molecule of ATP. And while some of each electron’s newfound energy is given up to form the ATP, it still arrives at PSI in a more energetic state than it had in the water molecule. In the second light reaction, the active center of PSI absorbs a photon and lifts this now higher-energy electron to a still higher energy state. The electron, combined with a proton derived from the split water molecule, can then reduce the redox carrier NADP+ to form NADPH, the ribonucleotide that stores reduction potential in all cells.
Figure 7.2 A simplified overview of the photosynthetic apparatus. The water-splitting reaction (bottom left) provides the electrons, which eventually serve to reduce NADP+ to NADPH (top right). This process produces an excess of protons on one side of the membrane and consumes them on the other. In parallel, electron transport drives the movement of still more protons across a membrane. The resulting concentration gradient later drives ATP synthesis. (PSI and PSII are photosystems I and II, respectively.)
In the next step of photosynthesis, NADPH moves over to the “dark reactions” (called this because they do not directly require the input of light), where its reduction potential is used in the Calvin cycle to “fix” carbon dioxide into reduced compounds that the cell can use. This biochemical cycle is named after its discoverer, Melvin Calvin of the University of California, Berkeley, whose early prebiotic chemistry studies we discussed briefly at the beginning of chapter 4. Calvin and his team elucidated the dark reactions of photosynthesis using radioactive 14C to trace the path of carbon from carbon dioxide to the final sugar in what was one of the first instances of using a radioactive tracer in biochemistry. His work in this area, for which he won the 1961 Nobel Prize in Chemistry, was aided by the fact that 14C was first synthesized at the Berkeley synchrotron just a few years earlier.
The Calvin cycle fixes carbon dioxide by covalently attaching it to the sugar ribulose-1,5-bisphosphate, splitting the sugar into two 3-phosphoglycerate molecules. The 3-phosphoglycerate is, in turn, reduced to glyceraldehyde-3-phosphate, from which the fixed carbon enters a complex metabolic shuffle among 10 sugar intermediates in all. Ultimately, for each six carbon dioxide molecules that enter the pathway, two glyceraldehyde-3-phosphates are split off (to serve as the starting material for the synthesis of other sugars, such as the hexoses, as well as amino acids, nucleobases, and all the other carbon-containing molecules the organism needs), and one molecule of ribulose-1,5-bisphosphate is regenerated. The latter allows the cycle to start anew. Overall, the formation of one six-carbon hexose, such as glucose, requires 12 molecules of NADPH, which in turn were synthesized from 24 electrons (generated using 48 photons) from the light reactions.
Comparison of cyanobacterial photosystems with those of the more primitive bacteria mentioned above shows that those of the green bacteria resemble PSI, while those of the purple bacteria resemble PSII. Studies of the similarities and differences among the various photosynthetic systems suggest an evolutionary history. Photosystems I and II arose in different branches of the bacterial family tree. The ancestors of modern cyanobacteria first had just one of these systems and only later acquired the second by horizontal gene transfer (cyanobacteria are notoriously efficient at pirating genes). After acquiring the second system, they managed to couple the two in a manner that enabled them to use water as a reductant.
The “Great Oxygenation Event”
The invention of photosynthesis and the subsequent advent of our oxic atmosphere had wide-ranging consequences for the anaerobic bacteria that until then ruled the biosphere. Indeed, the advent of an oxygen atmosphere—the “great oxygenation event”—has been called the greatest environmental catastrophe in the history of our planet, a catastrophe that killed off many branches of the tree of life and pruned back many others to a few anaerobic niches (anoxic mud, for example). The change was sufficiently drawn out, though, that there was time for some life to adapt to oxic conditions and, indeed, to benefit from the new opportunities it created.
The geological record provides a history of free oxygen on Earth, although one that remains the subject of significant debate among geologists.* Most experts believe that oxygen levels were quite low before about 2.2 billion years ago—at the time, the Earth’s atmosphere had presumably evolved away from its more reduced starting point but had become neutral rather than oxidized. Specifically, uraninite and pyrite (uranium and iron minerals, respectively) present in ancient “fossilized” river deltas provide the key evidence. These minerals are soluble in oxygen-rich water and would not have survived the trip downriver if the oxygen concentration were even a tiny fraction of today’s value. Similarly, James Farquhar of the University of Maryland has noted that the isotopic ratios in sulfates found in rocks provide a clue as to the free oxygen content of the Earth’s early atmosphere: photochemical reactions can shuffle the isotopic composition of atmospheric sulfur dioxide in a characteristic manner, but free oxygen would destroy the pattern before the sulfur could make it down to the surface to become locked into rocks. Based on this, Farquhar argues that the free oxygen concentration in the atmosphere could not have risen above a paltry one part per million before some 2.4 billion years ago.
A final line of evidence was the formation of banded iron formations, a process that started more than 3 billion years ago and lasted for at least a billion years. These enormous formations consist of alternating layers of red ferric oxide (rust) and the white silicate mineral chert and serve, incidentally, as the dominant commercial source of iron today. They form when highly soluble ferrous iron (Fe+2) is oxidized to ferric iron (Fe+3), which in turn forms an insoluble precipitate—as anyone who’s tried to wash rust off a car well knows. Current thinking is that banded iron formations represent the global transport of iron in the ancient ocean to sites where oxygen was being produced (by photosynthesis, or photolysis of water in the atmosphere, or perhaps both), oxidizing the iron and causing it to fall out of solution. After about a billion years or so, the ocean’s iron became depleted and the formation of banded iron formations stopped. No doubt linked to this depletion, oxygen levels seem to have started a rapid rise some 2.4 billion years ago, up to a few percent of total atmospheric pressure. Perhaps in concert with plants’ colonization of land, another large increase in oxygen began about 500 million years ago, leading, over a few hundred million years to oxygen levels of 20% to 30% (as compared to the current value of 21%).
The Evolution of Aerobic Metabolism
In learning how to turn sunlight, carbon dioxide, and water into carbohydrates and oxygen, the ancestors of cyanobacteria created new ecological niches that were probably quickly filled by organisms running the reverse reaction: burning carbohydrates to produce energy. That is, oxygen-producing photosynthesis paved the way for oxygen-consuming metabolism, including our own. This, in turn, provided the metabolic basis for the evolution of multicellular organisms. Without the oxygen revolution, metabolism would be limited to relatively low-energy fermentation reactions and life would probably have remained limited to simple, single-celled organisms.
Photosynthesis and oxidative metabolism both involve circular biochemical pathways in which a small organic molecule acts as a matrix to which carbon is added, only later to be removed in some other guise. In photosynthesis, the foundation molecule is the five-carbon sugar ribulose, to which carbon dioxide is added to form two compounds with three carbons each, which ultimately feed the production of a six-carbon sugar (fructose) and restoration of the ribulose carrier. Oxidative metabolism uses the four-carbon compound oxaloacetate as a matrix, which reacts with two reduced carbons in the form of an activated acetic acid to form citric acid, which gives the cycle one of its several names. It is also known as the TCA (tricarboxylic acid) cycle and the Krebs cycle, after Hans Krebs (1900–1981), who discovered it in 1937 following up on his earlier discovery of the urea cycle. At the time, some two decades before Calvin’s elucidation of the cyclic metabolic pathways of photosynthesis, such circular metabolic pathways were a revolutionary concept. Enough so that Krebs’s original publication on his now eponymous cycle, which was to earn him the 1953 Nobel Prize in Physiology or Medicine, was rejected outright when he submitted it to the journal Nature.
In the Krebs cycle, a six-carbon citric acid is oxidized in a series of 10 steps producing two carbon dioxide molecules and, ultimately, another molecule of the four-carbon oxaloacetate to continue the cycle. In eukaryotes, this occurs in the mitochondria, which are “fed” acetyl-CoA, representing an activated form of the two-carbon molecule acetic acid attached to an RNA “handle,” by the pathways degrading sugars (glycolysis) and fatty acids in the cytoplasm. The cycle uses the reduced electrons it extracts from citric acid to synthesize NADH (reduced nicotine adenine dinucleotide) and FADH2 (reduced flavin adenine dinucleotide), which are the “reduction currency” of the cell, delivering reducing power to any reaction that needs it. Both are also ribonucleotides and thus, as we’ve noted, may also represent vestiges of the RNA world. The cycle also delivers electrons (plus two protons) to oxygen to produce water in a process called oxidative phosphorylation, which uses the resultant energy to pump protons across the mitochondrial membrane to produce a concentration gradient. The energy released when protons flow back across the membrane is then harnessed by the F-ATPase to produce ATP, a potential vestige of the RNA world that is the energy currency of the cell: reactions that produce metabolically useful energy almost always produce it in the form of ATP, and metabolic processes that consume energy almost always use the energy stored in ATP.
What is the advantage of the Krebs cycle to the individual species that adopt an aerobic lifestyle? Let’s look at the numbers of high-energy molecules to be gained from the degradation of one molecule of glucose in each process. The anaerobic metabolism using glycolysis alone—that is, splitting glucose into two molecules of pyruvate—produces only two ATP. In contrast, the Krebs cycle followed by the electron transport chain squeezes 24 molecules of ATP out of each and every molecule of glucose. In combination with glycolysis and the decarboxylation of pyruvate to acetyl-CoA, the aerobic metabolism of glucose produces 36 ATP per sugar molecule, achieving an eighteenfold increase in energy yield over anaerobic glycolysis alone.
Because of the tremendous energy it can tap into, it is not surprising that the aerobic lifestyle evolved and spread soon after the atmosphere became oxic. Like photosynthesis, the Krebs cycle was invented by bacteria, some of which later joined forces with other cells in an odd form of intracellular symbiosis. Moreover, with the advent of this fusion, a much higher level of metabolism became possible and with that came the possibility of multicellular organisms. But first, a more complex class of single-celled organisms had to evolve, a topic we’ll return to in a moment.
When Did LUCA Live?
The paleontological record is not the only record we have of the history of life on Earth. By identifying metabolic pathways that are held in common across all life, we have defined the likely metabolic “tool kit” of LUCA, the last common ancestor of all life on Earth (see chapter 6). Inspection of what LUCA’s metabolism did and did not contain allows us to hazard a guess as to when she lived. For example, a number of LUCA’s metabolic pathways involved iron-containing enzymes that, on careful reflection, might seem like unfortunate choices to a contemporary biochemist. The problem is that in today’s oxic environment, iron is quickly oxidized to the ferric state, which, as described above, is extremely insoluble. Because of this, iron is the limiting nutrient in the ocean, and marine microorganisms have had to invent an impressive arsenal of “chemical warfare agents” (called siderophores) with which to steal iron from the grasp of other bacteria. If iron is so hard to get that its use represents a selective disadvantage, though, why did LUCA use it? The thought is that LUCA lived when soluble iron was plentiful, before rampant photosynthesis produced our now iron-limited, oxic environment. In contrast, the most oxidized form of copper (Cu+2) is much more soluble than the more reduced forms, so while many more recently invented branches of metabolism employ copper-containing enzymes, LUCA seems to have avoided that element. From these and similar arguments (e.g., LUCA expressed the nitrogen-fixing enzyme nitrogenase, which is poisoned by even small traces of oxygen), it seems clear that LUCA predated the formation of the oxic atmosphere, about 2.2 billion years ago. But there is a big gap between that date and the date of the earliest widely accepted evidence for life on Earth (about 3.5 billion years ago). Thus, although we have bounded the problem, we do not know when in this more than 1-billion-year span LUCA lived.
Eukaryotes: Bigger and Better
The invention of oxygen-producing photosynthesis paved the way for the evolution of multicellular life, a niche that was taken over in its entirety by eukaryotes. Look at cells through a microscope and you’ll be able to tell whether they are eukaryotes or not. Typically, our cells and those of most other eukaryotes are 10 times longer, and thus 1,000 times greater in volume, than the simpler prokaryotes. Peering down a light microscope, this makes the difference between seeing a cell with internal structures and just seeing a dot (fig. 7.3).
The defining difference that gives eukaryotes their name (eukaryote means “true nucleus”) is that their genetic material is isolated from the rest of the cell in the nucleus, which is surrounded by a membrane. The DNA in eukaryotes is typically organized in several long, linear units called chromosomes, whose coiling and packaging is usually controlled by histones, a class of protein that does not exist in bacteria (but does occur in some archaea). The synthesis of messenger RNA (transcription) also takes place in the nucleus, while protein synthesis (translation) is carried out by ribosomes in the cytoplasm. This separation creates additional logistical problems and appears rather troublesome at first glance. Given this, what is the evolutionary advantage that enticed eukaryotes to keep their DNA wrapped up? The clue may lie in the additional editing of messenger RNA that is made possible by this separation. In bacteria, the front end of a messenger RNA can go into the translation machinery while the rear end is still being transcribed. Eukaryotes, in contrast, synthesize messenger RNA in the cell’s nucleus before transporting it to the cytoplasm, where it is used to guide the synthesis of proteins. This separation in space and time allows the cell to introduce additional mechanisms to control gene expression, such as RNA editing, which in turn sets the stage for vastly more complex organisms.
Figure 7.3 A schematic cross section of a eukaryotic cell (a plant cell) is shown in comparison with several bacterial cells. Note that eukaryotic cells tend to be an order of magnitude larger in each dimension, so their volume exceeds that of a bacterium by several thousandfold.
The nucleus is not the only membrane-bound compartment (organelle) within a eukaryotic cell. The mitochondria, chloroplasts, lysosomes, and endoplasmic reticulum are also membrane bound and further distinguish eukaryotes from bacteria and archaea. Each of these compartments brings with it a complete set of important functions. Several of the organelles, most notably the mitochondria and the chloroplasts (in charge of aerobic metabolism and photosynthesis, respectively), are thought to have arisen from formerly independent bacterial symbionts that, over the generations, became better and better integrated into the host cell and lost their independence, along with most of their genes. Which, when you think about it, brings us to the question: where did the eukaryotes come from?
Comparison of protein and gene sequences has enabled researchers to trace back the family tree of life much more precisely than was possible using outward appearance (phenotype) alone. At first, they studied enzyme sequences but found that their efforts were limited by the effects of convergent evolution (remember: similar environmental requirements can lead to similar adaptations, at both the organismal and protein levels), which can produce similarities that do not imply relatedness. As described at the beginning of this chapter, Carl Woese focused his sights on ribosomal RNAs and came to the conclusion that, whereas living things had previously been divided only by the presence (eukaryotes) or absence (prokaryotes) of a nucleus, the oldest and deepest division between species separates the tree of life into three main branches. In the decades since, researchers have switched to the analysis of genes that, unlike even ribosomal RNA, contain variability that is under almost no selective pressure at all—such as codons where the third base is redundant and thus changing it doesn’t change the amino acid sequence of the encoded protein (see chapter 6). The ever-increasing numbers of protein, gene, and genome sequences that have become available provide more and more convincing evidence in favor of this tripartite tree of life.
The three domains of life are fundamentally different in many ways. In some aspects, there are resemblances between two of them that exclude the third (such as the facts that only bacteria and eukaryotes synthesize fatty acids, only archaea and eukaryotes wrap their DNA around histones, and only bacteria and archaea lack nuclei), but there is no longer a case for a grouping into two domains. The very last doubts about that were removed by the first complete genome sequence of an archaeon (Methanococcus jannaschii), which was published in 1996 and illustrated that archaea are pretty much as distinct from the E. coli living in our guts as they are from us.
Even the most modern analytical methods, however, have failed to answer two important questions: first, how do the three largest branches on the tree of life relate to each other; and second, where is the root? Comparisons based on different genes or groups of genes yield very different answers to these questions. From these contradictions, it seems increasingly likely that “vertical” descent of species from earlier species along the direct lines of a family tree does not account for the whole story of life on Earth (fig. 7.4). Exchange of genes between separate species living at the same time must have played an important role.* This kind of horizontal gene transfer can still be observed among microbes, for example, when researchers study the spread of genes that confer resistance to antibiotics or other crucial survival skills. Given the frequency of such horizontal gene transfer across the history of life, the attempt to draw simple family trees relating all living species to a smaller set of ancestors and ultimately to a common root was destined to fail.
Figure 7.4 The traditional view of a “family tree” of life has been replaced by a more complex representation that takes into account horizontal gene transfer and the likely merger of members of the archaeal and bacterial branches to produce eukaryotes, with the bacterial member of this fusion becoming our mitochondria. A second, later fusion with a photosynthetic bacterium produced the higher plants.
But all is not lost. In 2004, Maria Rivera and James Lake at the University of California, Los Angeles, delivered a different description for the crucial early phase of evolution when they applied a new set of algorithms to its modeling. They compared the genomes of 10 organisms representing all three domains of life using an algorithm (“conditioned reconstruction”) designed to cope with both horizontal and vertical gene transfer without discrimination. In this method, one of the genomes (the “conditioning genome”) is picked as a standard that does not enter the resulting tree as it only serves as a reference point for the others. Thus, there is a very simple inbuilt control: one can construct trees based on different choices of conditioning genome and then overlay them. Rivera and Lake first tested this method on the parts of the prokaryotic family tree that were already well described, then applied it to the question of how the deepest branches—the three domains of life—relate to each other. Sifting through the results with the highest statistical significance parameters, they realized that all of them were permutations of a single pattern that can best be described as a ring (see fig. 7.4).
Biologically, this finding implies that Eukarya arose from both Bacteria and Archaea, possibly through the fusion of two early cells. This interpretation is consistent with earlier results of genome comparisons revealing that eukaryotic genes in charge of information processing (ribosomes, translation factors, enzymes of DNA processing) are more closely related to their archaeal counterparts than to the bacterial ones, while the reverse is true for genes in charge of metabolism. With several independent studies now confirming a “mixed” origin of eukaryotes, it seems almost certain that they arose from some kind of marriage between the two older, more “primitive” domains.
Genomic analysis suggests that the Alphaproteobacteria are the extant bacteria most closely related to the bacterial symbiont whose vestiges remain in us today in the form of mitochondria. Perhaps not coincidentally, this bacterial class includes the Rickettsiales, a group of pathogens that are obligate intracellular parasites, that is, parasites that live inside the cells of their eukaryotic hosts and are responsible for such diseases as typhus and spotted fever.
In contrast to the bacterial ancestor of the mitochondria, the archaeal partner in the marriage was harder to find. In 2015, the group of Christa Schleper at the University of Vienna, Austria, identified a new archaeal phylum, called Lokiarchaeota, via genomic sequencing because the microorganism could not, at the time, be cultivated in the laboratory (see sidebar 7.2). Identified in mud samples collected near the Loki hydrothermal fields at the mid-Atlantic spreading center, the archaea feature a number of genes hitherto considered specific for eukaryotes, including those for cytoskeletal components such as actin. Further analyses of environmental DNA revealed other related lineages in the phylum, all of which are now named after Nordic deities (Loki being a god in Norse mythology) and thus collectively called the Asgard archaea. Genomic comparisons suggest that, among these, the phylum Heimdallarchaeota is the closest known archaeal relative to the eukaryotes.
Still, all these microorganisms were characterized on the basis of genomics. It was only in 2020 that the first species of the Asgard archaea was reported as having been successfully cultivated in the lab. Hiroyuki Imachi and his colleagues at the X-star institute in Yokosuka, Japan, had originally started cultivation attempts for unrelated reasons, even before Lokiarchaeota were identified. Their work eventually led to the characterization of Prometheoarchaeum as the first cultivated member of the Lokiarchaeota. The cells turned out to be very small but are equipped with spectacular membrane extrusions that, intriguingly, allow them to perform nutrient exchange with two associated, hydrogen- and methane-consuming bacterial species in a manner reminiscent of how eukaryotic cells “feed” reducing potential to their internal mitochondria.
If endosymbiotic fusion with one bacterial cell is good, wouldn’t fusion with two be better? The plants seem to represent just such thinking; sometime after the origins of the eukaryotes, a second endosymbiotic event occurred (see fig. 7.4), this time bringing in a cyanobacterium which then “devolved” (transferred many of its genes to the nuclear genome) into today’s chloroplasts, the photosynthetic organelles of the eukaryotic plants. In 2017, genomic analysis was provided suggesting that, among known bacteria, the closest living relative to the chloroplast ancestor is Gloeomargarita lithophora, a cyanobacterial species found in Lake Alchichica, an alkaline crater lake in the high desert of Puebla, Mexico.
And when did our eukaryotic branch first sprout off the tree of life? That’s not so easy to say since the nucleus, which is, by definition, the thing that separates eukaryotes from prokaryotes, doesn’t readily fossilize, and thus paleontologists base their claims on the sizes and shapes of microfossils, which are far from unambiguous indicators. Using this metric, for example, eukaryotic cell–sized microfossils have been claimed from as far back as 3.2 billion years. The oldest microfossils that appear to be widely accepted as eukaryotic, however, are large (>100 μm), spiny, organic-walled microfossils dating to 1.65 billion years ago. However, we’re on firmer footing if, instead of trying to identify the first eukaryote (which depends on what, precisely, it means to be a eukaryote), we focus on dating the last eukaryotic common ancestor (LECA), the most recent common ancestor of all living eukaryotes. Since almost all eukaryotes are aerobic, and those few that are not show clear signs of once having had (but then lost) mitochondria, it’s fairly clear that LECA lived more recently than 2.2 billion years ago, the time after which atmospheric oxygen climbed to an appreciable level. Consistent with this, molecular phylogeny studies generally suggest LECA lived between 1.1 and 1.7 billion years ago. Finally, efforts to trace the paleontological record using molecular markers unique to eukaryotes, such as the degradation products of cholesterol and its relatives, suggest that at least the sterol-synthesizing eukaryotes (which includes all current eukaryotes) did not arise, or at least did not become common, until more recently than 1.1 billion years ago. This said, by 650 million years ago, algae-derived sterols become common in marine sediments. Enough so that this is thought to have marked a transition from a biosphere that was predominantly driven by prokaryotes to one dominated by eukaryotes.
Multicellular Life and the Cambrian Explosion
The rise of the multicellular plants and animals that we tend to think of as “biology” occurred rather late in the history of our planet. Within a few hundred million years of Earth becoming inhabitable at the end of the late heavy bombardment, single-celled life seems to have been abundant. In contrast, the “next step,” the creation of multicellular life, took several billion years. In part, this was because multicellular life likely requires an energetic metabolism and thus had to await the advent of an oxic atmosphere. But multicellularity also requires a good deal of complexity at the cellular level, which might likewise have been slow in coming.
Green algae were among the pioneers of higher organization in colonies but didn’t immediately make the transition to developing a body plan. Not until several hundred million years later did things start to really take off, when the earliest known multicellular eukaryotic, the red alga Bangiomorpha pubescens, showed up in the fossil record some 1.05 billion years ago. The first clear evidence of animals crops up some 400 million years later, first as enigmatic forms that left behind a variety of tubular and frond-shaped fossils. These simple forms, with just two layers of cells, later evolved into forms with three layers, then three layers with a cavity, and, finally, onward to the human body plan of three layers of cells surrounding an internal cavity with both a mouth and an anus. This represented a significant advance; less-developed animals, such as the flatworms, have a mouth but lack an anus, and thus anything they can’t digest has to be vomited back up.
Why did bacteria fail to master this move? Cyanobacteria, for example, are amazingly sophisticated, having mastered photosynthesis, nitrogen fixation, symbiosis with fungi to form lichens, and even development of circadian clocks. So why did some obscure eukaryote steal the limelight from them, increasing the complexity of living beings and inventing the higher plants and animals? There are clearly many contributing factors, no doubt including some that we still don’t understand. But a few of the features that enabled the jump are clear: organization of space, organization of the genome, and sex.
The most striking difference that distinguishes eukaryotic cells from bacteria is not just the volume of their interior space, which is typically a thousandfold larger, but the way this space is organized into compartments of well-defined function. Bringing together the information processing of the nucleus, the aerobic metabolism of mitochondria, possibly the photosynthesis of chloroplasts, and other functions in separate entities, even a formally single-celled eukaryote is effectively a “multicellular” organism.
More importantly, eukaryotes abandoned the circular DNA that bacteria still use today and invented linear DNA strands wrapped around histones and capped with telomeres, resulting in the familiar chromosomes. Even the humble, single-celled eukaryote baker’s yeast has 16 separate linear chromosomes. There is a limit to how much DNA can be stored and processed in a single ring without ending up in a lethal tangle, but the organization into chromosomes offered not only more storage space but a natural way of expanding the space, namely by adding new chromosomes. Thus, the number of chromosomes varies widely among different eukaryotic species.
But, most importantly, their style of genome organization enabled eukaryotes to embark on a completely new way of fostering genetic diversity while ensuring the genetic stability that keeps the species together. This wonderful tool of evolution, invented around 1 billion years ago, is known as meiosis on the cellular level, but on the organismal level it is called sex. Biologists have argued about its usefulness. In comparison with an asexual reproduction mechanism, where every individual can have offspring without the need of a partner, the maintenance of a second gender contributing only a minor part to the reproductive process (e.g., the human male) is a complete waste of energy, one might argue. However, the success of sexual reproduction throughout the animal kingdom and in much of the plant world shows that the benefits to the species more than compensate for this energy loss.
So, equipped with these advantages, some protists (the generic name for single-celled eukaryotes) finally got their act together and became the founders of zoology, sometime before 600 million years ago. We know very little about their first efforts as they don’t show up in the fossil record very clearly, and the molecular analyses carried out so far have not resulted in a convincing reconstruction of the first animal. But these events laid the groundwork for something big because, only 50 million years later, the fossils document a sheer explosion of animal diversity.
Now isn’t that ironic? You wait some 3 billion years for animals to come along, and then they all arrive at once. Or so it may seem. Some 650 million years ago, several billion years after the first traces of life on Earth, there were still no traces of animals in the fossil record, and yet, 200 million years later, they were everywhere. In fact, more than a hundred different orders of animals have already been found in the fossil record within 200 million years of the first animal fossils, almost as many orders as exist today.* During the 100 million years of the Cambrian (541 to 485 million years ago) and Ordovician periods (485 to 444 million years ago) alone, evolution invented essentially every single body plan in use today and many more bizarre body forms that are not. This unrivaled burst of evolutionary inventiveness, known as the Cambrian explosion, has mystified biologists from the time of Darwin to the present. Today there are two fundamentally different schools of thought on this issue, each with its own tool kit of possible explanations and interpretations.
The “late arrival” school, represented by Stephen Jay Gould (1941–2002) from Harvard University, maintained that what we see in the fossil record is essentially true and that the diversification did indeed happen unusually fast, creating as many as 50 new orders in just 10 million years. One plausible explanation sees the explosion as an arms race triggered by the use of biomineralization by animals. The controlled deposition of minerals from body tissues enabled animals not only to develop skeletons (which allowed them to diversify into more complex shapes and larger sizes) but also to grow claws, rasps, and teeth with which they could prey on other animals. Predatory lifestyles opened up additional ecological niches and triggered defensive measures in the animals threatened by them. And biomineralization allowed animals to build protective shields, such as mollusk shells. Similarly, the development of eyes may have intensified the arms race between species.
To us, who can only see these animals when they are fossilized, the impression of an “explosion” is made even more dramatic by the fact that mineralized tissues such as bones, teeth, and shells have a much better chance of being preserved than the soft tissues of the animals that lived before the onset of biomineralization. This argument leads us to the second school of thought, the “early arrival” model (favored by Darwin), which claims that animal diversity existed for hundreds of millions of years before the Cambrian period but didn’t show up in the fossil record because either the animals were too soft to fossilize properly or the conditions were unfavorable for their preservation. Consistent with this, “molecular clock” studies that date divergences by counting the number of mutations suggest that some animal diversity existed before the explosion. Nevertheless, most researchers would not allow more than 150 million years for this hidden period of animal evolution. Several authorities, for example, place one of the deepest divisions in the family tree of multicellular life, the one between protostomes (including mollusks, insects, crustaceans) and deuterostomes (including vertebrates but also the echinoderms, such as starfish*), at 670 million years ago, some 130 million years before the start of the Cambrian.
Conquering Land
The Cambrian explosion happened in water. But in addition to providing enough energy to support the formation of multicellular life, the oxygen revolution also ultimately set the stage for the colonization of dry land: the only reason living organisms can thrive above the water line without suffering catastrophic DNA damage is the ozone content of the stratosphere. Although the phenomenon is often referred to as the “ozone layer” and is even measured in terms of the thickness it would have if there were such a thing, the ozone is in fact rather dilute and the compound as such is highly unstable. But its fleeting presence in the stratosphere (which extends between the heights of 16 and 50 km) is sufficient to absorb the damaging, far-UV component of sunlight.
The earliest non-marine eukaryotes appear to have been multicellular algae, which first came ashore about a billion years ago. These were followed by the higher plants, with the oldest known land-plant fossils dating to 420 million years ago. Fungi may have come along for the ride since phylogenomic studies of plants and the fungi that live symbiotically in their roots suggest that the two helped each other colonize this new world. For example, Susana Magallón, from the National University of Mexico in Mexico City, reported in 2018 that the phylogenies of both sides of the symbiosis go back 700 million years, likely before either group had moved onto dry land. Between them they made the bare surface of the continents habitable for the animals, with the first known land animals arising some 405 million years ago, and the first terrestrial animals in our line, the amphibians, climbing onto the land only 370 million years ago.
Conclusions
It has been a few chapters since we last said it, so it probably bears repeating here: biology is a parochial science. Given that all life on Earth arose from a biochemically complex common ancestor, it’s not so easy to figure out which aspects of our biochemistry and cell biology reflect adaptations to the fundamental issues related to life on a terrestrial planet and which are merely historical artifacts of evolutionary chance. But then again, we biologists have to play the cards we are dealt. From that perspective, detailed studies of the evolution of life on Earth are probably the best approach we have toward understanding how life is defined, constrained, and encouraged by the physical reality of growing up on a small, rocky planet.
What does this ultra-compressed history of life teach us in the context of astrobiology? That, at least on this planet, it took a good fraction of the age of the Universe itself for intelligent life to arise (see sidebar 7.3). The evidence that life existed by 3.43 billion years ago is strong and is pretty much rock solid by 3.2 billion years ago. It took another 1 or 2 billion years, however, for evolution to invent eukaryotes, and the first multicellular life didn’t arise until several hundred million years later still. In the end, it was not until at least a billion years after the first multicellular organism, and likely more than 3.5 billion years after the start of life itself, that an obscure, mammalian branch on the eukaryotic domain of the tree of life evolved a species that could spend endless years arguing in the scientific literature before ultimately deciding that Woese was right: the Archaea truly are distinct from the Bacteria.
Further Reading
Earliest Life / Evolution of Life / Origins of Eukaryotes
Knoll, Andrew. Life on a Young Planet: The First Three Billion Years of Evolution on Earth. Princeton, NJ: Princeton University Press, 2015.
Evidence for Life at 3.8 Billion Years
Dalton, Rex. “Fresh Study Questions Oldest Traces of Life in Akilia Rock.” Nature 429, no. 6993 (2004): 688.
Dodd, Matthew S., Dominic Papineau, Tor Grenne, John F. Slack, Martin Rittner, Franco Pirajno, Jonathan O’Neil, and Crispin T. S. Little. “Evidence for Early Life in Earth’s Oldest Hydrothermal Vent Precipitates.” Nature 543, no. 7643 (2017): 60–64.
Fedo, Christopher M., and Martin J. Whitehouse. “Metasomatic Origin of Quartz-Pyroxene Rock, Akilia, Greenland, and Implications for Earth’s Earliest Life.” Science 296, no. 5572 (2002): 1448–52.
Sano, Yuji, Kentaro Terada, Yoshio Takahashi, and Allen P. Nutman. “Origin of Life from Apatite Dating?” Nature 400 (1999): 127.
Evidence for Life at 3.46 Billion Years
Brasier, Martin D., Owen R. Green, Andrew P. Jephcoat, Annette K. Kleppe, Martin J. Van Kranendonk, John F. Lindsay, Andres Steele, and Nathalie V. Grassineau. “Questioning the Evidence for Earth’s Oldest Fossils.” Nature 416 (2002): 76–81.
Schopf, J. William. “Microfossils of the Early Archaean Apex Chert: New Evidence of the Antiquity of Life.” Science 260, no. 5108 (1993): 640–46.
Evidence for Life at 3.43 Billion Years
Allwood, Abigail C., Malcolm R. Walter, Balz S. Kamber, Craig P. Marshall, and Ian W. Burch. “Stromatolite Reef from the Early Archaean Era of Australia.” Nature 441 (2006): 714–18.
Origins of Photosynthesis
Gross, Michael. Light and Life. Oxford, UK: Oxford University Press, 2003.
Archaeal Ancestors of First Eukaryotes
Imachi, Hiroyuki, Masaru K. Nobu, Nozomi Nakahara, Yuki Morono, Miyuki Ogawara, Yoshihiro Takaki, Yoshinori Takano, et al. “Isolation of an Archaeon at the Prokaryote-Eukaryote Interface.” Nature 577 (2020): 519–25.
Evolution and Phylogenetics of Eukaryotes
Gross, Michael. “The Success Story of Plants and Fungi.” Current Biology 29, no. 6 (2019): R183–85.
Gross, Michael. “The Genome Sequence of Everything.” Current Biology 28, no. 13 (2018): R719–21.
- * In February 2020, the number was 128,000 and counting.
- * To quote Carl Sagan: “In science it often happens that scientists say, ‘You know that’s a really good argument; my position is mistaken,’ and then they actually change their minds and you never hear that old view from them again. They really do it. It doesn’t happen as often as it should, because scientists are human and change is sometimes painful. But it happens every day. I cannot recall the last time something like that has happened in politics or religion.” Carl Sagan, “The Burden of Skepticism,” Skeptical Inquirer 12, no. 1 (1987).
- * Matthew S. Dodd et al., “Evidence for Early Life in Earth’s Oldest Hydrothermal Vent Precipitates,” Nature 543 (2017): 60–64.
- * The numbers here denote the number of electrons lost (positive oxidation states) or gained (negative oxidation states).
- * Geological debates being very slow.
- * Gene exchange also weakens our argument that any traits shared across all three domains of life must have been inherited from LUCA; some of the shared traits could have arisen in one branch, after LUCA, and been horizontally transferred to the others. Still, most authorities seem to agree in broad detail with the description of LUCA we’ve given here.
- * An order is a phylogenetic group that is smaller than a class and larger than a genus. For example, Mammalia (mammals) is a class that contains the orders Primates (e.g., ourselves), Rodentia (e.g., mice), and Proboscidea (the elephants, of course). Likewise, the order Primates includes such genera as Homo (us), Pan (the chimpanzees), and Gorilla (the lowland and highland gorillas).
- * This is about the anus and the mouth again. In protostomes, the first opening to form during early embryonic development becomes the mouth, but in deuterostomes it develops into the anus; the mouth comes second.