contained the basic chemical elements out of which the building blocks of life were to be formed. Its distance from the sun was just right—far enough away for a slow process of cooling and condensation to begin and yet close enough to prevent its gases from being permanently frozen.
After half a billion years of gradual cooling, the steam filling the atmosphere finally condensed; torrential rains fell for thousands of years, and water gathered to form shallow oceans. During this long period of cooling, carbon, the chemical backbone of life, combined rapidly with hydrogen, oxygen, nitrogen, sulfur, and phosphorus to generate an enormous variety of chemical compounds. Those six elements—C, H, O, N, S, P—are now the main chemical ingredients in all living organisms.
For many years scientists debated the likelihood of life emerging from the “chemical soup” that formed as the planet cooled off and the oceans expanded. Several hypotheses of sudden triggering events competed with one another—a dramatic flash of lightning or even a seeding of the Earth with macromolecules by meteorites. Other scientists argued that the odds of any such event having happened are vanishingly small. However, the recent research on self-organizing systems indicates strongly that there is no need to postulate any sudden event.
As Margulis points out, “Chemicals do not combine randomly, but in ordered, patterned ways.” 22 The environment on the early Earth favored the formation of complex molecules, some of which became catalysts for a variety of chemical reactions. Gradually different catalytic reactions interlocked to form complex catalytic webs involving closed loops—first cycles, then “hypercycles”— with a strong tendency for self-organization and even self-replication. 23 Once this stage was reached, the direction for prebiotic evolution was set. The catalytic cycles evolved into dissipative structures and, by passing through successive instabilities (bifurcation points), generated chemical systems of increasing richness and diversity.
Eventually these dissipative structures began to form membranes—first, perhaps, from fatty acids without proteins, like the micelles recently produced in the laboratory. 24 Margulis speculates
that many different types of membrane-enclosed replicating chemical systems may have arisen, evolved for a while, and then disappeared again before the first cells emerged: “Many dissipative structures, long chains of different chemical reactions, must have evolved, reacted, and broken down before the elegant double helix of our ultimate ancestor formed and replicated with high fidelity.” 25 At that moment, about 3.5 billion years ago, the first auto- poietic bacterial cells were born, and the evolution of life began.
Weaving the Bacterial Web
The first cells led a precarious existence. The environment around them changed continually, and every hazard presented a new threat to their survival. In the face of all these hostile forces— harsh sunlight, meteorite impacts, volcanic eruptions, droughts, and floods—the bacteria had to trap energy, water, and food to maintain their integrity and stay alive. Each crisis must have wiped out large portions of the first patches of life on the planet and would certainly have extinguished them altogether, had it not been for two vital traits—the abilities of the bacterial DNA to replicate faithfully and to do so with extraordinary speed. Because of their enormous numbers, the bacteria were able, again and again, to respond creatively to all threats and to develop a great variety of adaptive strategies. Thus they gradually expanded, first in the waters and then in the surfaces of sediments and soil.
Perhaps the most important task was to develop a variety of new metabolic pathways for extracting food and energy from the environment. One of the first bacterial inventions was fermentation—the breaking down of sugars and conversion into ATP molecules, the “energy carriers” that fuel all cellular processes. 26 This innovation allowed the fermenting bacteria to live off chemicals in the earth, in mud and water, protected from the harsh sunlight.
Some of the fermenters also developed the ability to absorb nitrogen gas from the air and convert it into various organic compounds. To “fix” nitrogen—in other words, to capture it directly from the air—takes large amounts of energy and is a feat that even today can be performed only by a few special bacteria. Since
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nitrogen is an ingredient of the proteins in all cells, all living organisms today depend on the nitrogen-fixing bacteria for their survival.
Early on in the age of bacteria, photosynthesis—“undoubtedly the most important single metabolic innovation in the history of life on the planet” ~—became the primary source of life energy. The first processes of photosynthesis invented by the bacteria were different from those used by plants today. They used hydrogen sulfide, a gas spewed out by volcanoes, instead of water as their source of hydrogen, combined it with sunlight and C0 2 from the air to form organic compounds, and never produced oxygen.
These adaptive strategies not only enabled the bacteria to survive and evolve, but also began to change their environment. In fact, almost from the beginning of their existence, the bacteria established the first feedback loops that would eventually result in the tightly coupled system of life and its environment. Although the chemistry and climate of the early Earth were conducive to life, this favorable state would not have continued indefinitely without bacterial regulation. 2 8
As iron and other elements reacted with water, hydrogen gas was released and rose up through the atmosphere, where it broke down into hydrogen atoms. Since these atoms are too light to be held by the Earth’s gravity, all the hydrogen would have escaped if this process had continued unchecked, and a billion years later the oceans of the planet would have disappeared. Fortunately life intervened. In the later stages of photosynthesis free oxygen was released into the air, as it is today, and some of it combined with the rising hydrogen gas to form water, thus keeping the planet moist and preventing its oceans from evaporating.
However, the continuing removal of C0 2 from the air in the process of photosynthesis caused another problem. At the beginning of the age of bacteria, the sun was 25 percent less luminous than it is now, and the C0 2 in the atmosphere was very much needed as a greenhouse gas to keep the planetary temperatures in a comfortable range. Had the removal of C0 2 gone on without any compensation, the Earth would have frozen and early bacterial life would have been extinguished.
Such a disastrous course was prevented by the fermenting bacteria, which may have evolved already before the onset of photosynthesis. In the process of producing ATP molecules from sugars, the fermenters also produced methane and C0 2 as waste products. These were emitted into the atmosphere, where they restored the planetary greenhouse. In this way fermentation and photosynthesis became two mutually balancing processes of the early Gaia system.
The sunlight coming through the Earth’s early atmosphere still contained burning ultraviolet radiation, but now the bacteria had to balance their protection from exposure with their need for solar energy for photosynthesis. This led to the evolution of numerous sensing systems and of movement. Some bacterial species migrated into waters rich in certain salts that acted as sun filters; others found shelter in sand; yet others developed pigments that absorbed the harmful rays. Many species built huge colonies—multileveled microbial mats in which the top layers got scorched and died but shielded the lower layers with their dead bodies. 29
In addition to protective filtering the bacteria also developed mechanisms for repairing radiation-damaged DNA, evolving special enzymes for that purpose. Almost all organisms today still possess these repair enzymes—another lasting invention of the microcosmos. 30
Instead of using their own genetic material for the repair process, bacteria in crowded environments sometimes borrowed DNA fragments from their neighbors. This technique gradually evolved into the constant gene trading that became the most effective avenue of bacterial evolution. In higher forms of life the recombination of genes from different individuals is associated with reproduction, but in the world of bacteria the two phenomena take place independently. Bacterial cells reproduce asexually, but they continually trade genes. In the words of Margulis and Sagan:
We trade genes “vertically”—through the generations—whereas bacteria trade them “horizontally”—directly to their neighbors in the same generation. The result is that while genetically fluid bac-
teria are functionally immortal, in eukaryotes, sex becomes linked
with death. 31
Because of the small number of permanent genes in a bacterial cell—typically less than 1 percent of those in a nucleated cell— bacteria necessarily work in teams. Different species cooperate and help each other out with complementary genetic material. Large assemblies of such bacterial teams can operate with the coherence of a single organism, performing tasks that none of them can do individually.
By the end of the first billion years after the emergence of life, the Earth was teeming with bacteria. Thousands of biotechnologies had been invented—indeed, most of those known today—and by cooperating and continually trading genetic information the microorganisms had begun to regulate conditions for life on the entire planet, as they still do today. In fact, many of the bacteria living in the early age of the microcosm have survived essentially unchanged to this very day.
During subsequent stages of evolution, the microorganisms formed alliances and coevolved with plants and animals, and today our environment is so interwoven with bacteria that it is almost impossible to say where the inanimate world ends and life begins. We tend to associate bacteria with disease, but they are also vital for our survival, as they are for the survival of all animals and plants. “Beneath our superficial differences we are all of us walking communities of bacteria,” write Margulis and Sagan. “The world shimmers, a pointillist landscape made of tiny living be-
The Oxygen Crisis
As the bacterial web expanded and filled every available space in the waters, rocks, and mud flats of the early planet, its energy needs led to a severe depletion of hydrogen. The carbohydrates that are essential to all life are elaborate structures of carbon, hydrogen, and oxygen atoms. To build these structures the photo- synthesizing bacteria took the carbon and oxygen from the air in
the form of C0 2 , as all plants do today. They also found hydrogen in the air, in the form of hydrogen gas, and in the hydrogen sulfide bubbling up from volcanoes. But the light hydrogen gas kept escaping into space, and eventually the hydrogen sulfide became insufficient.
Hydrogen, of course, exists in great abundance in water (H 2 0), but the bonds between hydrogen and oxygen in water molecules are much stronger than those between the two hydrogen atoms in hydrogen gas (H 2 ) or hydrogen sulfide (H 2 S). The photosynthe- sizing bacteria were not able to break these strong bonds until a special kind of blue-green bacteria invented a new type of photosynthesis that solved the hydrogen problem forever.
The newly evolved bacteria, the ancestors of the modern-day blue-green algae, used sunlight of higher energy (shorter wavelength) to split water molecules into their hydrogen and oxygen components. They took the hydrogen for building sugars and other carbohydrates and emitted the oxygen into the air. This extraction of hydrogen from water, which is one of the planet’s most abundant resources, was an extraordinary evolutionary feat with far-reaching implications for the subsequent unfolding of life. Indeed, Lynn Margulis is convinced that “the advent of oxygenic photosynthesis was the singular event that led eventually to our modern environment.” 33
With their unlimited source of hydrogen, the new bacteria were spectacularly successful. They expanded rapidly across the Earth’s surface, covering rocks and sand with their blue-green film. Even today they are ubiquitous, growing in ponds and swimming pools, on moist walls and shower curtains—wherever there is sunlight and water.
However, this evolutionary success came at a heavy price. Like all rapidly expanding living systems, the blue-green bacteria produced massive amounts of waste, and in their case this waste was also highly toxic. It was the oxygen gas emitted as a by-product of the new type of water-based photosynthesis. Free oxygen is toxic because it reacts easily with organic matter, producing so-called free radicals that are extremely destructive to carbohydrates and other essential biochemical compounds. Oxygen also reacts easily
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with atmospheric gases and metals, triggering combustion and corrosion, the two most familiar forms of “oxidizing” (combining with oxygen).
At first the Earth easily absorbed the oxygen waste. There were enough metals and sulfur compounds from volcanic and tectonic sources that quickly captured the free oxygen and prevented it from building up in the air. But after absorbing oxygen for millions of years, the oxidizing metals and minerals became saturated and the toxic gas began to accumulate in the atmosphere.
About two billion years ago the oxygen pollution resulted in a catastrophe of unprecedented global proportions. Numerous species were wiped out completely, and the entire bacterial web had to fundamentally reorganize itself to survive. Many protective devices and adaptive strategies evolved, and finally the oxygen crisis led to one of the greatest and most successful innovations in the entire history of life:
In one of the greatest coups of all time, the [blue-green] bacteria invented a metabolic system that required the very substance that had been a deadly poison. . . . The breathing of oxygen is an ingeniously efficient way of channeling and exploiting the reactivity of oxygen. It is essentially controlled combustion that breaks down organic molecules and yields carbon dioxide, water, and a great deal of energy in the bargain. . . . The microcosm did more than adapt: it evolved an oxygen-using dynamo that changed life and its terrestrial dwelling place forever. 34
With this spectacular invention the blue-green bacteria had two complementary mechanisms at their disposal—the generation of free oxygen through photosynthesis and its absorption through respiration—and thus they could begin to set up the feedback loops that would henceforth regulate the atmosphere’s oxygen content, maintaining it at the delicate balance that enabled new oxygen-breathing forms of life to evolve. 35
The proportion of free oxygen in the atmosphere eventually stabilized at 21 percent, a value determined by its range of flammability. If it dropped to below 15 percent, nothing would burn. Organisms could not breathe and would asphyxiate. If the oxygen
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THE WEB OF LIFE
in the air rose to above 25 percent, everything would burn. Combustion would occur spontaneously and fires would rage around the planet. Accordingly, Gaia has kept the atmospheric oxygen at the level most comfortable for all plants and animals for millions of years. In addition, a layer of ozone (three-atom oxygen molecules) gradually built up at the top of the atmosphere and from then on protected life on Earth from the sun’s harsh ultraviolet rays. Now the stage was set for the evolution of the larger forms of life—fungi, plants, and animals—which occurred in relatively short periods of time.
The Nucleated Cell
The first step toward higher forms of life was the emergence of symbiosis as a new avenue for evolutionary creativity. This occurred around 2.2 billion years ago and led to the evolution of eukaryotic (“nucleated”) cells, which became the fundamental components of all plants and animals. Nucleated cells are much larger and far more complex than bacteria. Whereas the bacterial cell contains a single loose strand of DNA floating freely in the cell fluid, the DNA in a eukaryotic cell is coiled tightly into chromosomes, which are confined by a membrane inside the cell nucleus. The amount of DNA in nucleated cells is several hundred times that found in bacteria.
The other striking characteristic of the nucleated cell is an abundance of organelles—oxygen-using smaller cell parts that carry out a variety of highly specialized functions. 36 The sudden appearance of nucleated cells in the history of evolution and the discovery that their organelles are distinct self-reproducing organisms led Lynn Margulis to the conclusion that nucleated cells have evolved through long-term symbiosis, the permanent living together of various bacteria and other microorganisms. 37
The ancestors of the mitochondria and other organelles may have been vicious bacteria that invaded larger cells and reproduced inside them. Many of the invaded cells would have died, taking the invaders with them. However, some of the predators did not kill their hosts outright but began to cooperate with them,
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and eventually natural selection allowed only the cooperators to survive and evolve further. Nuclear membranes may have evolved to protect the host cells’ genetic material from attack by the invaders.
Over millions of years the cooperative relationships became ever more coordinated and interwoven, organelles reproducing offspring well adapted to living within larger cells and larger cells becoming ever more dependent on their lodgers. Over time these bacterial communities became so utterly interdependent that they functioned as single integrated organisms:
Life had moved another step, beyond the networking of free genetic transfer to the synergy of symbiosis. Separate organisms blended together, creating new wholes that were greater than the sum of their parts. 38
The recognition of symbiosis as a major evolutionary force has profound philosophical implications. All larger organisms, including ourselves, are living testimonies to the fact that destructive practices do not work in the long run. In the end the aggressors always destroy themselves, making way for others who know how to cooperate and get along. Life is much less a competitive struggle for survival than a triumph of cooperation and creativity. Indeed, since the creation of the first nucleated cells, evolution has proceeded through ever more intricate arrangements of cooperation and coevolution.
The avenue of evolution through symbiosis allowed the new forms of life to use well-tested specialized biotechnologies over and over again in different combinations. For example, whereas bacteria obtain their food and energy by a great variety of ingenious methods, only one of their numerous metabolic inventions is used by animals—that of oxygen breathing, the specialty of the mitochondria.
Mitochondria are also present in plant cells, which in addition contain the so-called chloroplasts, the green “solar stations” responsible for photosynthesis. 39 These organelles are remarkably similar to the blue-green bacteria, the inventors of oxygen photosynthesis, who in all likelihood were their ancestors. Margulis
speculates that those all-pervasive bacteria were routinely eaten by other microorganisms and that some variations must have resisted being digested by their hosts. 40 Instead they adapted to their new environments while continuing to produce energy through photosynthesis, upon which the larger cells soon became dependent.
While their new symbiotic relationships gave the nucleated cells access to the efficient use of sunlight and oxygen, they also gave them a third great evolutionary advantage—the capability of movement. Whereas the components of a bacterial cell float around slowly and passively in the cell fluid, those in a nucleated cell seem to move decisively; the cell fluid streams along, and the entire cell may expand and contract rhythmically or move rapidly as a whole, as, for example, in the case of blood cells.
Like so many other life processes, rapid motion was invented by bacteria. The fastest member of the microcosm is a tiny, hairlike creature called spirochete (“coiled hair”), also known as the “corkscrew bacterium,” which spirals in rapid motion. By attaching themselves symbiotically to larger cells, the rapidly moving corkscrew bacteria gave those cells the tremendous advantages of locomotion—the ability to avoid danger and seek out food. Over time the corkscrew bacteria progressively lost their distinct traits and evolved into the well-known “cell whips”— -flagellae, cilia, and the like—that propel a wide variety of nucleated cells with undulating or whipping motions.
The combined advantages of the three types of symbiosis described in the preceding paragraphs created a burst of evolutionary activity that generated a tremendous diversity of eukaryotic cells. With their two effective means of energy production and their dramatically increased mobility, the new symbiotic life forms migrated to many new environments, evolving into the primeval plants and animals that would eventually leave the water and take over the land.
As a scientific hypothesis the concept of symbiogenesis—the creation of new forms of life through the merging of different species—is barely thirty years old. But as a cultural myth the idea seems to be as old as humanity itself. 41 Religious epics, legends, fairy tales, and other mythical stories around the world are full of
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fantastic creatures—sphinxes, mermaids, griffons, centaurs, and more—born from the blending of two or more species. Like the new eukaryotic cells, these creatures are made of components that are entirely familiar, but their combinations are novel and star- ding.
Depictions of these hybrid beings are often frightening, but many of them, curiously, are seen as bearers of good fortune. For example, the god Ganesha, who has a human body with an elephant head, is one of the most revered deities in India, worshiped as a symbol of good luck and a helper in overcoming obstacles. Somehow the collective human unconscious seems to have known from ancient times that long-term symbioses are profoundly beneficial for all life.
Evolution of Plants and Animals
The evolution of plants and animals out of the microcosm proceeded through a succession of symbioses, in which the bacterial inventions from the previous two billion years were combined in endless expressions of creativity until viable forms were selected to survive. This evolutionary process is characterized by increasing specialization—from the organelles in the first eukaryotes to the highly specialized cells in animals.
An important aspect of cell specialization is the invention of sexual reproduction, which occurred about one billion years ago. We tend to think of sex and reproduction as being closely associated, but Margulis points out that the complex dance of sexual reproduction consists of several distinct components that evolved independently and only gradually became interlinked and unified. 42
The first component is a type of cell division, called meiosis (“diminution”), in which the number of chromosomes in the nucleus is reduced by exactly half. This creates specialized egg and sperm cells. These cells are then fused in the act of fertilization, in which the normal number of chromosomes is restored and a new cell, the fertilized egg, is created. This cell then divides repeatedly in the growth and development of a multicellular organism.
The fusion of genetic material from two different cells is widespread among bacteria, where it takes place as a continual trading of genes that is not linked to reproduction. In the early plants and animals reproduction and the fusion of genes became linked and subsequently evolved into elaborate processes and rituals of fertilization. Gender was a later refinement. The first germ cells— sperm and egg—were almost identical, but over time they evolved into small fast-moving sperm cells and large stationary eggs. The connection of fertilization with the formation of embryos came even later in the evolution of animals. In the world of plants fertilization led to intricate patterns of coevolution of flowers, insects, and birds.
As the specialization of cells continued in larger and more complex forms of life, the capability of self-repair and regeneration diminished progressively. Flatworms, polyps, and starfish can regenerate almost their entire bodies from small fractions; lizards, salamanders, crabs, lobsters, and many insects are still able to grow back lost organs or limbs; but in higher animals regeneration is limited to renewing tissues in the healing of injuries. As a consequence of this loss of regenerative capabilities, all large organisms age and eventually die. However, with sexual reproduction life has invented a new type of regenerative process, in which entire organisms are formed anew again and again, returning in every “generation” to a single nucleated cell.
Plants and animals are not the only multicellular creatures in the living world. Like other traits of living organisms, multicellu- larity evolved many times in many lineages of life, and today there still exist several kinds of multicellular bacteria and many multicellular protists (microorganisms with nucleated cells). Like animals and plants, most of these multicellular organisms are formed by successive cell divisions, but some may be generated by an a gg re gation of cells from different sources but of the same species.
A spectacular example of such aggregations is the slime mold, an organism that is macroscopic but is technically a protist. A slime mold has a complex life cycle involving a mobile (animallike) and an immobile (plant-like) phase. In the animal-like phase it starts out as a multitude of single cells, commonly found in
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forests under rotting logs and damp leaves, where they feed on other microorganisms and decaying vegetation. The cells often eat so much and divide so rapidly that they deplete the entire food supply in their environment. When this happens they aggregate into a cohesive mass of thousands of cells, resembling a slug and capable of creeping across the forest floor in amoebalike movements. When it has found a new source of food, the mold enters its plantlike phase, developing a stalk with a fruiting body and looking very much like a fungus. Finally the fruit capsule bursts, shooting out thousands of dry spores from which new individual cells are born, to move about independently in the search for food, starting a new cycle of life.
Among the many multicellular organizations that evolved out of tightly knit communities of microorganisms, three—plants, fungi, and animals—have been so successful in reproducing, diversifying, and expanding over the Earth that they are classified by biologists as “kingdoms,” the broadest category of living organisms. All in all there are five of these kingdoms—bacteria (microorganisms without cell nuclei), protists (microorganisms with nucleated cells), plants, fungi, and animals. 43 Each of the kingdoms is divided into a hierarchy of subcategories, or taxa, beginning with phylum and ending with genus and species.
The theory of symbiogenesis has allowed Lynn Margulis and her colleagues to base the classification of living organisms on clear evolutionary relationships. Figure 10-1 shows in simplified form how the protists, plants, fungi, and animals all evolved from the bacteria through a series of successive symbioses, described in more detail in the following pages.
When we follow the evolution of plants and animals we find ourselves in the macrocosm and have to shift our time scale from billions of years to millions. The earliest animals evolved around 700 million years ago, and the earliest plants emerged about 200 million years later. Both evolved first in water and came ashore 400—450 million years ago, the plants preceding the animals on land by several million years. Plants and animals both developed huge multicellular organisms, but whereas intercellular communication is minimal in plants, animal cells are highly specialized and
FUNGI