Tales from the Underground: A Natural History of Subterranean Life

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1: Origins

The origin of life appears...to be almost a miracle, so many are the conditions which would have had to be satisfied to get it going.
—Francis Crick, Life Itself: Its Nature and Origin (1981)

Why, who makes much of a miracle? As to me I know of nothing else but miracles,...Every cubic inch of space is a miracle, Every square yard of the surface of the earth is spread with the same, Every foot of the interior swarms with the same.
—Walt Whitman, Leaves of Grass (1855)

The Earth was not constructed with a delicate hand. It was hammered into shape slowly, by the brute force of a meteor bombardment that lasted hundreds of millions of years. The soils, the seas, and our primitive microbial ancestors emerged in the midst of apparent chaos and catastrophe. The process began billions of years ago as our entire solar system was congealing from a swirling cloud of hot gases and nuclear ashes left behind by exploded stars. Some of the objects colliding with the Earth at this time were plan-etesimals— objects as big as small planets. The kinetic energy released by these impacts literally shook the Earth to its core and melted much of the rocky crust and interior. Some chunks of the planetesimals and meteors became permanently embedded in the Earth, while other pieces were sent hurtling off into space like giant shrapnel. The mass of the primordial Earth accumulated slowly, like a globe that grows as a sculptor slaps on clay, one handful at a time. With greater size, Earth increased in its gravitational force, attracting even more of the wandering debris of space.

It is hard to come up with a specific date of birth for our planet, given its gradual development. Basing their calculations on the "radioactive clock"—measurements of the level of radioactive decay of certain elements found within the Earth's crust, such as uranium and lead—most geologists place the Earth's age at about four and a half billion years. The Earth went through horrendous growing pains during its first billion years. Just as the frequency of meteor impacts began to decline, violent volcanic eruptions began to spring up around the globe as the planet's hot interior "degassed." When the Earth's surface temperature finally began to cool, the massive volume of water vapor in the atmosphere condensed and poured down from the heavens in fierce rainstorms of truly biblical proportions. The torrential rains lasted millions of years, creating our oceans—the hydrosphere as we know it—in the process.

The original igneous and metamorphic rocks on the Earth's surface, left behind by volcanic eruptions and upliftings from the mantle layer below, were washed by the relentless rains, and their minerals flowed into the oceans. This was an essential first step in the formation of primitive soils that would eventually support a vibrant plant and animal life. These primitive soils lacked organic matter but contained sand, silt, and clay minerals in various proportions.

Clays are unique among the mineral components of soil. They are chemically reactive, microscopic, crystal-like structures that form out of saturated solutions of silicate and metal oxides. Sand and silt, in contrast, are large, chemically inert particles formed by the simple weathering and pulverization of rock. Some clays are crystallized deep within the Earth's mantle layer, at high temperature and pressure, and then brought to the surface by the churning motions of the Earth. This process is driven by radioactive heating deep within Earth's mantle and is part of the same plate tectonic geological cycle that gradually moves the continental crusts.

How the stardust components of our planet managed to buck the thermodynamic tendency for disorder, and organize into the intricate design of living systems, is a puzzle that has perplexed scientists for decades. This much is known: Life—the biosphere—originated sometime within those tumultuous first billion years of Earth's history. Microfossils discovered in recent years, and larger fossils formed by visible colonies of bacteria that clump together in mats called stromatolites, provide unequivocal evidence that microbial life was present as early as three and a half billion years ago, perhaps even earlier. Given what we recently have learned about the setting just prior to the emergence of these creatures—meteor bombardment, an epidemic of volcanic eruptions, and intense ultraviolet (UV) radiation (there was no ozone filter in the upper atmosphere)—many scientists are becoming convinced that the ancestors of Earth's first life forms must have originated well below the surface. Any new species that might have ventured out from Mother Earth's protective womb in those early years would have been quickly destroyed by one surface catastrophe or another, its evolutionary path nipped in the bud. The young Earth was like a war zone where the safest place to be—the only place to be—was underground.

The notion of the underground as the cradle of life is contrary to a popular theory held throughout much of the twentieth century that life began in a shallow body of water, or perhaps in the surface waters of the ocean, where evaporation might have concentrated just the right "primordial soup" of ingredients for life to emerge. This theory arose from Charles Darwin's speculation that life originated in "some warm little pond." Darwin wrote this in 1871 in an informal, private letter to his botanist colleague Joseph Dalton Hooker. It was not an idea that he had particular confidence in or intended to promote. Nevertheless, his followers took the remark quite seriously. The letter has been cited in virtually every book and review article on the subject of the origin of life since Darwin's day.

Darwin would probably be both surprised and a little dismayed to learn how much his casual comment influenced thinking on this matter in the twentieth century. In other writings, he made it abundantly clear that he felt the issue was best left to future generations, who would undoubtedly have a better foundation for tackling the subject. For example, in an 1881 letter to Nathaniel Wallich, curator of the Calcutta Botanical Gardens, Darwin refers to the issue as ultra vires (beyond the powers) of science at the time: "You expressed quite correctly my views where you said that I had intentionally left the question of the Origin of Life uncanvassed as being altogether ultra vires in the present state of knowledge."

Although it is possible that the details of the origin of life may foever be ultra vires, we have many exciting new leads to follow as we enter the twenty-first century. Most of these point toward a subterranean environment rather than a "warm little pond" as the cradle of life—possibly within the murky sediments of the ocean floor or deep within the water-filled pore spaces of the continental crusts. As we shall see, support for this idea goes well beyond the fact that the underground would have been the safest refuge from the violence and climatic turmoil of Earth's first billion years. The underground was also the place where the essential ingredients for primitive biochemistry were to be found, and where today we find bizarre microbes believed to be the direct descendants of Earth's first life forms.

Just a couple of years before Darwin wrote his frequently cited let-ter speculating about the warm little pond, another famous natural-ist of the day, Thomas Huxley, had published a bold and widely read essay entitled "On the Physical Basis of Life." Although Huxley agreed with Darwin that it was premature to attempt to pinpoint the origin of life, he explained that living organisms are constructed from atoms and that life's activities are ruled by the laws of physics and chemistry. Huxley reached very deep and stretched very far considering it would be another century before the field of molecular biology emerged. He was accused of religious heresy in many quarters, but this was nothing new for Huxley, who was already well known as a fearless and eloquent supporter of Darwin's evolutionary theory.

Huxley identified four elements as primary ingredients for the evolution of life—hydrogen, carbon, oxygen, and nitrogen. Modern chemical analyses verify that of the more than one hundred elements in our periodic table, these four account for more than 95 percent of the atoms found in the human body. The same is true for bacteria, fungi, earthworms, great white sharks, giant redwoods, you name it. This similarity in the elemental composition of all life forms (that we know of) is a point that Huxley also emphasized.

What is even more remarkable, however, is the similarity between the elemental composition of living organisms and that of the universe as a whole. Recent spectroscopy measurements of stars and interstellar dust confirm that the same four elements identified by Huxley as the main components of most of the biosphere also happen to rank within the top five in cosmic abundance. The miracle of life, as we shall see, lies in its complexity, not in the scarcity of start-up ingredients.

Hydrogen makes up more than 90 percent of all the matter in the universe, and more than 60 percent of the atoms in the human body. All of this hydrogen was formed in the fiery explosion of the "big bang" fifteen billion years ago. It is the simplest of all atoms, with a nucleus containing one proton and one neutron, orbited by a single electron. All of the other elements in the human body were forged some time later by the nuclear fusion reactions of burning stars. In these nuclear fusions, the nuclei of simple light elements, beginning with hydrogen, collide to form the larger nuclei of the heavier elements. As William Fowler said in accepting the Nobel Prize for his work on the origin of the elements in 1983: "All of us are truly and literally a little bit of stardust."

The Earth is by no means unique in the universe in containing the basic elements of life. In fact, due to the way things sorted themselves out in the initial formation of our solar system, the Earth has relatively less hydrogen, carbon, oxygen, and nitrogen than some of our planetary neighbors more distant from the sun. Nevertheless, the fact that we and all our biotic co-inhabitants are here is proof that the Earth contains enough of life's essential elements to build a thriving biosphere, provided that a system for recycling those elements is in place. Soil organisms play a central role in this recycling system, as we discuss later. The key question here is, why did life originate from these basic elements on our planet and presumably not on others?

Earth's great advantage as a life-generating planet lay not in a superior abundance of essential elements, but in the fact that many of these elements were combined into specific molecules that facilitated an evolution from geochemistry to biochemistry. The 1871 essay by Thomas Huxley goes on to identify three simple molecules that were essential for the formation of life on Earth: water (hydrogen and oxygen), carbonic acid (carbon, hydrogen, and oxygen), and ammonia (nitrogen and hydrogen). Huxley's assertion has stood the test of time. All modern theories of the origin of life recognize the important role played by these three molecules, and all concur that an abundance of one of them—water—is what is most unique about our blue planet....