Life on a Young Planet (24 page)

In the wake of this discovery, a number of molecular biologists, including Mitch Sogin, turned their attention to
Giardia
and other lineages
that branch early in trees based on ribosomal RNA genes.
All
contain nuclear genes of proteobacterial origin. Thus, all known eukaryotic cells show evidence of early symbiosis with bacterial cells. Either the endosymbiotic incorporation of mitochondria preceded the last common ancestor of all living eukaryotes, or early eukaryotes hosted a number of since-departed proteobacteria as symbionts or parasites. The latter possibility isn’t so far-fetched. We know from microbiological experience that proteobacteria—which include
E. coli
, the bacteria that fix nitrogen in soybean roots, and the chemosynthetic microbes that nourish tube worms along deep-sea rift vents, not to mention the bacterial vectors for Legionnaires’ disease, typhus, and Rocky Mountain spotted fever—are particularly good at taking advantage of the biological habitats offered by eukaryotes. Inserting genes for chaperone proteins into the host’s nucleus may be a widespread way of dropping proteobacterial anchor in a new biological harbor.

Regardless of how we interpret these migratory genes, comparative biology appears to leave us with few clues to the origins of eukaryotic cell biology. Or perhaps the clues are hiding in plain sight, awaiting a new Lynn Margulis to make sense of them. In a provocative essay published in 1998, William Martin and Miklos Müller hypothesized that primitively mitochondria-free eukaryotes never existed. Instead, they proposed, eukaryotic cell organization originated in a primordial symbiosis between two prokaryotes. One partner was a methanogenic archaean needing H
₂
and CO
₂
for fuel. The other was a proteobacterium able to respire aerobically in the presence of oxygen, but also able to live anaerobically by means of fermentation—producing H
₂
, CO
₂
, and acetate as waste products. Blessed with complementary metabolisms, the two partners united to form a microcosmic carbon cycle. Organic molecules produced by the methanogen were imported into the proteobacterium; the proteobacterium, in turn, provided the methanogen with the hydrogen and carbon dioxide it needed to produce more organic matter. As hydrogen levels declined in the ocean and atmosphere, driven in part by the great Proterozoic oxygen revolution, the methanogens clung ever closer to their partners, eventually jettisoning their walls and evolving flexible membranes that enabled them to maximize hydrogen gain by surrounding their bacterial confederates. In the absence of walls,
new, internal means of stabilizing cell contents were needed—and were accomplished by the evolution of cytoskeleton proteins. Genes were transferred or lost, and a new cellular organization emerged.

Martin and Müller were not the first to suggest that nucleated cells originated by primordial symbiosis, but their hypothesis is distinguished by its ecological logic as well as its phylogenetic predictions. It explains why all known eukaryotic cells contain proteobacterial genes. Further, it provides a rationale for the observation that bacterially derived genes in eukaryotes tend to be related to metabolism, while genes most closely related to those of archaeans commonly function in transcription and translation. (Note that in this view, the position of Eucarya in the Tree of Life tells us only about the ancestry of eukaryotic RNA genes; the origin of eukaryotes as new evolutionary entities requires a fusion of lineages that can’t be captured in full by phylogenies based on single genes.)

The hypothesis may even help to explain why proteobacteria have been so successful in establishing pathogenic and mutually beneficial relationships with eukaryotic organisms. Perhaps these organisms can exploit eukaryotic hosts because they recognize distantly shared genes.

The Martin-Müller hypothesis addresses one other, seemingly esoteric feature of eukaryotic cell biology. As noted earlier, eukaryotes that live in oxygen-free environments lack mitochondria. But some of them harbor another organelle, called the hydrogenosome, that directs anaerobic metabolism in these cells. More than twenty years ago Miklos Müller proposed that hydrogenosomes are, like mitochondria, energetic organelles derived from bacterial symbioses. That was a bold assertion because hydrogenosomes do not contain DNA. Thus, if they are descended from free-living bacteria, hydrogenosomes must have surrendered
all
of their genes. This claim seems preposterous, but, remarkably, increasing evidence suggests that it is correct. Studies of
Trichomonas
, a mitochondria-free parasite that contains hydrogenosomes, show that its nuclear genome contains several genes of proteobacterial origin. Moreover, the proteins encoded by these genes do their work in the hydrogenosome. Not only do hydrogenosomes appear to be proteobacterial symbionts reduced to gene-free metabolic slaves, but sequence comparisons of their telltale genes suggest that these organelles are most closely related to—mitochondria!

Despite these virtues, the Martin-Müller hypothesis can’t explain everything we know about eukaryotic cells. In recent years, scientists have begun to determine the nucleotide sequences for entire genomes—that is, for all the DNA in an organism, not just single genes. As more and more complete genomes become known, it is becoming possible to identify those genes that are shared universally and those that occur only in a specific domain.
²
Hyman Hartman and Alexei Fedorov, molecular biologists at MIT and Harvard, respectively, have identified hundreds of eukaryotic genes that do not occur in Bacteria or Archaea and, hence, appear to be molecular signatures of eukaryotic biology. Hartman and Fedorov contend that these genes identify a third partner in the aboriginal symbioses that led to eukaryotic cells, an early life-form that may be represented today only by the genes it contributed to eukaryotic cells. Not surprisingly, many of these genes relate specifically to the signature cellular features of eukaryotes—the cytoskeleton and nucleus.

Clearly, we are a long way from resolving all mysteries of eukaryotic cell origins. But hypotheses like those of Martin and Müller, and of Hartman and Fedorov, cap a strengthening view of early evolution in which nature appears not so much “red in tooth and claw” as “green in mergers and acquisitions”—a perspective as appropriate to twenty-first-century economics as competition and survival were to Victorian capitalism. These hypotheses are stimulating, radical, and provocative, just as Lynn Margulis’s thesis was in 1967. And, like Margulis’s ideas, they are catalyzing new research that promises fresh insights into one of biology’s deepest riddles. That’s what a good hypothesis does.

A P
OSTSCRIPT

Molecular investigations of eukaryotic phylogeny are currently in high gear. New genes are being sequenced, and analytical methods are improving. Equally important, biologists are sampling genes from an increasing large subset of eukaryotic diversity. The final word on eukaryotic
phylogeny is not yet in, but as shown in
figure 8.2
, increasing evidence suggests that animals are closely related to fungi (how about
that
for our family tree), and that animals fungi are further allied with amoebas and slime molds. Another branch, still contentious, unites red and green algae, supporting the thesis that the primary endosymbiosis between cyanobacteria and protozoans occurred only once. Other groupings unite apparently strange bedfellows: heterokont algae (which include kelps and diatoms) share a branch with the funguslike oomycetes, while ciliates, dinoflagellates, and plasmodia (the infectious agents of malaria) group together on a nearby limb. Perhaps most riveting, some bugs that occupied basal branches in Mitch Sogin’s early RNA-based trees have been relocated to higher limbs as more genes weigh in. Notably, the microsporidia, tiny parasites that branch near the base of the RNA tree, nest with the fungi in genetically more inclusive phylogenies. Evidently, rapid rates of evolution caused the ribosomal RNA genes of microsporidians to be quite different from those of other eukaryotes, forcing them toward the bottom of trees based on RNA gene similarity. The same may be true of some other parasites, but
Giardia
and the hydrogenosome-bearing trichomonads may persist as early branching protists. The tree is still growing and taking shape. But we now know enough that we can return to the fossil record to ask how eukaryotic evolution is reflected in Proterozoic rocks.

__________

¹
Euglenids, a group that includes tiny green flagellates, are an exception, but molecular biology and ultrastructure tell us that euglenids acquired photosynthesis by the endosymbiotic incorporation of green algal chloroplasts. Thus, their ability to harness sunlight must postdate the emergence of green algae.

²
As I write this, more than fifty species have been sequenced completely, and many more are in the pipeline.

Eukaryotic organisms have evolved patterns of cell shape and multicellularity unknown in bacteria and archaeans. Fossils with these features suggest that eukaryotes arose early, but emerged as prominent participants in marine ecosystems only late in the Proterozoic Eon, perhaps aided by renewed oxygen increase in the world’s oceans.

T
HE YOUNG MINER
taps insistently on my shoulder, gesturing vigorously and shouting (in Chinese) what must surely be instructions. He points toward a nearby truck—half a dozen workers have already dived beneath it. Being no fool, I follow their example, and seconds later an explosion jolts the ground, followed by a hail of rock debris that dents the cab above my head.

We are in Guizhou Province in southern China, visiting one of the many phosphate mines that pock the rugged landscape (
figure 9.1
). Phosphates find use in fertilizer, and the Guizhou mines play an integral role in the regional economy. What the miners don’t know is that Guizhou phosphate, spread on fields from Kunming to Kalamazoo, contains some of the most exquisite fossils ever found in Proterozoic rocks. Moreover, the fossils are predominantly eukaryotic. Sometime between the deposition of the Great Wall and these younger phosphatic rocks, nucleated organisms broke the 2-billion-year ecological hegemony of the bacteria. Prokaryotes didn’t go away, of course. They remain the foundation of all functioning ecosystems on this planet. But algae joined and then supplanted cyanobacteria as the principal primary producers in the oceans, and protozoans able to engulf microscopic victims added the complexity of predation and herbivory to food webs. Guizhou fossils provide a great introduction to the Proterozoic history of eukaryotes.

Figure 9.1.
Fossiliferous phosphate rocks of the Doushantuo Formation, exposed in a quarry at Weng’an, China.

The Guizhou phosphates lie along the thin edge of a massive wedge of sedimentary rocks deposited in southern China near the end of the Proterozoic Eon. To the north, where they are exposed in the spectacular Yangtze Gorges, these rocks can be divided into four units that lie one atop another. At the base is a discontinuous blanket of
red sandstones formed by meandering streams as they traversed a coastal plain; volcanic ash found in a thin layer within the sands yields a U-Pb age of 748 ± 12 million years. At the top of the succession is a thick cover of limestones and dolomites that contains Early Cambrian fossils in its uppermost part. In between are two units of particular interest: one provides a record of extreme climate, while the other contains spectacular fossils that have reshaped our understanding of Proterozoic life.

The lower unit, called the Nantuo Tillite, lies directly above the beds of red sandstone. A poorly sorted mixture of boulders, sand, and silt, this formation is widely distributed in southern China. Running water tends to separate sediment particles of differing size and density, so the intimate mixing of silt and football-size boulders suggests a different means of transport—ice. Other sedimentary features confirm a glacial origin for Nantuo rocks. For example, dropstones—isolated pebbles and cobbles plunged into finely laminated silts and muds—record icebergs that rafted coarse debris out onto the ocean before melting and dropping their rocky cargo onto fine-grained sediments below. Pebbles in the tillite display deeply incised striations formed by grinding as rock-studded ice moved across the landscape. Glacial rocks can be seen in younger Proterozoic successions around the world. As we shall see in
chapter 12
, they provide evidence for a series of ice ages so severe that life itself may have hung in the balance.

As the glaciers melted, rising seas began to deposit the second unit of interest—the fossiliferous Doushantuo Formation. In the Yangtze Gorges region, nearly 1,000 feet of shale, phosphatic rocks, and carbonates accumulated during two cycles of sea-level rise and fall. To the southwest, closer to the ancient shoreline, the formation thins and changes character. In Guizhou, where I got my lesson in mining safety, it is only 140–160 feet thick and consists mainly of phosphatic rocks deposited in near-shore marine environments. Only a few miles farther west, a mere 16 feet of phosphatic sandstone document this interval. To date, no volcanic rocks have been discovered in these beds, but experimental dating based on radioactive uranium and lutetium locked into phosphate crystals as they formed suggests an age of 590 to 600 million years. Encouragingly, this age falls within the range of estimates for Doushantuo deposition (younger than 600 million years and older than
555 million) based on the correlation of its fossils and chemical signatures with those of well-dated successions elsewhere.