OXFORD UNIVERSITY PRESS, JULY 2014The past 20 years has seen the tree of life take quite a beating. In the 1990s, the time-honored notion that the genealogy of all living beings could be represented as a single branching tree began to look shaky. By the turn of the century it had collapsed under a mound of molecular data too chaotic to ignore. Researchers found prokaryotic organisms—bacteria and archaea—to engage in rampant genetic exchange, both within and among their ranks. The extent of this horizontal gene transfer between distantly related prokaryotes is such that many biologists now see the tree of life as more of a tangled web, through which genes have flowed both vertically and horizontally since the dawn of cellular life on our planet.
Long before genomes could be sequenced and the implications of interspecies gene swapping debated, an even more perplexing issue was brought to bear on the sanctity of life’s tree: endosymbiosis. In the 1960s and ’70s, the American biologist Lynn Margulis (1938–2011) championed the idea that certain compartments within eukaryotic cells had evolved from once free-living bacteria. Fueled by the mixing and matching of genes from two evolutionarily distinct cells, endosymbiosis led to the formation of a single new organism with emergent and transformative biochemical properties.
The idea that our mitochondria and the light-gathering chloroplasts of algae and plants originated from outside the eukaryotic cell was heretical. It was also surprisingly old, having been published in various guises more than 100 years ago by scientists in Germany and Russia. But 40 years ago, it was an idea whose time had come. In One Plus One Equals One: Symbiosis and the Evolution of Complex Life, I tell the story of how molecular biology was used to test the endosymbiont hypothesis for the origins of mitochondria and chloroplasts. It was one of the first fundamental scientific problems to be addressed using molecular phylogenetics. The outcome marked a turning point in our understanding of cellular evolution.
The genetic material within the mitochondria and chloroplasts of present-day organisms was, even with 1970s-style technologies, demonstrably bacterial, highly distinct from that residing in the cell nucleus. Within a decade the molecular evidence for endosymbiosis was unassailable. What remained, what still remains, is to iron out the details.
Oxygenic photosynthesis evolved in the ancestors of aquatic cyanobacteria, entered the eukaryotic domain, and led to the very first chloroplast-bearing alga, paving the way for the colonization of land and the greening of planet Earth. A more recent and unexpected twist is the realization that cyanobacterium-derived chloroplasts have been passed from eukaryote to eukaryote: the ability to harness the sun’s energy is a precious commodity. Many ecologically significant algae—think planktonic diatoms and red tide–forming dinoflagellates—are in fact the cellular equivalent of Russian nesting dolls: cells within cells within cells whose nested sets of genomes reveal who ate whom in the distant and not-so-distant past. (See “Steal My Sunshine,” January 2013.)
When and precisely how the myriad internal structures that define the eukaryotic cell itself arose from simpler prokaryotic forms is much less obvious. The traditional view is that the nucleus, internal cytoskeleton, and other complex features arose in a stepwise fashion before the engulfment of the bacterium that was to become the mitochondrion. An increasingly popular alternative is that eukaryotic cellular complexity arose contemporaneously with the mitochondrion, powered by its novel metabolic capacities.
Which of these two scenarios is closer to the truth is not yet clear. What we know is that endosymbiosis has had a profound impact on the course of evolution. Complex cells probably wouldn’t have evolved without it; multicellular animals could not have arisen without the oxygen liberated by algal chloroplasts; and we wouldn’t be here to ask big questions of the world around us.
John Archibald is professor of biochemistry and molecular biology at Dalhousie University in Halifax, Nova Scotia, and a senior fellow of the Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity. Read an excerpt of One Plus One Equals One: Symbiosis and the Evolution of Complex Life.