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James A. Shapiro

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Cell Mergers and the Evolution of New Life Forms: Symbiogenesis Rather Than Selection

Posted: 08/21/2012 5:13 pm

In the last blog, I questioned the creative role of natural selection in evolutionary innovation. To clarify further what I had in mind, this blog will look at one of the truly creative processes of tremendous importance in evolutionary history: symbiotic mergers of two distinct organisms to generate a third new one (symbiogenesis). Without symbiogenetic mergers, we would not exist.

The classic example of symbiogenesis is the formation of lichens, the moss-like forms that live on rock surfaces. Lichens arise from a merger of a fungus and a photosynthetic microbe, either a cyanobacteria or (more commonly) an alga. The resulting lichen has both the fungus' ability to grow by spreading adherent filaments over the rocks and the photosynthetic capacity to produce food from sunlight and carbon dioxide in the atmosphere.

Lichens were considered a separate group of organisms until 1867, when Swiss botanist Simon Schwendener proposed they were a symbiotic association. It had to wait until 1939 for Eugen Thomas to artificially synthesize a lichen in the laboratory.

The great proponent of symbiogenesis as a major force in evolution was Lynn Margulis, who suddenly passed away late last year. She and her son, Dorion Sagan, summarized her ideas in the 2003 book, Acquiring Genomes: The Theory of the Origins of the Species.

Lynn was most widely known since the 1970s for championing ideas that organelles within nucleated eukaryotic cells are descended from endosymbiotic bacteria (Margulis, Origin of Eukaryotic Cells, 1970). Lynn's position was vindicated when the methods of molecular taxanomy and phylogeny, pioneered by Carl Woese at the University of Illinois (Woese 1981), made it possible to demonstrate that the oxidative energy-producing organelle of eukaryotic cells, the mitochondrion, actually descended from a specific type of bacterium.

Since all eukaryotic cells have mitochondria (or a degenerate form of this organelle), the ancestral eukaryotic cell must have had one too. Thus, the origin of the nucleated eukaryotic cell from prokaryotic (pre-nucleus) precursors involved at least one symbiogenetic event to acquire the mitochondrion.

Since all "higher" and large multicellular organisms, including ourselves, are eukaryotes, the formation of the eukaryotic cell is arguably the single most important evolutionary event since the origin of life.

It is likely, in fact, that there were additional cell mergers involved in the origins of the first eukaryote. From Woese's work, we know there are actually two kinds of prokaryotic cell: the familiar Bacteria, and other cells called Archaea because they were originally thought to be closer to the oldest (most archaic) cells. The eukaryotic cell is actually a mixture of archaea-like and bacteria-like features (Woese 1981). Thus, most theories of the origins of eukaryotes postulate a bacteria-archaea merger in addition to acquisition of the mitochondrion.

Photosynthetic organisms are the nutritional basis of most life on the planet. With the exceptions of prokaryotes that get their energy from chemical sources, sunlight provides the power for life, either directly or by providing photosynthesized food for consumption by non-photosynthetic organisms, like us.

The original photosynthetic organisms were bacteria. There are no photosynthetic archaea. There are actually three kinds of bacterial photosynthesis, and one of them produces oxygen. Oxygenic photosynthesis is also the process carried out in plants and other photosynthetic eukaryotes.

This bacterial-eukaryote similarity should hardly be surprising when we recognize that the photosynthetic organelles in eukaryotic cells, "chloroplasts" or "plastids," are all descended from an endosymbiont that belonged to the group known as cyanobacteria (blue-green photosynthetic bacteria).

In other words, all photosynthetic eukaryotes -- green plants, green algae, red algae, diatoms, and many others -- all owe their ability to use sunlight to a second, super-important symbiogenetic merger. Much of the photosynthetic capacity on earth came from cell mergers.

Symbiogenesis did not stop with two key events in the history of eukaryotes. Among photosynthetic organisms, secondary cell mergers have occurred involving both green and red algae and other lineages of eukaryotic cells. For example, diatoms (among the most abundant photosynthesizers on the planet) arose from a red algal endosymbiogenesis with a protozoan. Similarly, Euglena, a photosynthetic microorganism widely studied for its movements following light, arose from a green algal endosymbiogenesis with a protozoan relative of the sleeping sickness organism, Trypanosoma.

Since cell mergers involve independent cells with their own genomes, the symbiogenetic cells that result each has two or more genome compartments. In fact, we know the mitochondrion and plastids are descended from bacteria because we can isolate and sequence their DNA. When secondary symbiogeneses occur, the merged cells often have at least four genome compartments: the nucleus, the mitochondrion, the plastid, and a "nucleomorph" descended from the nucleus of the endosymbiotic alga.

In all these cases, there is active DNA transfer between genome compartments. Typically, DNA sequences travel from the organelle genomes to the nuclear genome. Thus, the nucleus actually encodes most of the proteins in each of its organelles, even though they have their own genomes and protein synthesis machinery.

Restructuring of both nuclear and organelle genomes is an important aspect of evolution. Some groups of organisms are actually identified by the organization of their mitochondrial DNA.

We see from the few examples discussed here that symbiogenesis by cell mergers has been an essential component in the evolution of life on earth. Once formed, symbiogenetic organisms have to succeed in the struggle for existence. But nothing about their origins involves Natural Selection.

Symbiogenesis is responsible for some of the most important innovations in evolution. It illustrates clearly why we have to think about the precise cellular and genomic events that create new organisms.

Making one organism out of two is far from a simple process. There are countless questions still to be answered about what makes these mergers succeed. The existence of so many unanswered questions illustrates that science is, as Vannevar Bush called it, the "endless frontier."

There can be few ideas less scientific than the argument that we have things all worked out, even in principle.


REFERENCES

  1. Margulis, L. (1970). Origin of Eukaryotic Cells, Yale Univ. Press.
  2. Woese, C. R. (1981). "Archaebacteria." Scientific American 244(6): 98 - 122.

 
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