The Origins of Multicellularity

There are two types of organisms on the earth - those that live predominantly as unicellular organisms, and those that prefer multicellularity. Multicellular organisms contain cells that are adhered to one another, which act as a cohesive evolutionary unit.  Although it is predominantly viewed as a eukaryotic trait, it can split both directions. Protozoa, umbrella classification used for roughly 50,000 types of unicellular eukaryotes, are abundant in almost any ecosystem with abundant water and moderate temperature. Prokaryotes on the other hand, the model unicellular organism, have been recently been found to spend significant portions of their life in multicellular growth. 

The many versions of protozoa. From top left, Blepharisma japonicum; Giardia muris, a parasitic flagellate; Centropyxis aculeata, a testate (shelled) amoeba; Peridinium willei, a dinoflagellate; Chaos carolinense, a naked amoebozoan; Desmerella moniliformis, a choanoflagellate. Not shown: the 49,994 other types.

It appears that multicellular behavior has evolved independently multiple times during the history of life on earth. The first appearance of this sort of lifestyle is preserved in fossilized stromatolites, remnants of enormous bacterial biofilms that scientists think were the first lifeforms on earth. Biofilm growth is still around today - in stromatolite form through the world’s tropical oceans, and in the microscopic form that is the dominant form of bacterial growth today. 

Stromatolite fossil from Wyoming. Horizontal layers are remnants of bacterial populations, vertical displacement is reflective of time. Closer to the base is older, the phlanges are younger.

Another form of multicellularity, that’s almost as ancient, is filamentous growth. The first sign of this kind of growth first shows up in the fossil record about 500,000 thousand years after the appearance of the stromatolites - but the bacteria that displayed it had a far greater effect on planetary conditions. Roughly 2.7 billion years ago, filamentous cyanobacteria, photosynthesizing bacteria, appeared on the planet. Instead of living dispersed in the environment, these creatures have a tendency of reproducing but never finishing the job. Instead, they live as long chains, with a single cytoplasm flowing through the whole thing.

A filament of cyanobacteria.

Magnetotactic multicellular prokaryotes are another oddity - these are clusters of between one to three dozen non-nucleated cells. Bacteria, in other words. But each cell contains a handful of metal particles that allow them to orient along magnetic field lines and move towards them. The strangest thing is that despite being prokaryotic, the cells are incapable of living and reproducing freely. Kill any one cell in the community, and the whole collection dies. It’s the only example of a multicellular bacterium that doesn’t appear to have a single-celled portion of its life cycle.  portion of its life that’s lived free in the environment - even cell division. The whole thing just doubles the number of cells and then breaks in half. 

Laser confocal image of magnetotactic bacteria colony. Bright lines are cell membranes, dark space in the middle is a hollow cavity.

Replication in magnetotactic bacteria. Colony doubles in size, then performs binary fission to produce two identical daughter colonies.

These discoveries have cast a shadow on our historical understanding of bacteria as simple unicellular organisms and eukaryotes as complex multicellular ones - and have demonstrated that multicellularity has arisen independently in multiple lineages of bacteria, fungi, plants, and animals. Moreover, there is a clear delineation between multicellularity and complexity - which would have appeared sequentially, but separated in time. This sort of independent arrival at a similar mechanism is common in biology, where there is evidence of convergent solutions to the problems of power harvesting, ambulation, and cell division. In this context, multicellularity is no different.

Collective fitness

There are few first principles in biology, but evolutionary selection makes the cut. After Darwin, evolution is the process that biologists point to in order to explain why things have come to be. The explanation of structure and function comes down to an analysis of comparative advantage, selective pressures, and reproductive fitness. The current appearance of an organism is thought to be explainable by considering the various selective pressures that could have been acting on it in order to force it into one conformation or another. So if there is multicellularity, there must have been an advantage to it - especially because the trait arose in multiple independent lineages, and remained fixed in the population. What is the comparative advantage that multicellularity offers? 

Luckily, theoretical biologists (which, who knew that was a thing?) have some proposals for the kinds of pressures that could lead to a shift from single-celled to many-celled:

“A multicellular existence could have been advantageous by reducing predation, improving the efficiency of food consumption, facilitating more effective means of dispersal, limiting interactions with noncooperative individuals, or dividing labor. 

For example, unicellular lifestyle conflicts, such as the dependence of flagellum-induced motility and mitosis on the same molecular machinery, or the requirement for spatial or temporal separation of certain metabolic processes, could have been easily resolved in a multicellular setting by functional specialization, at least in principle.”

A research group at the University of Wisconsin looked at predation back in the 90s and showed some promising evidence that predation had a lot to do with the emergence of multicellularity. They did a simple experiment. Each trial began with a high density culture of single-celled algae, that had been propagated in the laboratory for thousands of generations without any alteration to it’s unicellular life cycle. To this culture researchers added a collection of flagellated protists, which were natural predators of the unicellular algae. 

Multicellular colonies of a formerly single celled algae. On the left are colonies formed after 10 days of predation, on the right an 8-celled colony formed after 100 passages.

Over the course of 100 generations, they watched their unicellular lab strain become a stabilized multicellular organism. What was even more interesting, was that their experiments demonstrated that there was an active tradeoff between the costs and benefits of multicellularity. During the early portion of the 100 days, colonies passed through a 75-cell colony phase, prior to settling at the optimal size of 8 cells per multicellular algae. 

Time is on the left axis, Chlorella cells per cluster on the right. As time progresses, the population settles on eight cells per cluster, after a short period of <75 cells per cluster halfway through the experiment. The decrease in colony size is thought to have been a result of the costs of multicellular growth.

It’s a pretty cool discovery, but there’s still a lot of work to be done. Although it would seem like predation is the answer, there are alternative explanations. There could be a chemical change due to the presence of the protist, rather than predation. There could have been a shift in the composition of the medium due to another organism sharing the space. Predation is a likely answer, but it’s hard to say that it’s the only answer, or that it’s the exact same thing that’s happening in nature.

Volvox, a multicellular algae that has settled on a larger colony size than was optimal for Chlorella. The pressures that drive cells to aggregate into progressively more complex systems are still unknown.

Next week, we’ll explore other examples of the transition between unicellularity and multicellularity - and then eventually move onto the question of complexity. How did some organisms come to evolve beyond simple multicellularity, into the complex architecture shown by plants and animals?

Part II: The Last Universal Common Ancestor

Part III: What is Life?

Part IV: The Fundamental Split