Clonal-Aggregative Multicellularity: Adaptation to Extreme Salinity Gives Rise to Unconventional Intermediate Cellular Mechanism

Just when experts thought they had almost understood the origins of multicellular life, evolution throws another surprise. In a remarkable discovery, a group of scientists has just found a third kind of unconventional multicellularity which combines those we already knew about.

Kinds of Multicellularity

Multicellular organisms are those that are composed of more than one cell, with groups of cells working together to perform specialized functions. The emergence of multicellular organisms is considered as one of the most important breakthroughs of evolution, with several paths leading to multicellular arrangements.

 It was believed that multicellularity has evolved 45 times or more across the tree of life. Yet, the ancestor of each multicellular family relied on only one of two methods - either the individual cells stick together as they split, or those that have previously split come back together.

Clonal multicellularity involves cells remaining connected as they divide over and over again, giving rise to simple organisms and those with specialized tissues. Meanwhile, aggregation involves temporary clustering of free-living cells in response to predation or harsh environmental conditions.

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Unconventional Path to Multicellular Lifeforms

Evolutionary biologist Núria Ros-Rocher from the Pasteur Institute in France made a surprising discovery while studying choanoflagellates. These organisms are single-celled, water-dwelling creatures which form short-lived colonies and represent the closest living unicellular relatives of animals.

Ros-Rocher and her team were specifically observing a choanoflagellate known as Choanoeca flexa. This species creates remarkable colonies which look like exploding fireworks. Their behavior can help scientists better understand gastrulation, which is a vital step in embryonic development.

The researchers have observed that choanoflagellates always formed colonies through cell division, where they replicate themselves to increase their numbers. So nothing was unusual when the team saw cells dividing inside Choanoeca flexa colonies. However, they also noticed that these colonies reformed very fast after being separated by light forces, something that is too fast to be attributed to cell division.

When the scientists used fluorescent dyes to stain various types of Choanoeca flexa cells, they noticed distinct single-cell populations that form dual-labeled chimeric clusters. This would not be possible if they had divided from the same founder cell.

At first, Ros-Rocher and colleagues questioned their strange observations. But findings of the imaging experiments made them realize that the species can either aggregate into single-layer, sheet-like colonies or develop clonally. In other words, Choanoeca flexa can form through a purely clonal process, purely aggregative process, or a combination of both.

Further studies revealed that the multicellular form of Choanoeca flexa relied on the conditions of the shallow seawater pools in which they were found. When the salinity of the tidal pools tripled as the seawater evaporated, the colonies separated into single cyst-like cells to avoid getting dried out. When rehydrated in the laboratory, they reform colonies by aggregating and then dividing.

According to cell biologist Thibaut Brunet, the researchers have found an environmentally entrailed life cycle, where evaporation causes fast transitions into and out of multicellularity. The details of the study are discussed in the paper "Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals."

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