Atmospheric oxygen is thought to have played a vital role in the evolution of complex multicellular organisms. The so-called oxygen control hypothesis is the dominant explanation causally linking the concentration of oxygen with multicellular size. The hypothesis posits that, in organisms that lack a circulatory system, the ability for oxygen to diffuse into an organism places limits on organism size. It thus predicts that increasing atmospheric oxygen should generally increase the depth to which oxygen can diffuse, increasing the maximum size that can be attained before diffusive oxygen limitation impedes growth. The oxygen control hypothesis has proven difficult to test in a lab. Yet a team of scientists from the Georgia Institute of Technology, Umeå University and NASA’s Astrobiology Institute found a way — using directed evolution, synthetic biology, and mathematical modeling — all brought to bear on a simple multicellular lifeform called a ‘snowflake yeast.’
“The positive effect of oxygen on the evolution of multicellularity is entirely dose-dependent — our planet’s first oxygenation would have strongly constrained, not promoted, the evolution of multicellular life,” said Dr. G. Ozan Bozdag, a researcher in the School of Biological Sciences at the Georgia Institute of Technology.
“The positive effect of oxygen on multicellular size may only be realized when it reaches high levels.”
“We show that the effect of oxygen is more complex than previously imagined,” added Dr. Will Ratcliff, a researcher in the School of Biological Sciences at the Georgia Institute of Technology and NASA’s Astrobiology Institute.
“The early rise in global oxygen should in fact strongly constrain the evolution of macroscopic multicellularity, rather than selecting for larger and more complex organisms.”
“People have long believed that the oxygenation of Earth’s surface was helpful — some going so far as to say it is a precondition — for the evolution of large, complex multicellular organisms.”
“But nobody has ever tested this directly, because we haven’t had a model system that is both able to undergo lots of generations of evolution quickly, and able to grow over the full range of oxygen conditions, from anaerobic conditions up to modern levels.”
The researchers were able to do that, however, with snowflake yeast, simple multicellular organisms capable of rapid evolutionary change.
By varying their growth environment, they evolved snowflake yeast for over 800 generations in the lab with selection for larger size.
“I was astonished to see that multicellular yeast doubled their size very rapidly when they could not use oxygen, while populations that evolved in the moderately oxygenated environment showed no size increase at all. This effect is robust — even over much longer timescales,” Dr. Bozdag said.
“Our work not only challenges the oxygen control hypothesis, it also helps science understand why so little apparent evolutionary innovation was happening in the world of multicellular organisms in the billion years after the Great Oxygenation Event,” Dr. Ratcliff said.
“Geologists call this period the ‘Boring Billion’ in Earth’s history — a period when oxygen was present in the atmosphere, but at low levels, and multicellular organisms stayed relatively small and simple.”
The study was published in the journal Nature Communications.
G.O. Bozdag et al. 2021. Oxygen suppression of macroscopic multicellularity. Nat Commun 12, 2838; doi: 10.1038/s41467-021-23104-0