De novo evolution of macroscopic multicellularity

G. Ozan Bozdag (), Seyed Alireza Zamani-Dahaj, Thomas C. Day, Penelope C. Kahn, Anthony J. Burnetti, Dung T. Lac, Kai Tong, Peter L. Conlin, Aishwarya H. Balwani, Eva L. Dyer, Peter J. Yunker () and William C. Ratcliff ()
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G. Ozan Bozdag: Georgia Institute of Technology
Seyed Alireza Zamani-Dahaj: Georgia Institute of Technology
Thomas C. Day: Georgia Institute of Technology
Penelope C. Kahn: Georgia Institute of Technology
Anthony J. Burnetti: Georgia Institute of Technology
Dung T. Lac: Georgia Institute of Technology
Kai Tong: Georgia Institute of Technology
Peter L. Conlin: Georgia Institute of Technology
Aishwarya H. Balwani: Georgia Institute of Technology
Eva L. Dyer: Georgia Institute of Technology
Peter J. Yunker: Georgia Institute of Technology
William C. Ratcliff: Georgia Institute of Technology

Nature, 2023, vol. 617, issue 7962, 747-754

Abstract: Abstract While early multicellular lineages necessarily started out as relatively simple groups of cells, little is known about how they became Darwinian entities capable of sustained multicellular evolution1–3. Here we investigate this with a multicellularity long-term evolution experiment, selecting for larger group size in the snowflake yeast (Saccharomyces cerevisiae) model system. Given the historical importance of oxygen limitation4, our ongoing experiment consists of three metabolic treatments5—anaerobic, obligately aerobic and mixotrophic yeast. After 600 rounds of selection, snowflake yeast in the anaerobic treatment group evolved to be macroscopic, becoming around 2 × 104 times larger (approximately mm scale) and about 104-fold more biophysically tough, while retaining a clonal multicellular life cycle. This occurred through biophysical adaptation—evolution of increasingly elongate cells that initially reduced the strain of cellular packing and then facilitated branch entanglements that enabled groups of cells to stay together even after many cellular bonds fracture. By contrast, snowflake yeast competing for low oxygen5 remained microscopic, evolving to be only around sixfold larger, underscoring the critical role of oxygen levels in the evolution of multicellular size. Together, this research provides unique insights into an ongoing evolutionary transition in individuality, showing how simple groups of cells overcome fundamental biophysical limitations through gradual, yet sustained, multicellular evolution.

Date: 2023
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DOI: 10.1038/s41586-023-06052-1

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