Oxygen suppression of macroscopic multicellularity

• Published in: Nature communications 2021-05, Vol.12 (1), p.2838-10, Article 2838
• Main Authors: Bozdag, G. Ozan, Libby, Eric, Pineau, Rozenn, Reinhard, Christopher T., Ratcliff, William C.
• Format: Article
• Language: English
• Subjects: 42/35; 45; 45/23; 631/181/2468; 631/181/2475; 64; 704/445/3929; Aerobiosis; Anaerobic conditions; Anaerobiosis; Astrobiology; Atmospheric models; Biological Evolution; Biophysical Phenomena; Directed Molecular Evolution; Divergence; DNA-Binding Proteins - genetics; Eukaryotic Cells - cytology; Eukaryotic Cells - metabolism; Evolution; Gene Deletion; Genetic Engineering; Humanities and Social Sciences; Mathematical models; Metabolism; Models, Biological; multidisciplinary; Oceans; Organisms; Oxygen; Oxygen - metabolism; Oxygenation; Physiology; Respiration; Saccharomyces cerevisiae - cytology; Saccharomyces cerevisiae - genetics; Saccharomyces cerevisiae - metabolism; Saccharomyces cerevisiae Proteins - genetics; Science; Science (multidisciplinary); Selection, Genetic; Sequences; Synthetic Biology; Transcription Factors - genetics; Yeast; Yeasts
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-021-23104-0

Atmospheric oxygen is thought to have played a vital role in the evolution of large, complex multicellular organisms. Challenging the prevailing theory, we show that the transition from an anaerobic to an aerobic world can strongly suppress the evolution of macroscopic multicellularity. Here we select for increased size in multicellular ‘snowflake’ yeast across a range of metabolically-available O 2 levels. While yeast under anaerobic and high-O 2 conditions evolved to be considerably larger, intermediate O 2 constrained the evolution of large size. Through sequencing and synthetic strain construction, we confirm that this is due to O 2 -mediated divergent selection acting on organism size. We show via mathematical modeling that our results stem from nearly universal evolutionary and biophysical trade-offs, and thus should apply broadly. These results highlight the fact that oxygen is a double-edged sword: while it provides significant metabolic advantages, selection for efficient use of this resource may paradoxically suppress the evolution of macroscopic multicellular organisms. The evolution of multicellular life is hypothesized to have been promoted by rising oxygen levels. Through experimental evolution and modeling, Bozdag et al. demonstrate that our planet’s first oxygenation would have strongly constrained, not promoted, the evolution of multicellular life.