Oxygen suppression of macroscopic multicellularity

Abstract

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 O2 levels. While yeast under anaerobic and high-O2 conditions evolved to be considerably larger, intermediate O2 constrained the evolution of large size. Through sequencing and synthetic strain construction, we confirm that this is due to O2-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.

Hidden paths to endless forms most wonderful: ecology latently shapes evolution of multicellular development in predatory bacteria

“…A recently-emerged focus on eco-evo-devo seeks to quantitatively understand such ecological causation of developmental evolution 4 – 6 . Many biotic ecological factors, such as predator–prey 7 – 9 and social interactions 10 – 12 , as well as abiotic factors such as temperature 13 – 15 and oxygen level 16 – 18 , are hypothesized or known to play important roles in shaping the evolution of developmental features 5 , 19 , including developmental plasticity 20 – 26 . Direct tests for such ecological causality can be performed with experimental evo-devo, i.e., evolution experiments that examine hypotheses about multicellular development 27 .…”

Vertical growth dynamics of biofilms

“…The anaerobic strain has lost part of its mitochondrial genome and is therefore only capable of fermentation, which is not oxygen-dependent. Multicellular anaerobic yeast have recently been shown to overcome group size constraints that aerobic yeast face due to the oxygen diffusion limitation into the center of a group( Bozdag et al, 2021 ). The aerobic strain grows faster than the anaerobic strain ( Bozdag et al, 2021 ), but in each case the vertical growth dynamics proceed following the interface model.…”

“…Multicellular anaerobic yeast have recently been shown to overcome group size constraints that aerobic yeast face due to the oxygen diffusion limitation into the center of a group( Bozdag et al, 2021 ). The aerobic strain grows faster than the anaerobic strain ( Bozdag et al, 2021 ), but in each case the vertical growth dynamics proceed following the interface model. In a different vein, we directly compare the vertical growth dynamics of strains of V. cholerae with and without EPS.…”

Microphase separation of living cells

“…Finally, multicellular aerobic life is inevitably constrained by the fact that diffusion is slow over large distances [44, 45]. While the genesis of multicellularity remains debated [46], one may wonder whether microphase separation is involved and possibly reassess the role of oxygen in pattern formation and life evolution. We expect physical concepts to be instrumental in this endeavour.…”