skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


This content will become publicly available on January 30, 2026

Title: Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity
Oxygen availability is a key factor in the evolution of multicellularity, as larger and more sophisticated organisms often require mechanisms allowing efficient oxygen delivery to their tissues. One such mechanism is the presence of oxygen-binding proteins, such as globins and hemerythrins, which arose in the ancestor of bilaterian animals. Despite their importance, the precise mechanisms by which oxygen-binding proteins influenced the early stages of multicellular evolution under varying environmental oxygen levels are not yet clear. We address this knowledge gap by heterologously expressing the oxygen-binding proteins myoglobin and myohemerythrin in snowflake yeast, a model system of simple, undifferentiated multicellularity. These proteins increased the depth and rate of oxygen diffusion, increasing the fitness of snowflake yeast growing aerobically. Experiments show that, paradoxically, oxygen-binding proteins confer a greater fitness benefit for larger organisms when O2is least limiting. We show via biophysical modeling that this is because facilitated diffusion is more efficient when oxygen is abundant, transporting a greater quantity of O2which can be used for metabolism. By alleviating anatomical diffusion limitations to oxygen consumption, the evolution of oxygen-binding proteins in the oxygen-rich Neoproterozoic may have been a key breakthrough enabling the evolution of increasingly large, complex multicellular metazoan lineages.  more » « less
Award ID(s):
1845363
PAR ID:
10584986
Author(s) / Creator(s):
; ; ; ;
Editor(s):
Shou, Wenying
Publisher / Repository:
PLOS Biology
Date Published:
Journal Name:
PLOS Biology
Volume:
23
Issue:
1
ISSN:
1545-7885
Page Range / eLocation ID:
e3002975
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; (, Nature Communications)
    null (Ed.)
    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 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. 
    more » « less
  2. ; ; ; ; ; ; (, eLife)
    Mitri, S (Ed.)
    A key step in the evolutionary transition to multicellularity is the origin of multicellular groups as biological individuals capable of adaptation. Comparative work, supported by theory, suggests clonal development should facilitate this transition, although this hypothesis has never been tested in a single model system. We evolved 20 replicate populations of otherwise isogenic clonally reproducing ‘snowflake’ yeast (Δace2/∆ace2) and aggregative ‘floc’ yeast (GAL1p::FLO1 /GAL1p::FLO1) with daily selection for rapid growth in liquid media, which favors faster cell division, followed by selection for rapid sedimentation, which favors larger multicellular groups. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Aggregative floc yeast obtained nearly all their increased fitness from faster growth, not improved group survival; indicating that selection acted primarily at the level of cells. In contrast, clonal snowflake yeast mainly benefited from higher group-dependent fitness, indicating a shift in the level of Darwinian individuality from cells to groups. Through genome sequencing and mathematical modeling, we show that the genetic bottlenecks in a clonal life cycle also drive much higher rates of genetic drift—a result with complex implications for this evolutionary transition. Our results highlight the central role that early multicellular life cycles play in the process of multicellular adaptation. 
    more » « less
  3. ; ; ; ; ; ; (, bioRxiv)
    The ecological and evolutionary success of multicellular lineages is due in no small part to their increased size relative to unicellular ancestors. However, large size also poses biophysical challenges, especially regarding the transport of nutrients to all cells; these constraints are typically overcome through multicellular innovations (e.g., a circulatory system). Here we show that an emergent biophysical mechanism — spontaneous fluid flows arising from metabolically-generated density gradients — can alleviate constraints on nutrient transport, enabling exponential growth in nascent multicellular clusters of yeast lacking any multicellular adaptations for nutrient transport or fluid flow. Surprisingly, beyond a threshold size, the metabolic activity of experimentally-evolved snowflake yeast clusters drives large-scale fluid flows that transport nutrients throughout the cluster at speeds comparable to those generated by the cilia of extant multicellular organisms. These flows support exponential growth at macroscopic sizes that theory predicts should be diffusion limited. This work demonstrates how simple physical mechanisms can act as a ‘biophysical scaffold’ to support the evolution of multicellularity by opening up phenotypic possibilities prior to genetically-encoded innovations. More broadly, our findings highlight how cooption of conserved physical processes is a crucial but underappreciated facet of evolutionary innovation across scales. 
    more » « less
  4. ; ; ; ; ; ; ; ; ; (, Nature Ecology & Evolution)
    The evolution of multicellular life spurred evolutionary radiations, fundamentally changing many of Earth’s ecosystems. Yet little is known about how early steps in the evolution of multicellularity affect eco-evolutionary dynamics. Through long-term experimental evolution, we observed niche partitioning and the adaptive divergence of two specialized lineages from a single multicellular ancestor. Over 715 daily transfers, snowflake yeast were subjected to selection for rapid growth, followed by selection favouring larger group size. Small and large cluster-forming lineages evolved from a monomorphic ancestor, coexisting for over ~4,300 generations, specializing on divergent aspects of a trade-off between growth rate and survival. Through modelling and experimentation, we demonstrate that coexistence is maintained by a trade-off between organismal size and competitiveness for dissolved oxygen. Taken together, this work shows how the evolution of a new level of biological individuality can rapidly drive adaptive diversification and the expansion of a nascent multicellular niche, one of the most historically impactful emergent properties of this evolutionary transition. 
    more » « less
  5. ; ; ; ; ; ; ; (, Evolution Letters)
    Abstract The evolution of multicellularity represents a major transition in life’s history, enabling the rise of complex organisms. Multicellular groups can evolve through multiple developmental modes, but a common step is the formation of permanent cell–cell attachments after division. The characteristics of the multicellular morphology that emerges have profound consequences for the subsequent evolution of a nascent multicellular lineage, but little prior work has investigated these dynamics directly. Here, we examine a widespread yet understudied emergent multicellular morphology: cuboidal packing. Extinct and extant multicellular organisms across the tree of life have evolved to form groups in which spherical cells divide but remain attached, forming approximately cubic subunits. To experimentally investigate the evolution of cuboidal cell packing, we used settling selection to favor the evolution of simple multicellularity in unicellular, spherical Schizosaccharomyces pombe yeast. Multicellular clusters with cuboidal organization rapidly evolved, displacing the unicellular ancestor. These clusters displayed key hallmarks of an evolutionary transition in individuality: groups possess an emergent life cycle driven by physical fracture, group size is heritable, and they respond to group-level selection via multicellular adaptation. In 2 out of 5 lineages, group formation was driven by mutations in the ace2 gene, preventing daughter cell separation after division. Remarkably, ace2 mutations also underlie the transition to multicellularity in Saccharomyces cerevisiae and Candida glabrata, lineages that last shared a common ancestor >300 million years ago. Our results provide insight into the evolution of cuboidal cell packing, an understudied multicellular morphology, and highlight the deeply convergent potential for a transition to multicellular individuality within fungi. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email