Disadvantages and benefits of evolved unicellularity versus multicellularity in budding yeast.

Jennie J Kuzdzal‐Fick,Lin Chen,Gábor Balázsi

doi:10.1002/ece3.5322

Abstract

Multicellular organisms appeared on Earth through several independent major evolutionary transitions. Are such transitions reversible? Addressing this fundamental question entails understanding the benefits and costs of multicellularity versus unicellularity. For example, some wild yeast strains form multicellular clumps, which might be beneficial in stressful conditions, but this has been untested. Here, we show that unicellular yeast evolve from clump‐forming ancestors by propagating samples from suspension after larger clumps have settled. Unicellular yeast strains differed from their clumping ancestors mainly by mutations in the AMN1 (Antagonist of Mitotic exit Network) gene. Ancestral yeast clumps were more resistant to freeze/thaw, hydrogen peroxide, and ethanol stressors than their unicellular counterparts, but they grew slower without stress. These findings suggest disadvantages and benefits to multicellularity and unicellularity that may have impacted the emergence of multicellular life forms.

Highlights

Multicellularity has evolved over 20 different times on Earth, leading to complex life forms in algae, animals, plants, and fungi (Grosberg & Strathmann, 2007)
Unicellular yeast strains differed from their clumping ancestors mainly by mutations in the AMN1 (Antagonist of Mitotic exit Network) gene
Ancestral yeast clumps were more resistant to freeze/ thaw, hydrogen peroxide, and ethanol stressors than their unicellular counterparts, but they grew slower without stress. These findings suggest disadvantages and ben‐ efits to multicellularity and unicellularity that may have impacted the emergence of multicellular life forms

Summary

| INTRODUCTION

Multicellularity has evolved over 20 different times on Earth, leading to complex life forms in algae, animals, plants, and fungi (Grosberg & Strathmann, 2007). Addressing this problem requires charting the environment‐dependent downsides and benefits of unicellularity versus multicellularity. Clumps form by incomplete daughter cell separation, as budding continues while daughter cells remain attached to the mother cell (Kuranda & Robbins, 1991). Such yeast clumps aid nutrient acquisition in sucrose (Koschwanez et al, 2011), but their role in stress response is unclear. To address these questions, here we compared how various en‐ vironmental stressors affect the growth of genetically similar clump‐ forming and unicellular “EvoTop” yeast cells that we obtained by reversing the strategy of “snowflake” yeast evolution (Ratcliff et al, 2012). This work sheds light on the genetic bases, as well as on the disadvantages and benefits of unicellularity versus clump‐ ing multicellularity in yeast, with implications for bidirectional transi‐ tions between other unicellular and multicellular life forms

| MATERIALS AND METHODS

Findings

| DISCUSSION