Resource plasticity-driven carbon-nitrogen budgeting enables specialization and division of labor in a clonal community.

Sriram Varahan,Adhish Walvekar,Vaibhhav Sinha,Sandeep Krishna,Sunil Laxman

doi:10.7554/elife.57609

Abstract

Previously, we found that in glucose-limited Saccharomyces cerevisiae colonies, metabolic constraints drive cells into groups exhibiting gluconeogenic or glycolytic states. In that study, threshold amounts of trehalose - a limiting, produced carbon-resource, controls the emergence and self-organization of cells exhibiting the glycolytic state, serving as a carbon source that fuels glycolysis (Varahan et al., 2019). We now discover that the plasticity of use of a non-limiting resource, aspartate, controls both resource production and the emergence of heterogeneous cell states, based on differential metabolic budgeting. In gluconeogenic cells, aspartate is a carbon source for trehalose production, while in glycolytic cells using trehalose for carbon, aspartate is predominantly a nitrogen source for nucleotide synthesis. This metabolic plasticity of aspartate enables carbon-nitrogen budgeting, thereby driving the biochemical self-organization of distinct cell states. Through this organization, cells in each state exhibit true division of labor, providing growth/survival advantages for the whole community.

Highlights

During the development of microbial communities, groups of cells come together and exhibit heterogeneity within spatial organization (Ackermann 2015)
Amino acid driven gluconeogenesis is critical for emergence of metabolic heterogeneity: In a previous study (Varahan et al, 2019), we discovered that trehalose controls the emergence of spatially organized, metabolically heterogeneous groups of cells within a yeast colony growing in low glucose
In 81 this system, cells start in a gluconeogenic state, and these cells produce trehalose

Summary

Introduction

During the development of microbial communities, groups of cells come together and exhibit heterogeneity within spatial organization (Ackermann 2015). Cells can present specialization of function, which allows the community as a whole to perform various tasks including the acquisition of food, defense against competing microorganisms, or more efficient growth (Newman, 2016; Niklas, 2014; West and Cooper, 2016) This division of labor allows breakdown of complex biological processes into simpler steps, eliminating the need for individual cells to perform several tasks simultaneously, thereby enhancing the overall efficiency with which cells in the community function 2012; Rueffler et al, 2012; van Gestel et al, 2015) Due to these advantages, division of labor is widely prevalent across diverse microbial communities and can be found at different levels of biological organization (Gordon, 2016; Kirk, 2003; Tarnita et al, 2013). The underlying rules that enable division of labor within cell populations remain to be deciphered

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