The trade-off between individual metabolic specialization and versatility determines the metabolic efficiency of microbial communities

Miaoxiao Wang; Xiaoli Chen; Yuan Fang; Xin Zheng; Ting Huang; Yong Nie; Xiao-Lei Wu

doi:10.1016/j.cels.2023.12.004

The trade-off between individual metabolic specialization and versatility determines the metabolic efficiency of microbial communities

Cell Syst. 2024 Jan 17;15(1):63-74.e5. doi: 10.1016/j.cels.2023.12.004.

Authors

Miaoxiao Wang¹, Xiaoli Chen², Yuan Fang³, Xin Zheng³, Ting Huang³, Yong Nie⁴, Xiao-Lei Wu⁵

Affiliations

¹ College of Engineering, Peking University, Beijing 100871, China; Department of Environmental Systems Science, ETH Zürich, Zürich 8092, Switzerland; Department of Environmental Microbiology, Eawag, Dübendorf 8600, Switzerland.
² College of Engineering, Peking University, Beijing 100871, China; Institute of Ocean Research, Peking University, Beijing 100871, China.
³ School of Resource and Environmental Engineering, Hefei University of Technology, Hefei 230000, China.
⁴ College of Engineering, Peking University, Beijing 100871, China. Electronic address: nieyong@pku.edu.cn.
⁵ College of Engineering, Peking University, Beijing 100871, China; Institute of Ocean Research, Peking University, Beijing 100871, China; Institute of Ecology, Peking University, Beijing 100871, China. Electronic address: xiaolei_wu@pku.edu.cn.

PMID: 38237552
DOI: 10.1016/j.cels.2023.12.004

Abstract

In microbial systems, a metabolic pathway can be either completed by one autonomous population or distributed among a consortium performing metabolic division of labor (MDOL). MDOL facilitates the system's function by reducing the metabolic burden; however, it may hinder the function by reducing the exchange efficiency of metabolic intermediates among individuals. As a result, the function of a community is influenced by the trade-offs between the metabolic specialization and versatility of individuals. To experimentally test this hypothesis, we deconstructed the naphthalene degradation pathway into four steps and introduced them individually or combinatorically into different strains with varying levels of metabolic specialization. Using these strains, we engineered 1,456 synthetic consortia and found that 74 consortia exhibited higher degradation function than both the autonomous population and rigorous MDOL consortium. Quantitative modeling provides general strategies for identifying the most effective MDOL configuration. Our study provides critical insights into the engineering of high-performance microbial systems.

Keywords: functional redundancy; metabolic division of labor; metabolic specialization; metabolic versatility; microbial communities.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Humans
Metabolic Networks and Pathways
Microbial Consortia*
Microbiota*