Microbial Systems Ecology to Understand Cross-Feeding in Microbiomes.

Victor Mataigne,Nathan Vannier,Stéphane Hacquard,Philippe Vandenkoornhuyse

doi:10.3389/fmicb.2021.780469

Abstract

Understanding how microorganism-microorganism interactions shape microbial assemblages is a key to deciphering the evolution of dependencies and co-existence in complex microbiomes. Metabolic dependencies in cross-feeding exist in microbial communities and can at least partially determine microbial community composition. To parry the complexity and experimental limitations caused by the large number of possible interactions, new concepts from systems biology aim to decipher how the components of a system interact with each other. The idea that cross-feeding does impact microbiome assemblages has developed both theoretically and empirically, following a systems biology framework applied to microbial communities, formalized as microbial systems ecology (MSE) and relying on integrated-omics data. This framework merges cellular and community scales and offers new avenues to untangle microbial coexistence primarily by metabolic modeling, one of the main approaches used for mechanistic studies. In this mini-review, we first give a concise explanation of microbial cross-feeding. We then discuss how MSE can enable progress in microbial research. Finally, we provide an overview of a MSE framework mostly based on genome-scale metabolic-network reconstruction that combines top-down and bottom-up approaches to assess the molecular mechanisms of deterministic processes of microbial community assembly that is particularly suitable for use in synthetic biology and microbiome engineering.

Highlights

Deciphering the assembly rules of microbial communities is vital for a mechanistic understanding of the general principles driving microbiome activity and functions (Vellend et al, 2014; Morrison-Whittle and Goddard, 2015)
Microbial communities are governed by both stochastic and deterministic factors (Vellend, 2010; Stegen et al, 2012), and recent advances show that deterministic processes largely contribute to shaping microbial community assembly
Their relative contribution varies according to the ecology of microorganisms and the stability of the environment (Figure 1E, Stegen et al, 2012; Ning et al, 2020; Xu et al, 2020)

Summary

INTRODUCTION

Deciphering the assembly rules of microbial communities is vital for a mechanistic understanding of the general principles driving microbiome activity and functions (Vellend et al, 2014; Morrison-Whittle and Goddard, 2015). Results vary and some studies suggest that microbial communities are governed by antagonistic interactions and rarely cross-feed or cooperate (Biggs et al, 2017; Venturelli et al, 2018), others revealed rich networks of metabolic interactions among microorganisms (Medlock et al, 2018). In a set of five bacteria, such models found that species-specific metabolism is related to secondary metabolism, and metabolic cooperation was required to perform copper bioleaching, an important biohydrometallurgic process in ancient microbial communities that harbors an economic interest (Bordron et al, 2016) Such a community was chosen for its simplicity, allowing a reductionist approach while maintaining realistic ecological conditions. In order to obtain a holistic and mechanistic view, an integration of all approaches is required

Metabolic Network Reconstruction

CONCLUSION