Microbial Systems Ecology to Understand Cross-Feeding in Microbiomes

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.

Plant microbiota dysbiosis and the Anna Karenina Principle

“…A priority effect, primed at an early stage of microbiota composition, could lead to microbial variation between hosts [41]. In this situation, the apparent heterogeneity could be driven by microbe-microbe determinist interactions through evolution of dependencies among microorganisms [42]. Nevertheless, the host-plant could likely be the driver of a 'healthy' microbiota resulting from host-plant active microbial filtration to positively influence the plant holobiont fitness.…”

Evaluating the hologenome concept by analyzing the root-endosphere microbiota of chimeric plants

“… 46 Thus, the predominantly deterministic nature of the composition of the plant microbiota may be explained at least in part by these kinds of molecules produced and emitted by the plant that determine the composition of the microbiota. Other processes including microbe-microbe interactions either being antagonistic-(i.e., competition for niche colonization) or synergistic-interactions (e.g., evolution of dependencies among microorganisms) can occur 47 and can also explain part of the observed determinism.…”

Ecological corridors homogenize plant root endospheric mycobiota

“…fungus–fungus and fungus–bacteria) that constitute the plant microbiota may indeed impact the carrying capacity of plants for microorganisms. Interactions include competition for habitat, available nutrients, exclusion through antimicrobial compounds and reciprocally, via facilitation processes such as cross‐feeding, cometabolism, evolution of dependencies (Mataigne et al ., 2021 ), but these ideas are still mostly theoretical and empirical support is needed. Beyond these microbial interactions that putatively at least partially explain microbial community assembly, we cannot exclude possible indirect effects of T. repens on soil characteristics and thereby habitat conditions for fungi.…”