Synthetic Microbial Ecology: Engineering Habitats for Modular Consortia

Abstract

The metabolic diversity present in microbial communities enables cooperation toward accomplishing more complex tasks than possible by a single organism. Members of a consortium communicate by exchanging metabolites or signals that allow them to coordinate their activity through division of labor. In contrast with monocultures, evidence suggests that microbial consortia self-organize to form spatial patterns, such as observed in biofilms or in soil aggregates, that enable them to respond to gradient, to improve resource interception and to exchange metabolites more effectively. Current biotechnological applications of microorganisms remain rudimentary, often relying on genetically engineered monocultures (e.g., pharmaceuticals) or mixed-cultures of partially known composition (e.g., wastewater treatment), yet the vast potential of “microbial ecological power” observed in most natural environments, remains largely underused. In line with the Unified Microbiome Initiative (UMI) which aims to “discover and advance tools to understand and harness the capabilities of Earth's microbial ecosystems,” we propose in this concept paper to capitalize on ecological insights into the spatial and modular design of interlinked microbial consortia that would overcome limitations of natural systems and attempt to optimize the functionality of the members and the performance of the engineered consortium. The topology of the spatial connections linking the various members and the regulated fluxes of media between those modules, while representing a major engineering challenge, would allow the microbial species to interact. The modularity of such spatially linked microbial consortia (SLMC) could facilitate the design of scalable bioprocesses that can be incorporated as parts of a larger biochemical network. By reducing the need for a compatible growth environment for all species simultaneously, SLMC will dramatically expand the range of possible combinations of microorganisms and their potential applications. We briefly review existing tools to engineer such assemblies and optimize potential benefits resulting from the collective activity of their members. Prospective microbial consortia and proposed spatial configurations will be illustrated and preliminary calculations highlighting the advantages of SLMC over co-cultures will be presented, followed by a discussion of challenges and opportunities for moving forward with some designs.

From Axenic to Mixed Cultures: Technological Advances Accelerating a Paradigm Shift in Microbiology

“…Engineering of microbial consortia is, although technical challenging, implementable for industrial and biotech purposes [111,112]. The group of Akio Ozaki showed large-scale production of commercially-valuable mono-and oligosaccharides by tri-partite cultures of recombinant E. coli strains and Corynebacterium ammoniagenes [113,114].…”

Synthetic Biology for Terraformation Lessons from Mars, Earth, and the Microbiome

“…All biological macro-molecules are mainly formed by a small subset of atoms, namely H, C, N, O, S, and P. These are the main building blocks of planetary biogeochemical cycles: a set of nested abiotic acid-based and biotic red-ox reactions, have evolved to require low external energy. The biological fluxes of these elements are carried out by reversible metabolic pathways of synergistic cooperation of multi-species assemblages [167,168]. In this context, engineering closed catalytic populations might be essential to all the scenarios discussed here.…”

Artificial Microbial Arenas: Materials for Observing and Manipulating Microbial Consortia

“…Physical separation in spatially linked consortia (top) and artificial microbial arenas for cocultivation (bottom). The top scheme was adapted under the terms of the CC‐BY 4.0 Creative Commons license ( https://creativecommons.org/licenses/by/4.0/) . Copyright 2017, The Authors, published by Frontiers Media SA.…”