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. 2017 Jun 16;8:1125.
doi: 10.3389/fmicb.2017.01125. eCollection 2017.

Synthetic Microbial Ecology: Engineering Habitats for Modular Consortia

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Free PMC article

Synthetic Microbial Ecology: Engineering Habitats for Modular Consortia

Sami Ben Said et al. Front Microbiol. .
Free PMC article

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.

Keywords: consortia assembly; engineering consortia; engineering habitats; microbial consortia; microbial ecology; modular consortia; synthetic ecology.

Figures

Figure 1
Figure 1
Conceptual overview and design of a spatially linked microbial consortium (SLMC). (A) Natural microbial consortium. (B) Artificial microbial consortium: selection of the members based on their ability to accomplish part of a bioprocess of interest (convert substrate A to product E). The reduced need for compatible environmental conditions that SLMC offers, would allow the combination of microbial species with incompatible requirements. This would enable the construction of de novo consortia (not found in nature) resulting in new products or applications. Left to right: hydrothermal vent, desert biocrust, (sub-glacial) lake Vostok, and deciduous forest. (C) Each module offers different environments to promote a specific biochemical function. Connections between modules enable interactions. (D) The modularity of SLMC would allow to incorporate this microbial consortium (sub-consortium) as part of a larger biochemical network (super-consortia). Images sources: Flickr (seedling, hydrothermal vent: Ocean Networks Canada, lake Vostok: US National Science Foundation, forest: G. Crutchley) and Arizona State University, Estelle Couradeau (biocrust).
Figure 2
Figure 2
Microfluidics vs. Bioreactors. (Top) The microfluidic platform (nL to μL) would be made of PDMS and connecting channels would allow the exchange of media and intermediate products between the chambers as well as the replacement of the cells (here only represented on one side). The fluxes would be controlled by pumps and valves. Microbial species cultured in those chambers would be contained by membranes. (Bottom) In the sequential bioreactors platform (100 mL to hL), well-stirred bioreactors would be connected by hollow-fiber bridges and overhead pressure or pumps would allow the flow of media and intermediates between bioreactors. Cells could additionally be confined by membranes (right bioreactor) should this be necessary.
Figure 3
Figure 3
Potential applications of SLMC. (A) Nitrogen removal: Nitrogen cycle and suggested layout of the consortium for direct conversion of ammonium to nitrogen gas. This bioprocess requires the conversion of part of the ammonium to nitrite under aerobic conditions (here by Nitrosomonas sp.) before the anaerobic ammonium oxidation (anammox), here performed by Candidatus Brocadia anammoxidans, can take place and combine ammonium (NH4) and nitrite (NO2) to nitrogen gas (N2). (B) Bioremediation: Porous alginate microbeads containing a microbial consortium. The left illustration represents a porous bead and an embedded microbial consortium degrading a specific pollutant. The microorganism responsible for the degradation of the pollutant (blue: e.g., Geobacter metallireducens) could be placed in the core of the porous bead, while the metabolic activities of microbes surrounding it provide the necessary anoxic conditions (green: oxygen consumer) and nutrients (red: by-products feed the blue member) the degrader requires to fulfil its catabolic function. Alternatively, all three microbes could each perform one step of a three steps biodegradation process. The right scans (electron microscope) show alginate beads, a cross-section and the porous network of such a bead. (C) Pharmaceuticals: Pharmaceutical application of modular microbial consortia. E. coli would generate the basic components as they are a prolific organisms that is easy to engineer and can produce high yields while being cost effective. As E. coli mostly lacks the ability to perform posttranslational modifications and since those are vital for the biological activity of human proteins, other systems such as yeasts (Saccharomyces cerevisiae, Pichia pastoris,..) or mammalian cells (CHO,..) could be used to modify those building blocks and produce the biologically active protein. (D) Biofuels: Biodiesel production from lignocellulosic material. Clostridium thermocellum would first break down lignocellulose into 5- and 6-carbon sugars at high temperature and anaerobic condition, that would then be fermented by Zymomonas mobilis and Pichia stipidis to ethanol. Finally, the strict aerobe Acinetobacter baylyi would convert ethanol to biodiesel. Image source (B) Soliman et al. (2013).
Figure 4
Figure 4
Co-culture vs. Sequential: steady-state values. This illustration shows the two layouts of bioreactors that are compared for their ability to convert ammonia to nitrate. In the co-culture (red) both microbial species are cultured together, whereas in the sequential scenario they grow in separate bioreactors. The first chamber contains Nitrosomonas sp. which convert ammonia (NH3) to nitrite (NO2-) and its content is fed to the second bioreactor culturing Nitrobacter sp. which oxidizes nitrite to nitrate (NO3-). The steady-state values of the microbial populations, nitrogen species (total ammonium nitrogen, TAN =N-NH3+N-NH4+, total nitrite nitrogen, TNN =N-HNO2+N-NO2- and total nitrate nitrogen, TNNa =N-HNO3+N-NO3-) and oxygen concentration (first and second bioreactor values) are listed for the co-culture and the sequential bioreactors (same pH and temperature as in co-culture). Microbial populations are given in [mg biomass/L] and the chemical species in [mg/L]. The percentages indicated next to the values are relative to the total nitrogen injected into the system (TANin) therefore the sum of all the nitrogen species is equal to the input concentration, here [TANin] = 1, 000 [mg TAN/L]. The values for the nitrogen species indicated for the sequential scenario are the output concentrations of the second bioreactor (containing Nitrobacter).
Figure 5
Figure 5
Pulsing mode. The height of the pulses represents the flux Q of media into an operational unit. The period T and pulse length L determine the duty cycle (L/T), which is the percentage of one period during which the pulse is “ON”. The volume V injected with each pulse is V = Q*L.

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