Artificial consortium demonstrates emergent properties of enhanced cellulosic-sugar degradation and biofuel synthesis

Abstract

Planktonic cultures, of a rationally designed consortium, demonstrated emergent properties that exceeded the sums of monoculture properties, including a >200% increase in cellobiose catabolism, a >100% increase in glycerol catabolism, a >800% increase in ethanol production, and a >120% increase in biomass productivity. The consortium was designed to have a primary and secondary-resource specialist that used crossfeeding with a positive feedback mechanism, division of labor, and nutrient and energy transfer via necromass catabolism. The primary resource specialist was Clostridium phytofermentans (a.k.a. Lachnoclostridium phytofermentans), a cellulolytic, obligate anaerobe. The secondary-resource specialist was Escherichia coli, a versatile, facultative anaerobe, which can ferment glycerol and byproducts of cellobiose catabolism. The consortium also demonstrated emergent properties of enhanced biomass accumulation when grown as biofilms, which created high cell density communities with gradients of species along the vertical axis. Consortium biofilms were robust to oxic perturbations with E. coli consuming O2, creating an anoxic environment for C. phytofermentans. Anoxic/oxic cycling further enhanced biomass productivity of the biofilm consortium, increasing biomass accumulation ~250% over the sum of the monoculture biofilms. Consortium emergent properties were credited to several synergistic mechanisms. E. coli consumed inhibitory byproducts from cellobiose catabolism, driving higher C. phytofermentans growth and higher cellulolytic enzyme production, which in turn provided more substrate for E. coli. E. coli necromass enhanced C. phytofermentans growth while C. phytofermentans necromass aided E. coli growth via the release of peptides and amino acids, respectively. In aggregate, temporal cycling of necromass constituents increased flux of cellulose-derived resources through the consortium. The study establishes a consortia-based, bioprocessing strategy built on naturally occurring interactions for improved conversion of cellulose-derived sugars into bioproducts.

Interaction Networks Are Driven by Community-Responsive Phenotypes in a Chitin-Degrading Consortium of Soil Microbes

“…Central to these functions are interactions between the species that comprise soil microbial communities ( 4 – 6 ). While the combined genomic and metabolic potential of the individual species of the soil microbiome is vast, novel functions can emerge at the community level through metabolic interactions ( 7 ). A better understanding of these interactions will lead to a more complete view of the constituent organism’s and community’s functional capacity and will greatly expand our knowledge of how interaction networks can be affected by nutrient or environmental shifts ( 8 , 9 ).…”

Environment Constrains Fitness Advantages of Division of Labor in Microbial Consortia Engineered for Metabolite Push or Pull Interactions

“…The ability to control variables within synthetic communities also provides a powerful tool to investigate ecological theories ( 40 ). To this end, synthetic communities have been applied to problems of understanding the benefits of cooperation, the role of division of labor in the simultaneous utilization of different sugars, mechanisms for enhanced conversion of cellulose to biofuels, and the role of quorum sensing in coordinating consortial behavior, among others ( 1 , 2 , 21 , 41 , 42 ).…”

Ecological modelling approaches for predicting emergent properties in microbial communities

“…The threshold is property-specific and may also (non-linearly) depend on environmental factors [ 21 ]. Hence, descriptions of emergent properties have been largely qualitative, although synthetic biology approaches are starting to characterise emergent properties quantitatively [ 14 , 22 ].…”