Synthetic Ecosystems: From the Test Tube to the Biosphere

Abstract

The study of ecosystems, both natural and artificial, has historically been mediated by population dynamics theories. In this framework, quantifying population numbers and related variables (associated with metabolism or biological-environmental interactions) plays a central role in measuring and predicting system-level properties. As we move toward advanced technological engineering of cells and organisms, the possibility of bioengineering ecosystems (from the gut microbiome to wildlands) opens several questions that will require quantitative models to find answers. Here, we present a comprehensive survey of quantitative modeling approaches for managing three kinds of synthetic ecosystems, sharing the presence of engineered strains. These include test tube examples of ecosystems hosting a relatively low number of interacting species, mesoscale closed ecosystems (or ecospheres), and macro-scale, engineered ecosystems. The potential outcomes of synthetic ecosystem designs and their limits will be relevant to different disciplines, including biomedical engineering, astrobiology, space exploration and fighting climate change impacts on endangered ecosystems. We propose a space of possible ecosystems that captures this broad range of scenarios and a tentative roadmap for open problems and further exploration.

Keywords: Ecological Engineering; Synthetic Biology; climate change; ecospheres; life support systems.

Figure 1

Microcosms, novel, and synthetic ecosystems. Simplified communities have been studied within the context of (a) micro- and (b) mesocosm experiments, while a large-scale scenario is provided by Biosphere 2 (c), including different habitats. New kinds of human-related ecosystems have also been obtained by assembling many exotic species, as is the case of Ascension Island (d), or have emerged within an Anthropogenic waste, such as plastic (e), providing a new habitat to the so-called Plastisphere. Space missions (f) present extra challenges associated with closed environments. Synthetic biology not only offers ways to both interrogate nature, as it occurs with competition (g) and cooperation (h) in the Petri dish, but also as ways to modify extant communities, such as (i) the skin microbiome.

Figure 2

Minimal synthetic ecological networks. Here, we display six types of distinct SE and their characterization using quantitative analyses, qualitative stability properties, and candidate mathematical models. In each case, the nature of the species–species interactions is indicated. At the same time, quantification of their underlying behavior is illustrated by both time series (for the three first examples) and statistical, stationary measures for the last two. Beyond the specific quantitative results, each motif displays some class of generic behavior that can be described in terms of attractor states. Here, we display, on a (c₁, c₂) space, the trajectories exhibited by the system, which connect stable (filled circles) and unstable (open circles) states. In some systems, alternative states are present, while in others there is a single, global attractor and in some they follow a periodic orbit. These attractors are often represented as marbles on a landscape. Here, stable and unstable states (darker and lighter spheres, respectively) correspond to the bottom of valleys and peaks. Simple mathematical models (right column) provide a mechanistic explanation of how nonlinear interactions generate different kinds of attractor states.

Figure 3

Systems and synthetic biology for life support systems. In (a), the BIOS-3 design of a closed ecosphere is represented here as a graph (including the closed cycling of O₂ and CO₂, along with higher plants and humans). This coarse-graining allows defining a set of equations (b) that describe the system. Here O = [O₂], C = [CO₂], and P_k indicate plant abundance; V_o is the rate of human metabolism; ν_1|2 stands for plant maximum growth rate; γ and δ rate of plant growth; μ is rate of human metabolism related to oxygen consumption; R_1|2 is the assimilation quotients for plants; R stands for human respiratory quotient and q the fraction of human metabolism supported by plants. Synthetic biology could enhance and stabilize this design, achieving a fully closed system and recycling plant and human waste as food and fertilizer are produced (c). Here, an extra compartment is added. The tag “Synthetic Biology” stands for the necessary closure of metabolic pathways, here to be conducted in bioreactor tanks. The corresponding mathematical model (d) is obtained from (b) by adding S_i, where i = 1, ..., N, where N is the number of species performing biochemical reactions. Here we could propose a closed catalytic architecture, i.e., hypercycle dynamics governing S_i. Here δ_1iα and δ_2iα stand for Dirac’s delta function to tag who is producing or recycling from or to plant and human compartment, respectively; i.e., δ_iα = 1 when i = α and zero otherwise. The catalytically assisted replication species j provides to i is denoted by ξ_ij. Recycling and production rates are ω_i, σ_i and π_i, ρ_i, respectively. The last term, Φ(S), is the dilution outflow.

Figure 4

Synthetic ecosystems for dryland restoration and conservation. A visual summary of the three levels of analysis. From bottom to top: (1) competitive strains in liquid media, theoretically described by standard ode models, with a ”test tube” implementation; (2) micro/mesocosms implementation of engineered cooperators and the soil crust, where models are now extended to include environmental feedbacks; and (3) large-scale systems can be approached using formal models involving a network-level description. As we move from one level to another, new, emergent properties must be considered.

Figure 5

Synthetic ecosystems in context. A space is defined using three axes, namely, the degree of community development, species (strain) diversity, and the amount of human intervention. Each sphere represents a given system and locations are just relative to each other, and the three scales considered in this paper appear as three nested cubes (C₁ ⊂ C₂ ⊂ C₃). Novel and synthetic domains are indicated by the gray and yellow areas, respectively. Anthropogenic actions create conditions for the emergence of so-called novel ecosystems. Beyond, synthetic ecosystems span out of design effort. On the left, we have the test tube scale designs that involve standard motifs, small-scale microbiomes living in man-made artifacts, mesocosm experiments and life support systems. These two scales are shown within the larger cube C₁ (right) that contains undisturbed and designed (terraformed) ecosystems as two corners on the right upper part. Gray spheres stand for human-driven ecosystems and blue marbles indicate scenarios of ecosystem intervention.