PerspectiveEcology

Ecological communities by design

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Science  26 Jun 2015:
Vol. 348, Issue 6242, pp. 1425-1427
DOI: 10.1126/science.aab0946
Learning from nature.

Photomicrograph of cyanobacterial-heterotroph microbial consortia derived from a phototrophic microbial mat community from a saline lake. Emerging understanding of cooperative mechanisms in such communities may be helpful in the design of synthetic communities for use in biotechnology.

PHOTO: ALICE DOHNALKOVA/PNNL

In synthetic ecology, a nascent offshoot of synthetic biology, scientists aim to design and construct microbial communities with desirable properties. Such mixed populations of microorganisms can simultaneously perform otherwise incompatible functions (1). Compared with individual organisms, they can also better resist losses in function as a result of environmental perturbation or invasion by other species (2). Synthetic ecology may thus be a promising approach for developing robust, stable biotechnological processes, such as the conversion of cellulosic biomass to biofuels (3). However, achieving this will require detailed knowledge of the principles that guide the structure and function of microbial communities (see the image).

Recent work with synthetic communities is shedding light on microbial interactions that may lead to new principles for community design and engineering. In game theory, cooperators provide publicly available goods that benefit all, whereas cheaters exploit those goods without reciprocation. The tragedy of the commons predicts that cheaters are more fit than cooperators, eventually destroying the cooperation. Yet, this is not borne out by observations. For example, using a synthetic consortium of genetically modified yeast to represent cooperators and cheaters, Waite and Shou (4) found that, although initially less fit than cheaters, cooperators rapidly dominated in a fraction of the cultures. The evolved cooperators harbored mutations allowing them to grow at much lower nutrient concentrations than their ancestor. This suggests that the tragedy of the commons can be avoided if, during adaptation, the fitness gain of cooperators exceeds that of the cheaters by at least the cost of cooperation (see the figure).

The work by Asfahl et al. provides another example of deferring the tragedy of the commons via nonsocial adaptation (5). The opportunistic pathogen Pseudomonas aeruginosa uses diffusible signaling molecules, in a process known as quorum sensing (QS), to regulate public goods—resources that can benefit the entire community. Under growth conditions that require QS-regulated public goods, mutations in the transcriptional regulator psdR give rise to a nonsocial adaptation. This mutation has no effect on public goods expression; rather, it increases the fitness of individuals harboring the mutation by improving intracellular metabolism of the goods. Although the adapted population is still subject to invasion by cheaters, the mutation affords a higher fitness (growth rate) that increases the population's tolerance of cheaters, thus maintaining cooperative behavior. This suggests that fitness adaptations are a fundamental mechanism by which cooperative communities can be maintained under the persistent threat of cheaters.

Adaptive race.

In cooperative communities, cheaters use common goods without paying the cost to produce them. In the absence of adaptation or adaptive mutations, the cheaters eventually win out but cause the system to collapse. In synthetic communities of cooperators that excrete lysine and cheaters that require lysine, both species adapt to cope with limited resources. In the example shown, a mutation in a cooperator allows the mutated strain to outcompete its ancestors over time. This mechanism explains why cooperating microbial communities can persist in changing environments. For further details, see ( 4).

Microbial communities also cooperate through metabolic cross-feeding or syntrophy, where one organism synthesizes a compound that another organism requires but cannot produce. For example, amino acids and sugar exchange are common mutualistic interactions in co-occurring subcommunities from different habitats (6). In a recent study, Mee et al. (7) explored the basic principles of syntrophic exchange in synthetic communities consisting of Escherichia coli mutants auxotrophic for different amino acids. They found that stronger cooperative interactions were promoted between cells exchanging metabolically expensive amino acids compared to those that are cheaper to synthesize. Hence, amino acid auxotrophy may be a common strategy by which microbial communities lessen the collective metabolic burden of biosynthesis and stabilize cooperation. Further evidence for this comes from the persistence of metabolic cooperation between different E. coli amino acid auxotrophs in adaptively evolved cocultures (8).

Inherent to community productivity is the question of what maintains crossfeeding in the presence of metabolically independent noncooperators. Pande et al. (9) addressed this question with synthetic communities of E. coli that had been genetically modified to require uptake of certain amino acids for growth and to release other amino acids into the environment. Most cross-feeding consortia grew more rapidly than the parental bacterium that could synthesize all the amino acids needed for growth; this was the case even when the consortia were cultivated with the parent and therefore in direct competition for nutrients. The authors attributed the greater fitness of the cooperating consortia to a metabolic division of labor. Here, the added costs of producing an excess of one or more amino acids to benefit the community were more than compensated for by the reduced costs incurred by not having to synthesize all amino acids de novo. The loss of specific biosynthetic functions can give rise to stable metabolic interactions that benefit the interacting organisms. This likely explains why amino acid exchange is common among members of microbial communities throughout the biosphere (7).

In some cases, the interactions between community members that give rise to higher-order properties emerge only when distinct physical structures are formed. A coculture of P. aeruginosa, Pseudomonas protegens, and Klebsiella pneumoniae forms a mixed-species biofilm that collectively exhibits greater resistance to antimicrobials (tobramycin and sodium dodecyl sulfate) than do biofilms of the individual species (10). Furthermore, when the mixed culture is grown planktonically and treated with tobramycim, only the more resistant P. protegens survive. The results indicate that species composition and spatial organization can affect higher-order properties such as stress resistance. It remains unclear how the spatial organization of different species in mixed biofilms helps to make them resilient.

Model systems derived from natural communities have tremendous untapped potential to uncover the genetic, biochemical, and evolutionary bases for ecological interactions at play in more complex systems (11). Microbial oxygenic phototrophs are ubiquitous worldwide and host diverse microbes that can influence the physiology and ecology of the host. Sison-Mangus et al. (12) investigated how coadaptation affects the interactions between Pseudo-nitzschia, a genus of marine diatoms, and the bacteria associated with them. They discovered that individual species of the diatom harbor phylogenetically distinct bacterial communities and that the communities associated with species that produce the toxin domoic acid are less diverse. Transplant experiments to assess coevolution effects on host fitness revealed that bacteria conferred stronger fitness to their natural host than to non-native diatoms. That some organisms may select for specific microbes they host, possibly through metabolite secretion, suggests this may be an effective approach for designing synthetic communities.

Colonization resistance, defined as the capacity for the native community to resist invasion, is thought to be a major function of the microbiome. To explore mechanisms of colonization resistance, He et al. (13) investigated a community cultivated from mouse oral cavity that could detect the presence of E. coli and enhance its lethality toward the invader by elevating H2O2 production (14). Using information from the simplified oral microbiome, the authors constructed a synthetic consortia consisting of three mice oral bacterial species from previous studies and used it to investigate colonization resistance mechanisms. Their results revealed the roles of the three species: Streptococcus saprophyticus functions as a sensor by detecting E. coli lipopolysaccharide, whereas Streptococcus infantis serves as a mediator that detects a diffusible signal from the sensor and relays information to the killer (Staphylococcus sanguinus), which turns on H2O2 production. These mechanistic details of interactions provide insight into how microbiomes might be designed and engineered to resist invasion.

Substantial challenges remain before synthetic ecology can be successfully applied to biotechnologies such as consolidated bioprocessing of lignocellulosic biomass for biofuel production. For example, it remains to be shown how interactions among community members drive assembly and structure and how these interactions give rise to higher-order properties. To gain a better understanding of these processes, scientists must identify and quantify the numerous biomolecules produced and secreted by microbes in communities and link the exchanges of these molecules to specific organisms and the genes involved in production and consumption.

References and Notes

  1. Acknowledgments: This work was supported by the U.S. Department of Energy, Office of Biological and Environmental Research (BER), as part of BER's Genomic Science Program (GSP). This contribution originates from the GSP Foundational Scientific Focus Area at the PNNL. Image courtesy of A. Dohnalkova, PNNL.

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