Harnessing ecological and evolutionary principles to guide the design of microbial production consortia

Giri, Samir; Shitut, Shraddha; Kost, Christian

doi:10.1016/j.copbio.2019.12.012

Cited by 37 publications

(26 citation statements)

References 93 publications

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“…A mutualistic relationship is thus necessarily established between leaker and consumer cells. Mutualistic cell-cell interaction usually leads to stable coexistence, as discussed in previous studies (Tokita and Yasutomi, 2003;Pande et al, 2014;Giri et al, 2020). In contrast, leakage of the metabolites by random xed di usion coe cients does not necessarily bene t leaker cells, thereby making leaker-consumer interactions often parasitic or even competitive (see Fig.…”

Section: Decrease In Species Diversity In the Absence Of Cell-level Amentioning

confidence: 72%

“…In contrast, if only few cell species leak a few chemicals, the ecosystem would have a unidirectional structure similar to a “food chain.” In such cases, keystone/core species could exist, and the system would not be resilient to removal of such species. Empirical studies suggest that diverse microbial communities are more resistant to environmental disturbances than monocultures ( Giri et al, 2020 ). Experimentally estimating S Cell or S Chem in these microbial communities and investigating their relationship with their resilience could be interesting.…”

Section: Discussionmentioning

confidence: 99%

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Microbial Potlatch: Cell-level adaptation of leakiness of metabolites leads to resilient symbiosis among diverse cells

Yamagishi

Saito

Kaneko

2020

Preprint

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Microbial communities display extreme diversity, facilitated by the secretion of chemicals that can create new niches. However, it is unclear why cells often secrete even essential metabolites after evolution. By noting that cells can enhance their own growth rate by leakage of essential metabolites, we show that such leaker cells can benefit from coexistence with cells that consume the leaked chemicals in the environment. This leads to an unusual form of mutualism between "leaker" and "consumer" cells, resulting in frequency-dependent coexistence of multiple microbial species, as supported by extensive simulations. Remarkably, such symbiotic relationships generally evolve when each species adapts its leakiness to optimize its own growth rate under crowded conditions and nutrient limitations, leading to ecosystems with diverse species exchanging many metabolites with each other. In addition, such ecosystems are resilient against structural and environmental perturbations. Thus, we present a new basis for diverse, complex microbial ecosystems.

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Section: Decrease In Species Diversity In the Absence Of Cell-level Amentioning

confidence: 72%

Section: Discussionmentioning

confidence: 99%

Microbial Potlatch: Cell-level adaptation of leakiness of metabolites leads to resilient symbiosis among diverse cells

Yamagishi

Saito

Kaneko

2020

Preprint

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“…However, the rules that determine the assembly, function, and evolution of these microbial communities remain poorly understood. Understanding the underlying governing principles is central to microbial ecology and crucial for designing microbial consortia for biotechnological [13] or medical applications [14, 15].…”

Section: Introductionmentioning

confidence: 99%

Metabolic dissimilarity determines the establishment of cross-feeding interactions in bacteria

Giri

Oña

Waschina

et al. 2020

Preprint

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The exchange of metabolites among different bacterial genotypes is key for determining the structure and function of microbial communities. However, the factors that govern the establishment of these cross-feeding interactions remain poorly understood. While kin selection theory predicts that individuals should direct benefits preferentially to close relatives, the potential benefits resulting from a metabolic exchange may be larger for more distantly related species. Here we distinguish between these two possibilities by performing pairwise cocultivation experiments between auxotrophic recipients and 25 species of potential amino acid donors. Auxotrophic recipients were able to grow in the vast majority of pairs tested (78%), suggesting that metabolic cross-feeding interactions are readily established. Strikingly, both the phylogenetic distance between donor and recipient as well as the dissimilarity of their metabolic networks was positively associated with the growth of auxotrophic recipients. Finally, this result was corroborated in an in-silico analysis of a co-growth of species from a gut microbial community. Together, these findings suggest metabolic cross-feeding interactions are more likely to establish between strains that are metabolically more dissimilar. Thus, our work identifies a new rule of microbial community assembly, which can help predict, understand, and manipulate natural and synthetic microbial systems.SignificanceMetabolic cross-feeding is critical for determining the structure and function of natural microbial communities. However, the rules that determine the establishment of these interactions remain poorly understood. Here we systematically analyze the propensity of different bacterial species to engage in unidirectional cross-feeding interactions. Our results reveal that synergistic growth was prevalent in the vast majority of cases analyzed. Moreover, both phylogenetic and metabolic dissimilarity between donors and recipients favored a successful establishment of metabolite exchange interactions. This work identifies a new rule of microbial community assembly that can help predict, understand, and manipulate microbial communities for diverse applications.

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“…Natural microbial consortia exemplify how multi-organismic communities achieve robustness to environmental fluctuations by augmenting metabolic capacity through division of labor, and have inspired recent research to rationally design synthetic microbial consortia [27]. Similarly, synthetic consortia can be engineered to distribute the cost of heterologous expression of metabolic pathways, compartmentalize competing cross-inhibiting yet complementary pathways, and expand their metabolic capabilities compared to monocultures [28].…”

Section: Synthetic Population Controlmentioning

confidence: 99%

Autonomous and Assisted Control for Synthetic Microbiology

Banderas

Bec

Cordier

et al. 2020

IJMS

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The control of microbes and microbial consortia to achieve specific functions requires synthetic circuits that can reliably cope with internal and external perturbations. Circuits that naturally evolved to regulate biological functions are frequently robust to alterations in their parameters. As the complexity of synthetic circuits increases, synthetic biologists need to implement such robust control “by design”. This is especially true for intercellular signaling circuits for synthetic consortia, where robustness is highly desirable, but its mechanisms remain unclear. Cybergenetics, the interface between synthetic biology and control theory, offers two approaches to this challenge: external (computer-aided) and internal (autonomous) control. Here, we review natural and synthetic microbial systems with robustness, and outline experimental approaches to implement such robust control in microbial consortia through population-level cybergenetics. We propose that harnessing natural intercellular circuit topologies with robust evolved functions can help to achieve similar robust control in synthetic intercellular circuits. A “hybrid biology” approach, where robust synthetic microbes interact with natural consortia and—additionally—with external computers, could become a useful tool for health and environmental applications.

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Harnessing ecological and evolutionary principles to guide the design of microbial production consortia

Cited by 37 publications

References 93 publications

Microbial Potlatch: Cell-level adaptation of leakiness of metabolites leads to resilient symbiosis among diverse cells

Microbial Potlatch: Cell-level adaptation of leakiness of metabolites leads to resilient symbiosis among diverse cells

Metabolic dissimilarity determines the establishment of cross-feeding interactions in bacteria

Autonomous and Assisted Control for Synthetic Microbiology

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