Defining Higher-Order Interactions in Synthetic Ecology: Lessons from Physics and Quantitative Genetics

Sánchez, Álvaro

doi:10.1016/j.cels.2019.11.009

Cited by 41 publications

(36 citation statements)

References 12 publications

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“…This definition of an interaction as a deviation from a null model that assumes independent effects is commonplace in systems-level biology [12] .…”

Section: Resultsmentioning

confidence: 99%

Nutrient dominance governs the assembly of microbial communities in mixed nutrient environments

Estrela

Sánchez-Gorostiaga

Vila

et al. 2020

Preprint

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A major open question in microbiome research is whether we can predict how the components of a diet collectively determine the taxonomic composition of microbial communities. Motivated by this challenge, here we ask whether communities assembled in a mixed nutrient environment can be predicted from those assembled in every single nutrient in isolation. To that end, we first formulate a quantitative null model of community assembly in a mixture of nutrients that recruit species independently. We then test the model predictions by assembling replicate communities in synthetic environments that contain either a pair of nutrients, or each nutrient in isolation. We find that the null, naturally additive model generally predicts well the family-level community composition. However, we also identify systematic deviations from the additive predictions that reflect generic patterns of nutrient dominance at the family-level of taxonomy. Pairs of more-similar nutrients (e.g. two sugars) are on average more additive than pairs of more dissimilar nutrients (e.g. one sugar and one organic acid). A simple dominance rule emerges, where we find that sugars generally dominate organic acids. This simple dominance rule extends to most families and most sugar-organic acid pairs in our experiment. Our results suggest that regularities in the ways nutrients interact may help us predict how microbial communities respond to changes in nutrient composition.

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“…This definition of an interaction as a deviation from a null model that assumes independent effects is commonplace in systems-level biology [12] .…”

Section: Resultsmentioning

confidence: 99%

Nutrient dominance governs the assembly of microbial communities in mixed nutrient environments

Estrela

Sánchez-Gorostiaga

Vila

et al. 2020

Preprint

Self Cite

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“…Interestingly, the main driver of taxonomic variability among replicates was the dominant member of the respirator group (a sub-dominant species). Amelioration of competition between two fermenter strains in the presence of one (but not the other) dominant respirator points to the subtle role that high-order interactions may play in community assembly (Billick and Case 1994;Mickalide and Kuehn 2019;Sanchez 2019;Sanchez-Gorostiaga et al 2019;Senay et al 2019;Levine et al 2017;Grilli et al 2017) . This is also in line with previous observations of the potential importance of sub-dominant bacteria in shaping the composition of microbial communities ) .…”

Section: Discussionmentioning

confidence: 99%

Metabolic rules of microbial community assembly

Estrela

Vila

et al. 2020

Preprint

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To develop a quantitative theory that can predict how microbiomes assemble, and how they respond to perturbations, we must identify which descriptive features of microbial communities are reproducible and predictable, which are unpredictable, and why. The emergent metagenomic structure of communities is often quantitatively convergent in similar habitats, with highly similar fractions of the metagenome being devoted to the same metabolic pathways. By contrast, the species-level taxonomic composition is often highly variable even in replicate environments. The mechanisms behind these patterns are not yet understood. By studying the self-assembly of hundreds of communities in replicate, synthetic habitats, we show that the reproducibility of microbial community assembly reflects an emergent metabolic structure, which is quantitatively predictable from first-principles, genome-scale metabolic models. Taxonomic variability within functional groups arises through multistability in population dynamics, and the species-level community composition is predictably governed by the mutual competitive exclusion of two sub-dominant strains. Our findings provide a mechanistic bridge between microbial community structure at different levels of organization, and show that the evolutionary conservation of metabolic traits, both in terms of growth responses and niches constructed, can be leveraged to quantitatively predict the taxonomic and metabolic structure of microbial communities.

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“…An issue whose importance has been realized for decades is the extent to which interspecies interactions are pairwise additive or whether higher-order (often called indirect) interactions are necessary to explain community structure ( 41 , 42 ). The term “higher-order interactions” has been defined in various ways in the ecological literature ( 42 , 43 ), in some cases referring specifically to nonadditive changes in a species’ growth rate given the presence of additional species, or to changes in the nature of the interaction between two species induced by additional species. In other cases it refers more generally to any interaction that cannot be captured by a pairwise model.…”

Section: Introductionmentioning

confidence: 99%

Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome

Sundarraman

Hay

et al. 2020

mBio

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The microbial communities resident in animal intestines are composed of multiple species that together play important roles in host development, health, and disease. Due to the complexity of these communities and the difficulty of characterizing them in situ, the determinants of microbial composition remain largely unknown. Further, it is unclear for many multispecies consortia whether their species-level makeup can be predicted based on an understanding of pairwise species interactions or whether higher-order interactions are needed to explain emergent compositions. To address this, we examine commensal intestinal microbes in larval zebrafish, initially raised germfree, to allow the introduction of controlled combinations of bacterial species. Using a dissection and plating assay, we demonstrate the construction of communities of one to five bacterial species and show that the outcomes from the two-species competitions fail to predict species abundances in more complex communities. With multiple species present, interbacterial interactions become weaker, suggesting that higher-order interactions in the vertebrate gut stabilize complex communities. IMPORTANCE Understanding the rules governing the composition of the diverse microbial communities that reside in the vertebrate gut environment will enhance our ability to manipulate such communities for therapeutic ends. Synthetic microbial communities, assembled from specific combinations of microbial species in germfree animals, allow investigation of the fundamental question of whether multispecies community composition can be predicted solely based on the combined effects of interactions between pairs of species. If so, such predictability would enable the construction of communities with desired species from the bottom up. If not, the apparent higher-order interactions imply that emergent community-level characteristics are crucial. Our findings using up to five coexisting native bacterial species in larval zebrafish, a model vertebrate, provide experimental evidence for higher-order interactions and, moreover, show that these interactions promote the coexistence of microbial species in the gut.

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Defining Higher-Order Interactions in Synthetic Ecology: Lessons from Physics and Quantitative Genetics

Abstract: A new paper from Mickalide and Kuehn studies a well-controlled microbial trophic chain and identifies a highorder interaction between its species.

Cited by 41 publications

References 12 publications

Nutrient dominance governs the assembly of microbial communities in mixed nutrient environments

Nutrient dominance governs the assembly of microbial communities in mixed nutrient environments

Metabolic rules of microbial community assembly

Higher-Order Interactions Dampen Pairwise Competition in the Zebrafish Gut Microbiome

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