Emergent simplicity in microbial community assembly

Published in final edited form as: Science. 2018 August 03; 361(6401): 469–474. doi:10.1126/science.aat1168.A major unresolved question in microbiome research is whether the complex taxonomic architectures observed in surveys of natural communities can be explained and predicted by fundamental, quantitative principles. Bridging theory and experiment is hampered by the multiplicity of ecological processes that simultaneously affect community assembly in natural ecosystems. We addressed this challenge by monitoring the assembly of hundreds of soil- and plant-derived microbiomes in well-controlled minimal synthetic media. Both the community-level function and the coarse-grained taxonomy of the resulting communities are highly predictable and governed by nutrient availability, despite substantial species variability. By generalizing classical ecological models to include widespread nonspecific cross-feeding, we show that these features are all emergent properties of the assembly of large microbial communities, explaining their ubiquity in natural microbiomes.The funding for this work partly results from a Scialog Program sponsored jointly by the Research Corporation, for Science Advancement and. the Gordon and Betty Moore Foundation through grants to Yale University and Boston University by the Research Corporation and by the Simons Foundation. This work was also supported by a young; investigator award from the Human Frontier Science Program to A.S. (RGY0077/2016) and by NIH NIGMS grant 1R35GM119461 and a Simons Investigator as in the Mathematical Modeling of Living Systems (MMLS) to P.M.; D.S. and J.E.G. additionally acknowledge funding from the Defense Advanced Research Projects Agency (purchase request no. HR0011515303, contract no.. HR0011-15-0-0091), the U.S. Department of Energy (DE-SC0012627), the NIH (T32GM100842, 5R01DE024468, R01GM121950, and Sub_P30DK036836_P&F), the National Science Foundation (1457695), the Human Frontier Science Program (RGP0020/2016) and the Boston University Interdisciplinary Biomedical Research Office. (Research Corporation, for Science Advancement; Gordon and Betty Moore Foundation; Boston University by the Research Corporation; Simons Foundation.; RGY0077/2016 - uman Frontier Science Program; 1R35GM119461 - NIH NIGMS grant; Simons Investigator as in the Mathematical Modeling of Living Systems (MMLS); HR0011515303 - Defense Advanced Research Projects Agency; HR0011-15-0-0091 - Defense Advanced Research Projects Agency; T32GM100842 - NIH; 5R01DE024468 - NIH; R01GM121950 - NIH; ub_P30DK036836 - NIH; 1457695 - National Science Foundation; RGP0020/2016 - Human Frontier Science Program; Boston University Interdisciplinary Biomedical Research Office)Accepted manuscrip

High-order interactions distort the functional landscape of microbial consortia.

Understanding the link between community composition and function is a major challenge in microbial population biology, with implications for the management of natural microbiomes and the design of synthetic consortia. Specifically, it is poorly understood whether community functions can be quantitatively predicted from traits of species in monoculture. Inspired by the study of complex genetic interactions, we have examined how the amylolytic rate of combinatorial assemblages of six starch-degrading soil bacteria depend on the separate functional contributions from each species and their interactions. Filtering our results through the theory of biochemical kinetics, we show that this simple function is additive in the absence of interactions among community members. For about half of the combinatorially assembled consortia, the amylolytic function is dominated by pairwise and higher-order interactions. For the other half, the function is additive despite the presence of strong competitive interactions. We explain the mechanistic basis of these findings and propose a quantitative framework that allows us to separate the effect of behavioral and population dynamics interactions. Our results suggest that the functional robustness of a consortium to pairwise and higher-order interactions critically affects our ability to predict and bottom-up engineer ecosystem function in complex communities

High-order interactions distort the functional landscape of microbial consortia

© 2019 Sanchez-Gorostiaga et al.Understanding the link between community composition and function is a major challenge in microbial population biology, with implications for the management of natural microbiomes and the design of synthetic consortia. Specifically, it is poorly understood whether community functions can be quantitatively predicted from traits of species in monoculture. Inspired by the study of complex genetic interactions, we have examined how the amylolytic rate of combinatorial assemblages of six starch-degrading soil bacteria depend on the separate functional contributions from each species and their interactions. Filtering our results through the theory of biochemical kinetics, we show that this simple function is additive in the absence of interactions among community members. For about half of the combinatorially assembled consortia, the amylolytic function is dominated by pairwise and higher-order interactions. For the other half, the function is additive despite the presence of strong competitive interactions. We explain the mechanistic basis of these findings and propose a quantitative framework that allows us to separate the effect of behavioral and population dynamics interactions. Our results suggest that the functional robustness of a consortium to pairwise and higher-order interactions critically affects our ability to predict and bottom-up engineer ecosystem function in complex communities.This work was also supported by a young investigator award from the Human Frontier Science Program (RGY0077/2016) and by the National Institutes of Health through grant 1R35 GM133467-01 to AS. In addition, JFP was supported by grant FIS2016-78781-R from the Spanish Ministerio de Economía y Competitividad

Functional attractors in microbial community assembly

For microbiome biology to become a more predictive science, we must identify which descriptive features of microbial communities are reproducible and predictable, which are not, and why. We address this question by experimentally studying parallelism and convergence in microbial community assembly in replicate glucose-limited habitats. Here, we show that the previously observed family-level convergence in these habitats reflects a reproducible metabolic organization, where the ratio of the dominant metabolic groups can be explained from a simple resource-partitioning model. In turn, taxonomic divergence among replicate communities arises from multistability in population dynamics. Multistability can also lead to alternative functional states in closed ecosystems but not in metacommunities. Our findings empirically illustrate how the evolutionary conservation of quantitative metabolic traits, multistability, and the inherent stochasticity of population dynamics, may all conspire to generate the patterns of reproducibility and variability at different levels of organization that are commonplace in microbial community assembly

A randomized trial of planned cesarean or vaginal delivery for twin pregnancy

Background: Twin birth is associated with a higher risk of adverse perinatal outcomes than singleton birth. It is unclear whether planned cesarean section results in a lower risk of adverse outcomes than planned vaginal delivery in twin pregnancy.\ud \ud Methods: We randomly assigned women between 32 weeks 0 days and 38 weeks 6 days of gestation with twin pregnancy and with the first twin in the cephalic presentation to planned cesarean section or planned vaginal delivery with cesarean only if indicated. Elective delivery was planned between 37 weeks 5 days and 38 weeks 6 days of gestation. The primary outcome was a composite of fetal or neonatal death or serious neonatal morbidity, with the fetus or infant as the unit of analysis for the statistical comparison.\ud \ud Results: A total of 1398 women (2795 fetuses) were randomly assigned to planned cesarean delivery and 1406 women (2812 fetuses) to planned vaginal delivery. The rate of cesarean delivery was 90.7% in the planned-cesarean-delivery group and 43.8% in the planned-vaginal-delivery group. Women in the planned-cesarean-delivery group delivered earlier than did those in the planned-vaginal-delivery group (mean number of days from randomization to delivery, 12.4 vs. 13.3; P = 0.04). There was no significant difference in the composite primary outcome between the planned-cesarean-delivery group and the planned-vaginal-delivery group (2.2% and 1.9%, respectively; odds ratio with planned cesarean delivery, 1.16; 95% confidence interval, 0.77 to 1.74; P = 0.49).\ud \ud Conclusion: In twin pregnancy between 32 weeks 0 days and 38 weeks 6 days of gestation, with the first twin in the cephalic presentation, planned cesarean delivery did not significantly decrease or increase the risk of fetal or neonatal death or serious neonatal morbidity, as compared with planned vaginal delivery