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      Social dynamics modeling of chrono-nutrition

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          Abstract

          Gut microbiota and human relationships are strictly connected to each other. What we eat reflects our body-mind connection and synchronizes with people around us. However, how this impacts on gut microbiota and, conversely, how gut bacteria influence our dietary behaviors has not been explored yet. To quantify the complex dynamics of this interplay between gut and human behaviors we explore the “gut-human behavior axis” and its evolutionary dynamics in a real-world scenario represented by the social multiplex network. We consider a dual type of similarity, homophily and gut similarity, other than psychological and unconscious biases. We analyze the dynamics of social and gut microbial communities, quantifying the impact of human behaviors on diets and gut microbial composition and, backwards, through a control mechanism. Meal timing mechanisms and “chrono-nutrition” play a crucial role in feeding behaviors, along with the quality and quantity of food intake. Considering a population of shift workers, we explore the dynamic interplay between their eating behaviors and gut microbiota, modeling the social dynamics of chrono-nutrition in a multiplex network. Our findings allow us to quantify the relation between human behaviors and gut microbiota through the methodological introduction of gut metabolic modeling and statistical estimators, able to capture their dynamic interplay. Moreover, we find that the timing of gut microbial communities is slower than social interactions and shift-working, and the impact of shift-working on the dynamics of chrono-nutrition is a fluctuation of strategies with a major propensity for defection (e.g. high-fat meals). A deeper understanding of the relation between gut microbiota and the dietary behavioral patterns, by embedding also the related social aspects, allows improving the overall knowledge about metabolic models and their implications for human health, opening the possibility to design promising social therapeutic dietary interventions.

          Author summary

          Human gut microbiota is able to influence different aspects of physiology, such as human behaviors. Our close social connections, in turn, impact on eating behaviors and diets, which play a key role in driving the gut microbial composition and its metabolic processes. To quantify the dynamic interplay between gut microbiota and human behaviors in a social multiplex network, we investigate the “gut-human behavior axis”. We propose statistical estimators able to quantify the relation between human behaviors and gut microbiota in a social multiplex network. Furthermore, considering a population of shift workers, we explore the dynamic interplay between their eating behaviors and their gut microbiota, quantifying the social dynamics of chrono-nutrition in a multiplex network. Our findings, coherently with what one can expect in the case of shift-working, demonstrate how the timing of gut microbial communities is slower than social interactions and shift-working. Thus, the impact of shift-working on chrono-nutrition is a fluctuation of behaviors, with a major propensity for poor food choices or high-fat meals. Acquiring a deeper knowledge about the metabolic models of gut microbiota and quantifying the complex interplay of social and gut microbial communities pave the way to targeted social therapeutic interventions.

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          Most cited references51

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          Emergence of scaling in random networks

          Systems as diverse as genetic networks or the World Wide Web are best described as networks with complex topology. A common property of many large networks is that the vertex connectivities follow a scale-free power-law distribution. This feature was found to be a consequence of two generic mechanisms: (i) networks expand continuously by the addition of new vertices, and (ii) new vertices attach preferentially to sites that are already well connected. A model based on these two ingredients reproduces the observed stationary scale-free distributions, which indicates that the development of large networks is governed by robust self-organizing phenomena that go beyond the particulars of the individual systems.
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            Spatial structure often inhibits the evolution of cooperation in the snowdrift game.

            Understanding the emergence of cooperation is a fundamental problem in evolutionary biology. Evolutionary game theory has become a powerful framework with which to investigate this problem. Two simple games have attracted most attention in theoretical and experimental studies: the Prisoner's Dilemma and the snowdrift game (also known as the hawk-dove or chicken game). In the Prisoner's Dilemma, the non-cooperative state is evolutionarily stable, which has inspired numerous investigations of suitable extensions that enable cooperative behaviour to persist. In particular, on the basis of spatial extensions of the Prisoner's Dilemma, it is widely accepted that spatial structure promotes the evolution of cooperation. Here we show that no such general predictions can be made for the effects of spatial structure in the snowdrift game. In unstructured snowdrift games, intermediate levels of cooperation persist. Unexpectedly, spatial structure reduces the proportion of cooperators for a wide range of parameters. In particular, spatial structure eliminates cooperation if the cost-to-benefit ratio of cooperation is high. Our results caution against the common belief that spatial structure is necessarily beneficial for cooperative behaviour.
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              Recon3D: A Resource Enabling A Three-Dimensional View of Gene Variation in Human Metabolism

              Genome-scale network reconstructions have helped uncover the molecular basis of metabolism. Here we present Recon3D, a computational resource that includes three-dimensional (3D) metabolite and protein structure data and enables integrated analyses of metabolic functions in humans. We use Recon3D to functionally characterize mutations associated with disease, and identify metabolic response signatures that are caused by exposure to certain drugs. Recon3D represents the most comprehensive human metabolic network model to date, accounting for 3,288 open reading frames (representing 17% of functionally annotated human genes), 13,543 metabolic reactions involving 4,140 unique metabolites, and 12,890 protein structures. These data provide a unique resource for investigating molecular mechanisms of human metabolism. Recon3D is available at http://vmh.life.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, CA USA )
                1553-734X
                1553-7358
                January 2019
                30 January 2019
                : 15
                : 1
                : e1006714
                Affiliations
                [1 ] Dipartimento di Ingegneria Elettrica, Elettronica e Informatica (DIEEI), CNIT (National Inter-University Consortium for Telecommunications) Catania, Italy
                [2 ] Department of Computer Science and Information Systems, Teesside University, Middlesbrough, United Kingdom
                [3 ] Computer Laboratory, University of Cambridge, Cambridge, United Kingdom
                National Cancer Institute, United States of America and Tel Aviv University, Israel, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-4905-3309
                http://orcid.org/0000-0002-4785-0067
                http://orcid.org/0000-0001-6357-0439
                http://orcid.org/0000-0002-3140-7909
                http://orcid.org/0000-0003-0370-7717
                http://orcid.org/0000-0002-0540-5053
                Article
                PCOMPBIOL-D-17-02022
                10.1371/journal.pcbi.1006714
                6370249
                30699206
                c544d4d2-d8fd-4f57-b4b5-58644a21feaa
                © 2019 Di Stefano et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 December 2017
                : 14 December 2018
                Page count
                Figures: 4, Tables: 3, Pages: 25
                Funding
                This work was partially supported by the Research Grants: Italian Ministry of University and Research (MIUR) - PON REC 2007 - 2013 - PON-03PE-00132-1 “Servify” and Italian Ministry of Economic Development (MISE) - PON 2014-2020 FESR - F/050270/01-03/X32 “SUMMIT”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Bacteria
                Gut Bacteria
                Biology and Life Sciences
                Psychology
                Behavior
                Social Sciences
                Psychology
                Behavior
                Biology and Life Sciences
                Nutrition
                Diet
                Medicine and Health Sciences
                Nutrition
                Diet
                Computer and Information Sciences
                Network Analysis
                Multiplex Networks
                Biology and Life Sciences
                Microbiology
                Microbial Evolution
                Biology and Life Sciences
                Evolutionary Biology
                Organismal Evolution
                Microbial Evolution
                Biology and Life Sciences
                Psychology
                Behavior
                Habits
                Eating Habits
                Social Sciences
                Psychology
                Behavior
                Habits
                Eating Habits
                Computer and Information Sciences
                Network Analysis
                Metabolic Networks
                Biology and Life Sciences
                Psychology
                Emotions
                Happiness
                Social Sciences
                Psychology
                Emotions
                Happiness
                Custom metadata
                vor-update-to-uncorrected-proof
                2019-02-11
                All relevant data are within the paper and its Supporting Information files.

                Quantitative & Systems biology
                Quantitative & Systems biology

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