Dataset Information

Topological distortion and reorganized modular structure of gut microbial co-occurrence networks in inflammatory bowel disease.

ABSTRACT: The gut microbiome plays a key role in human health, and alterations of the normal gut flora are associated with a variety of distinct disease states. Yet, the natural dependencies between microbes in healthy and diseased individuals remain far from understood. Here we use a network-based approach to characterize microbial co-occurrence in individuals with inflammatory bowel disease (IBD) and healthy (non-IBD control) individuals. We find that microbial networks in patients with IBD differ in both global structure and local connectivity patterns. While a "core" microbiome is preserved, network topology of other densely interconnected microbe modules is distorted, with potent inflammation-mediating organisms assuming roles as integrative and highly connected inter-modular hubs. We show that while both networks display a rich-club organization, in which a small set of microbes commonly co-occur, the healthy network is more easily disrupted by elimination of a small number of key species. Further investigation of network alterations in disease might offer mechanistic insights into the specific pathogens responsible for microbiome-mediated inflammation in IBD.

SUBMITTER: Baldassano SN

PROVIDER: S-EPMC4870640 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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Topological distortion and reorganized modular structure of gut microbial co-occurrence networks in inflammatory bowel disease.

Baldassano Steven N SN Bassett Danielle S DS

Scientific reports 20160518

The gut microbiome plays a key role in human health, and alterations of the normal gut flora are associated with a variety of distinct disease states. Yet, the natural dependencies between microbes in healthy and diseased individuals remain far from understood. Here we use a network-based approach to characterize microbial co-occurrence in individuals with inflammatory bowel disease (IBD) and healthy (non-IBD control) individuals. We find that microbial networks in patients with IBD differ in bo ...[more]

PMID: 27188829

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Project description:BackgroundThe extent to which deterministic rather than stochastic processes guide gut bacteria co-existence and ultimately their assembling into a community remains largely unknown. Co-occurrence networks of bacterial associations offer a powerful approach to begin exploring gut microbial community structure, maintenance and dynamics, beyond compositional aspects alone. Here we used an iconic model system, the cichlid fishes, with their multiple lake assemblages and extraordinary ecological diversity, to investigate a) patterns of microbial associations that were robust to major phylogeographical variables, and b) changes in microbial network structure along dietary shifts. We tackled these objectives using the large gut microbiota sequencing dataset available (nine lakes from Africa and America), building geographical and diet-specific networks and performing comparative network analyses.ResultsMajor findings indicated that lake and continental microbial networks were highly resembling in global topology and node taxonomic composition, despite the heterogeneity of the samples. A small fraction of the observed co-occurrences among operational taxonomic units (OTUs) was conserved across all lake assemblages. These were all positive associations and involved OTUs within the genera Cetobacterium and Turicibacter and several OTUs belonging to the families of Peptostreptococcaceae and Clostridiaceae (order Clostridiales). Mapping of diet contribution on the African Lake Tanganyika network (therefore excluding the geographic variable) revealed a clear community change from carnivores (C) to omnivores (O) to herbivores (H). Node abundances and effect size for pairwise comparisons between diets supported a strong contrasting pattern between C and H. Moreover, diet-associated nodes in H formed complex modules of positive interactions among taxonomically diverse bacteria (mostly Verrucomicrobia and Proteobacteria).ConclusionsConservation of microbial network topologies and specific bacterial associations across distinct lake assemblages point to a major host-associated effect and potential deterministic processes shaping the cichlid gut microbiota. While the origin and biological relevance of these common associations remain unclear, their persistence suggests an important functional role in the cichlid gut. Among the very diverse cichlids of L. Tanganyika, diet nonetheless represents a major driver of microbial community changes. By intersecting results from predictive network inferences and experimental trials, future studies will be directed to explore the strength of these associations, predict the outcome of community alterations driven by diet and ultimately help understanding the role of gut microbiota in cichlid trophic diversification.

Project description:Microbes commonly organize into communities consisting of hundreds of species involved in complex interactions with each other. 16S ribosomal RNA (16S rRNA) amplicon profiling provides snapshots that reveal the phylogenies and abundance profiles of these microbial communities. These snapshots, when collected from multiple samples, can reveal the co-occurrence of microbes, providing a glimpse into the network of associations in these communities. However, the inference of networks from 16S data involves numerous steps, each requiring specific tools and parameter choices. Moreover, the extent to which these steps affect the final network is still unclear. In this study, we perform a meticulous analysis of each step of a pipeline that can convert 16S sequencing data into a network of microbial associations. Through this process, we map how different choices of algorithms and parameters affect the co-occurrence network and identify the steps that contribute substantially to the variance. We further determine the tools and parameters that generate robust co-occurrence networks and develop consensus network algorithms based on benchmarks with mock and synthetic data sets. The Microbial Co-occurrence Network Explorer, or MiCoNE (available at https://github.com/segrelab/MiCoNE) follows these default tools and parameters and can help explore the outcome of these combinations of choices on the inferred networks. We envisage that this pipeline could be used for integrating multiple data sets and generating comparative analyses and consensus networks that can guide our understanding of microbial community assembly in different biomes. IMPORTANCE Mapping the interrelationships between different species in a microbial community is important for understanding and controlling their structure and function. The surge in the high-throughput sequencing of microbial communities has led to the creation of thousands of data sets containing information about microbial abundances. These abundances can be transformed into co-occurrence networks, providing a glimpse into the associations within microbiomes. However, processing these data sets to obtain co-occurrence information relies on several complex steps, each of which involves numerous choices of tools and corresponding parameters. These multiple options pose questions about the robustness and uniqueness of the inferred networks. In this study, we address this workflow and provide a systematic analysis of how these choices of tools affect the final network and guidelines on appropriate tool selection for a particular data set. We also develop a consensus network algorithm that helps generate more robust co-occurrence networks based on benchmark synthetic data sets.

Project description:Network modules are used for diverse purposes, ranging from delineation of biogeographical provinces to the study of biotic interactions. We assess spatial scaling effects on modular structure, using a multi-step process to compare fish co-occurrence networks at three nested scales. We first detect modules with simulated annealing and use spatial clustering tests (interspecific distances among species' range centroids) to determine if modules consist of species with broadly overlapping ranges; strong spatial clustering may reflect environmental filtering, while absence of spatial clustering may reflect positive interspecific relationships (commensalism or mutualism). We then use non-hierarchical, multivariate cluster analysis as an alternative method to identify fish subgroups, we repeat spatial clustering tests for the multivariate clusters, then compare spatial clustering results among modules and clusters. Next, we compare species lists within modules and clusters, and estimate congruence as the proportion of species assigned to the same groups by the two methods. Finally, we use a well-documented nest associate complex (fishes that deposit eggs in the gravel nests of a common host) to assess whether strong within-group associations may, in fact, reflect positive interspecific relationships. At each scale, 2-4 network modules were detected but a consistent relationship between scale and the number of modules was not observed. Significant spatial clustering was detected at all scales for network modules and multivariate clusters but was less prevalent at smaller scales. Congruence between modules and clusters was always < 90% and generally decreased as the number of groups increased. At all scales, the complete nest associate complex was completely preserved within a single network module, but not within a single multivariate cluster. Collectively, our results suggest that network modules are promising tools for studying positive interactions and that smaller scales may be preferable in this research.

Dataset Information

Topological distortion and reorganized modular structure of gut microbial co-occurrence networks in inflammatory bowel disease.

Publications

Topological distortion and reorganized modular structure of gut microbial co-occurrence networks in inflammatory bowel disease.

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