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The Use of Defined Microbial Communities To Model Host-Microbe Interactions in the Human Gut.

ABSTRACT: The human intestinal ecosystem is characterized by a complex interplay between different microorganisms and the host. The high variation within the human population further complicates the quest toward an adequate understanding of this complex system that is so relevant to human health and well-being. To study host-microbe interactions, defined synthetic bacterial communities have been introduced in gnotobiotic animals or in sophisticated in vitro cell models. This review reinforces that our limited understanding has often hampered the appropriate design of defined communities that represent the human gut microbiota. On top of this, some communities have been applied to in vivo models that differ appreciably from the human host. In this review, the advantages and disadvantages of using defined microbial communities are outlined, and suggestions for future improvement of host-microbe interaction models are provided. With respect to the host, technological advances, such as the development of a gut-on-a-chip system and intestinal organoids, may contribute to more-accurate in vitro models of the human host. With respect to the microbiota, due to the increasing availability of representative cultured isolates and their genomic sequences, our understanding and controllability of the human gut "core microbiota" are likely to increase. Taken together, these advancements could further unravel the molecular mechanisms underlying the human gut microbiota superorganism. Such a gain of insight would provide a solid basis for the improvement of pre-, pro-, and synbiotics as well as the development of new therapeutic microbes.

SUBMITTER: Elzinga J

PROVIDER: S-EPMC6684003 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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The Use of Defined Microbial Communities To Model Host-Microbe Interactions in the Human Gut.

Elzinga Janneke J van der Oost John J de Vos Willem M WM Smidt Hauke H

Microbiology and molecular biology reviews : MMBR 20190313 2

The human intestinal ecosystem is characterized by a complex interplay between different microorganisms and the host. The high variation within the human population further complicates the quest toward an adequate understanding of this complex system that is so relevant to human health and well-being. To study host-microbe interactions, defined synthetic bacterial communities have been introduced in gnotobiotic animals or in sophisticated <i>in vitro</i> cell models. This review reinforces that ...[more]

PMID: 30867232

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Project description:Mutualisms between microbes and insects are ubiquitous and facilitate exploitation of various trophic niches by host insects. Dictyopterans (mantids, cockroaches and termites) exhibit trophisms that range from omnivory to strict wood-feeding and maintain beneficial symbioses with the obligate endosymbiont, Blattabacterium, and/or diverse gut microbiomes that include cellulolytic and diazotrophic microbes. While Blattabacterium in omnivorous Periplaneta is fully capable of provisioning essential amino acids, in wood-feeding dictyopterans it has lost many genes for their biosynthesis (Mastotermes and Cryptocercus) or is completely absent (Heterotermes). The conspicuous functional degradation and absence of Blattabacterium in most strict wood-feeding dictyopteran insects suggest that alternative means of acquiring nutrients limited in their diet are being employed. A 16S rRNA gene amplicon resequencing approach was used to deeply sample the composition and diversity of gut communities in related dictyopteran insects to explore the possibility of shifts in symbiont allegiances during termite and cockroach evolution. The gut microbiome of Periplaneta, which has a fully functional Blattabacterium, exhibited the greatest within-sample operational taxonomic unit (OTU) diversity and abundance variability than those of Mastotermes and Cryptocercus, whose Blattabacterium have shrunken genomes and reduced nutrient provisioning capabilities. Heterotermes lacks Blattabacterium and a single OTU that was 95% identical to a Bacteroidia-assigned diazotrophic endosymbiont of an anaerobic cellulolytic protist termite gut inhabitant samples consistently dominates its gut microbiome. Many host-specific OTUs were identified in all host genera, some of which had not been previously detected, indicating that deep sampling by pyrotag sequencing has revealed new taxa that remain to be functionally characterized. Further analysis is required to uncover how consistently detected taxa in the cockroach and termite gut microbiomes, as well as the total community, contribute to host diet choice and impact the fate of Blattabacterium in dictyopterans.

Project description:Background The gut microbiome is altered in patients with inflammatory bowel disease, yet how these alterations contribute to intestinal inflammation is poorly understood. Murine models have demonstrated the importance of the microbiome in colitis since colitis fails to develop in many genetically susceptible animal models when re-derived into germ-free environments. We have previously shown that Wiskott-Aldrich syndrome protein (WASP)-deficient mice (Was−/−) develop spontaneous colitis, similar to human patients with loss-of-function mutations in WAS. Furthermore, we showed that the development of colitis in Was−/− mice is Helicobacter dependent. Here, we utilized a reductionist model coupled with multi-omics approaches to study the role of host-microbe interactions in intestinal inflammation. Results Was−/− mice colonized with both altered Schaedler flora (ASF) and Helicobacter developed colitis, while those colonized with either ASF or Helicobacter alone did not. In Was−/− mice, Helicobacter relative abundance was positively correlated with fecal lipocalin-2 (LCN2), a marker of intestinal inflammation. In contrast, WT mice colonized with ASF and Helicobacter were free of inflammation and strikingly, Helicobacter relative abundance was negatively correlated with LCN2. In Was−/− colons, bacteria breach the mucus layer, and the mucosal relative abundance of ASF457 Mucispirillum schaedleri was positively correlated with fecal LCN2. Meta-transcriptomic analyses revealed that ASF457 had higher expression of genes predicted to enhance fitness and immunogenicity in Was−/− compared to WT mice. In contrast, ASF519 Parabacteroides goldsteinii’s relative abundance was negatively correlated with LCN2 in Was−/− mice, and transcriptional analyses showed lower expression of genes predicted to facilitate stress adaptation by ASF519 in Was−/−compared to WT mice. Conclusions These studies indicate that the effect of a microbe on the immune system can be context dependent, with the same bacteria eliciting a tolerogenic response under homeostatic conditions but promoting inflammation in immune-dysregulated hosts. Furthermore, in inflamed environments, some bacteria up-regulate genes that enhance their fitness and immunogenicity, while other bacteria are less able to adapt and decrease in abundance. These findings highlight the importance of studying host-microbe interactions in different contexts and considering how the transcriptional profile and fitness of bacteria may change in different hosts when developing microbiota-based therapeutics. Video abstract Supplementary Information The online version contains supplementary material available at 10.1186/s40168-021-01161-3.

Dataset Information

The Use of Defined Microbial Communities To Model Host-Microbe Interactions in the Human Gut.

Publications

The Use of Defined Microbial Communities To Model Host-Microbe Interactions in the Human Gut.

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