A Microbial Community Ecology Perspective on the Gut-Microbiome-Brain Axis

Goot, Els van der; Spronsen, Francjan J. van; Salles, Joana Falcão; Zee, Eddy A. van der

doi:10.3389/fendo.2020.00611

Cited by 7 publications

(5 citation statements)

References 65 publications

(69 reference statements)

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“…A better understanding of the factors driving microbial invasions may help to prevent the spread and establishment of invasive species, or to aid the intentional introduction of a new species for a desired purpose. For example, it might be desirable to prevent the invasion of a species that reduces the efficiency of a bioremediation system [4], or to promote the colonization of probiotic species in the intestinal microbiome of a patient [5,6].…”

Section: Introductionmentioning

confidence: 99%

Microbial invasion of a toxic medium is facilitated by a resident community but inhibited as the community co-evolves

et al. 2022

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Predicting whether microbial invaders will colonize an environment is critical for managing natural and engineered ecosystems, and controlling infectious disease. Invaders often face competition by resident microbes. But how invasions play out in communities dominated by facilitative interactions is less clear. We previously showed that growth medium toxicity can promote facilitation between four bacterial species, as species that cannot grow alone rely on others to survive. Following the same logic, here we allowed other bacterial species to invade the four-species community and found that invaders could more easily colonize a toxic medium when the community was present. In a more benign environment instead, invasive species that could survive alone colonized more successfully when the residents were absent. Next, we asked whether early colonists could exclude future ones through a priority effect, by inoculating the invaders into the resident community only after its members had co-evolved for 44 weeks. Compared to the ancestral community, the co-evolved resident community was more competitive toward invaders and less affected by them. Our experiments show how communities may assemble by facilitating one another in harsh, sterile environments, but that arriving after community members have co-evolved can limit invasion success.

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Section: Introductionmentioning

confidence: 99%

Microbial invasion of a toxic medium is facilitated by a resident community but inhibited as the community co-evolves

et al. 2022

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“…The microbiome and small molecules also have roles in the aging process [ 51 ]. For PKU, the microbiome and dysbiosis may contribute to a more complete understanding of PKU pathophysiology [ 52 ]. Of course, our metabolic study is restricted only to a possible dysbiosis reflected by altered concentrations of metabolites derived from bacterial origin.…”

Section: Discussionmentioning

confidence: 99%

Phenylketonuria (PKU) Urinary Metabolomic Phenotype Is Defined by Genotype and Metabolite Imbalance: Results in 51 Early Treated Patients Using Ex Vivo 1H-NMR Analysis

et al. 2023

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Phenylketonuria (PKU) is a rare metabolic disorder caused by mutations in the phenylalanine hydroxylase gene. Depending on the severity of the genetic mutation, medical treatment, and patient dietary management, elevated phenylalanine (Phe) may occur in blood and brain tissues. Research has recently shown that high Phe not only impacts the central nervous system, but also other organ systems (e.g., heart and microbiome). This study used ex vivo proton nuclear magnetic resonance (1H-NMR) analysis of urine samples from PKU patients (mean 14.9 ± 9.2 years, n = 51) to identify the impact of elevated blood Phe and PKU treatment on metabolic profiles. Our results found that 24 out of 98 urinary metabolites showed a significant difference (p < 0.05) for PKU patients compared to age-matched healthy controls (n = 51) based on an analysis of urinary metabolome. These altered urinary metabolites were related to Phe metabolism, dysbiosis, creatine synthesis or intake, the tricarboxylic acid (TCA) cycle, end products of nicotinamide-adenine dinucleotide degradation, and metabolites associated with a low Phe diet. There was an excellent correlation between the metabolome and genotype of PKU patients and healthy controls of 96.7% in a confusion matrix model. Metabolomic investigations may contribute to a better understanding of PKU pathophysiology.

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“…A high(er) diversity leads to a biotic barrier, preventing the establishment and growth of (non-)pathogenic invaders from the environment. These disturbances are common and can lead to significant shifts in the community due to microbial competition if the resident microbial community is not able to outcompete the invader and return to the original (healthy) state ( 16 , 43 , 44 ). Therefore, from an ecological perspective, the semi Phe-restricted diet could potentially lead to an altered but more stable and resilient gut microbiome than the high Phe or Phe-restricted diets.…”

Section: Discussionmentioning

confidence: 99%

“…Due to the lack of knowledge about microbial functioning and the inconsistency in the function of specific bacterial genera, the importance of isolating and identifying particular species for the development of microbiome-based therapeutic strategies should be emphasized. We have previously argued that for successful probiotic supplementation, general concepts of community dynamics (i.e., the potential interactions within the gut microbiome) and microbial invasions and colonization should be taken into consideration during the development of microbiome-based therapeutic strategies to increase the treatment effectiveness and safety ( 44 ). Isolation of the specific species will allow the determination of their metabolic potential and reinoculation of these species to examine their effects specifically in the context of PKU-related alterations in the microbiome composition.…”

Section: Discussionmentioning

confidence: 99%

Gut-Microbiome Composition in Response to Phenylketonuria Depends on Dietary Phenylalanine in BTBR Pahenu2 Mice

et al. 2022

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Phenylketonuria (PKU) is a metabolic disorder caused by a hepatic enzyme deficiency causing high blood and brain levels of the amino acid Phenylalanine (Phe), leading to severe cognitive and psychological deficits that can be prevented, but not completely, by dietary treatment. The behavioral outcome of PKU could be affected by the gut-microbiome-brain axis, as diet is one of the major drivers of the gut microbiome composition. Gut-microbiome alterations have been reported in treated patients with PKU, although the question remains whether this is due to PKU, the dietary treatment, or their interaction. We, therefore, examined the effects of dietary Phe restriction on gut-microbiome composition and relationships with behavioral outcome in mice. Male and female BTBR Pahenu2 mice received either a control diet (normal protein, “high” Phe), liberalized Phe-restricted (33% natural protein restriction), or severe Phe-restricted (75% natural protein restriction) diet with protein substitutes for 10 weeks (n = 14 per group). Their behavioral performance was examined in an open field test, novel and spatial object location tests, and a balance beam. Fecal samples were collected and sequenced for the bacterial 16S ribosomal RNA (rRNA) region. Results indicated that PKU on a high Phe diet reduced Shannon diversity significantly and altered the microbiome composition compared with wild-type animals. Phe-restriction prevented this loss in Shannon diversity but changed community composition even more than the high-Phe diet, depending on the severity of the restriction. Moreover, on a taxonomic level, we observed the highest number of differentially abundant genera in animals that received 75% Phe-restriction. Based on correlation analyses with differentially abundant taxa, the families Entereococacceae, Erysipelotrichaceae, Porphyromonadaceae, and the genus Alloprevotella showed interesting relationships with either plasma Phe levels and/or object memory. According to our results, these bacterial taxa could be good candidates to start examining the microbial metabolic potential and probiotic properties in the context of PKU. We conclude that PKU leads to an altered gut microbiome composition in mice, which is least severe on a liberalized Phe-restricted diet. This may suggest that the current Phe-restricted diet for PKU patients could be optimized by taking dietary effects on the microbiome into account.

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A Microbial Community Ecology Perspective on the Gut-Microbiome-Brain Axis

Cited by 7 publications

References 65 publications

Microbial invasion of a toxic medium is facilitated by a resident community but inhibited as the community co-evolves

Microbial invasion of a toxic medium is facilitated by a resident community but inhibited as the community co-evolves

Phenylketonuria (PKU) Urinary Metabolomic Phenotype Is Defined by Genotype and Metabolite Imbalance: Results in 51 Early Treated Patients Using Ex Vivo 1H-NMR Analysis

Gut-Microbiome Composition in Response to Phenylketonuria Depends on Dietary Phenylalanine in BTBR Pahenu2 Mice

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