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Parasite infections, neuroinflammation, and potential contributions of gut microbiota.

ABSTRACT: Many parasitic diseases (including cerebral malaria, human African trypanosomiasis, cerebral toxoplasmosis, neurocysticercosis and neuroschistosomiasis) feature acute or chronic brain inflammation processes, which are often associated with deregulation of glial cell activity and disruption of the brain blood barrier's intactness. The inflammatory responses of astrocytes and microglia during parasite infection are strongly influenced by a variety of environmental factors. Although it has recently been shown that the gut microbiota influences the physiology and immunomodulation of the central nervous system in neurodegenerative diseases like Alzheimer's disease and Parkinson's, the putative link in parasite-induced neuroinflammatory diseases has not been well characterized. Likewise, the central nervous system can influence the gut microbiota. In parasite infections, the gut microbiota is strongly perturbed and might influence the severity of the central nervous system inflammation response through changes in the production of bacterial metabolites. Here, we review the roles of astrocytes and microglial cells in the neuropathophysiological processes induced by parasite infections and their possible regulation by the gut microbiota.

SUBMITTER: Alloo J

PROVIDER: S-EPMC9772015 | biostudies-literature | 2022

REPOSITORIES: biostudies-literature

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Parasite infections, neuroinflammation, and potential contributions of gut microbiota.

Alloo Jérémy J Leleu Ines I Grangette Corinne C Pied Sylviane S

Frontiers in immunology 20221208

Many parasitic diseases (including cerebral malaria, human African trypanosomiasis, cerebral toxoplasmosis, neurocysticercosis and neuroschistosomiasis) feature acute or chronic brain inflammation processes, which are often associated with deregulation of glial cell activity and disruption of the brain blood barrier's intactness. The inflammatory responses of astrocytes and microglia during parasite infection are strongly influenced by a variety of environmental factors. Although it has recently ...[more]

PMID: 36569929

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Project description:Animals and their associated microbiota share long evolutionary histories. However, it is not always clear how host genotype and microbiota interact to affect phenotype. We applied a hologenomic approach to explore how host-microbiota interactions shape lifetime growth and parasite infection in farmed Atlantic salmon (Salmo salar). Multi-omics data sets were generated from the guts of 460 salmon, 82% of which were naturally infected with an intestinal cestode. A single Mycoplasma bacterial strain, MAG01, dominated the gut metagenome of large, non-parasitized fish, consistent with previous studies showing high levels of Mycoplasma in the gut microbiota of healthy salmon. While small and/or parasitized salmon also had high abundance of MAG01, we observed increased alpha diversity in these individuals, driven by increased frequency of low-abundance Vibrionaceae and other Mycoplasma species that carried known virulence genes. Colonization by one of these cestode-associated Mycoplasma strains was associated with host individual genomic variation in long non-coding RNAs. Integrating the multi-omic data sets revealed coordinated changes in the salmon gut mRNA transcriptome and metabolome that correlated with shifts in the microbiota of smaller, parasitized fish. Our results suggest that the gut microbiota of small and/or parasitized fish is in a state of dysbiosis that partly depends on the host genotype, highlighting the value of using a hologenomic approach to incorporate the microbiota into the study of host-parasite dynamics.IMPORTANCEStudying host-microbiota interactions through the perspective of the hologenome is gaining interest across all life sciences. Intestinal parasite infections are a huge burden on human and animal health; however, there are few studies investigating the role of the hologenome during parasite infections. We address this gap in the largest multi-omics fish microbiota study to date using natural cestode infection of farmed Atlantic salmon. We find a clear association between cestode infection, salmon lifetime growth, and perturbation of the salmon gut microbiota. Furthermore, we provide the first evidence that the genetic background of the host may partly determine how the gut microbiota changes during parasite-associated dysbiosis. Our study therefore highlights the value of a hologenomic approach for gaining a more in-depth understanding of parasitism.

Project description:Background/objectivesDespite efforts within the framework of the Sustainable Development Goal to end malnutrition by 2030, malnutrition and soil-transmitted helminth infections persist in sub-Saharan Africa. A significant barrier to success is the inadequate understanding of effective intervention methods. Most research on the gut microbiota's role in health has been conducted in developed countries, leaving a critical gap in knowledge regarding low-income populations. This study addresses this gap by expanding research on the gut microbiota of underprivileged populations to help tackle these public health challenges.MethodsWe employed 16S rDNA sequencing to assess the bacterial gut microbiota composition of 60 children (mean age: 26.63 ± 6.36 months) and their 58 mothers (mean age: 30.03 ± 6.31 years) in Pemba, with a focus on helminth infection and nutritional status.ResultsOur differential abundance analysis identified bacterial taxa that were significantly negatively associated with both helminth infections and malnutrition, highlighting the potential for microbiota-directed interventions to address these health issues simultaneously. Notably, we identified Akkermansia, Blautia, Dorea, and Odoribacter as promising probiotic candidates for such interventions. In stunted children, positive co-occurrences were observed between Lactobacillus, Prevotella, and Bacteroides, while Escherichia/Shigella displayed negative co-abundance relationships with short-chain fatty acid (SCFA) producers in the gut microbiota. These findings suggest that administering Lactobacillus and SCFA-producing probiotics to children may foster the growth of beneficial bacteria like Prevotella and Bacteroides while reducing the relative abundance of Escherichia/Shigella, potentially enhancing overall health.ConclusionsThis study underscores the importance of microbiota-directed interventions in children and women of reproductive age as promising strategies, alongside established approaches, for combating helminth infections and malnutrition in vulnerable populations.

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Parasite infections, neuroinflammation, and potential contributions of gut microbiota.

Publications

Parasite infections, neuroinflammation, and potential contributions of gut microbiota.

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