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Fish oil ameliorates neuropsychiatric behaviors and gut dysbiosis by elevating selected microbiota-derived metabolites and tissue tight junctions in rats under chronic sleep deprivation.
Neuropsychiatric behaviors caused by sleep deprivation (SD) are severe public health problems in modern society worldwide. This study investigated the effect of fish oil on neuropsychiatric behaviors, barrier injury, microbiota dysbiosis, and microbiota-derived metabolites in SD rats. The rats subjected to SD had significantly elevated blood levels of corticosteroid and lipopolysaccharides and exhibited anxiety-like behavior in the open field test, depression-like behavior in the forced swim test, and cognitive impairment in the Morris water maize test. We observed that the upregulation of proinflammatory cytokines in the SD rats resulted in colonic epithelial barrier injury including a decreased number of goblet cells and increased expression of selected tight junction proteins in the gut and brain. The gut microbiome status revealed a significant decrease in the microbial diversity in the SD rats, especially in probiotics. By contrast, a fish oil-based diet reversed SD-induced behavioral changes and improved the epithelial barrier injury and dysbiosis of the microbiota in the colon. These findings could be attributable to the increase in probiotics and short-chain fatty acid (SCFAs) production, improvement in selected intestinal barrier proteins, increase in SCFA receptor expression, and decrease in blood circulation proinflammatory status due to fish oil supplementation.
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Oral polyphenol-armored nanomedicine for targeted modulation of gut microbiota-brain interactions in colitis.
Developing oral nanomedicines that suppress intestinal inflammation while modulating gut microbiota and brain interactions is essential for effectively treating inflammatory bowel disease. Here, we report an oral polyphenol-armored nanomedicine based on tumor necrosis factor-α (TNF-α)-small interfering RNA and gallic acid-mediated graphene quantum dot (GAGQD)-encapsulated bovine serum albumin nanoparticle, with a chitosan and tannin acid (CHI/TA) multilayer. Referred to "armor," the CHI/TA multilayer resists the harsh environment of the gastrointestinal tract and adheres to inflamed colon sites in a targeted manner. TA provides antioxidative stress and prebiotic activities that modulate the diverse gut microbiota. Moreover, GAGQD protected TNF-α-siRNA delivery. Unexpectedly, the armored nanomedicine suppressed hyperactive immune responses and modulated bacterial gut microbiota homeostasis in a mouse model of acute colitis. Notably, the armored nanomedicine alleviated anxiety- and depression-like behaviors and cognitive impairment in mice with colitis. This armor strategy sheds light on the effect of oral nanomedicines on bacterial gut microbiome-brain interactions.
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Dietary Geranylgeraniol Mitigates Pain-Associated Behaviors via Improving Mitochondrial Function and Colon Integrity and Suppressing Neuroinflammation in Male Diabetic Neuropathy Rats.
Growing evidence highlights the links between diabetic neuropathy (DNP), gut dysbiosis, mitochondrial dysfunction and neuroinflammation in colon and bone microstructure deterioration. Geranylgeraniol (GG) shows neuroprotective and osteoprotective capacity. Our study examines GG's effects on pain-associated behaviors, glucose homeostasis, gut microbiota, mitochondrial homeostasis, and bone microstructure in DNP rats. We randomly assigned 27 male Sprague Dawley rats to three groups (n = 8-10/group): a control group (regular low-fat diet), a DNP group (high-fat diet + a single dose of 35 mg/kg streptozotocin), and a GG-treated DNP group (a single dose of 35 mg/kg streptozotocin + GG at 800 mg/kg in diet) for 6 weeks. Nocifensive response was assessed via the von Frey test and an open field test, and the elevated plus maze was used to assess anxio-depressive behaviors. The mRNA expression levels of tight junction protein, mitochondrial homeostasis, and neuroinflammation were measured in the colon using qRT-PCR. We collected fecal samples for microbiota composition analysis with 16S rRNA gene sequencing and analyzed by QIIME 2. All other data were analyzed via one-way ANOVA followed by post hoc Tukey's multiple comparison. p < 0.05 was defined as statistical significance. Our study showed GG's ability to mitigate mechanical hypersensitivity and anxio-depressive behavior in rats with DNP. GG supplementation did not improve glucose homeostasis (i.e., glucose intolerance, insulin sensitivity, pancreatic β-cell dysfunction) and bone microstructure. GG increased alpha-diversity without changing microbial abundance. DNP rats exhibited elevated Clostridium sensu stricto and reduced Eubacterium coprostanoligenes, Lachnospiraceae, Oscillospiraceae, and Peptococcaceae compared with controls. GG did not reverse DNP-induced gut dysbiosis but increased colonic claudin-3 (tight junction), MFN1 (mitochondria fusion), and TFAM (mitochondria biogenesis), while reducing FIS1 (mitochondria fission), GFAP (glial activation), P62 and PINK1 (mitophagy), and TNFα (inflammation). Functionally, GG reduced pain behaviors, improved intestinal integrity and mitochondrial homeostasis, increased alpha-diversity, and suppressed neuroinflammation, but did not improve glucose homeostasis or bone microstructure in obese DNP rats.
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Vagal sensing of altered gut microbiota links to externalizing behaviors.
Interoceptive brain responses triggered by intestinal microbiota influence mood-related behaviors such as anxiety and depression. Although genetic mutations can alter the gut microbiome, how alterations in the gut microbiome associated with host genetic variations relate to behavioral outcomes is not fully understood. We investigated how Sirtuin 3 (Sirt3) deficiency is linked to altered gut-brain interactions and mood-related behaviors. Gut microbiota composition and behavior were compared between Sirt3-knockout (KO) and wild-type (WT) mice. Cohousing and heterozygous littermate controls were used to assess microbiome-related contributions to behavioral differences. Transcriptomic profiling assessed region-specific gene expression in the limbic system. Metabolites in the nucleus of the solitary tract (NTS), potentially related to gut-brain vagal signaling, were analyzed. The role of the vagus nerve was further tested using subdiaphragmatic vagotomy in the Sirt3-KO mouse model, along with measurements of plasma choline levels in mice. Sirt3-KO mice displayed mood-related neurobehavioral changes and alterations in synaptic plasticity-related genes in the amygdala and the bed nucleus of the stria terminalis (BNST), accompanied by alterations in gut microbiome composition. Elevated plasma choline levels in Sirt3-KO mice, together with reduced neurotransmitter-related metabolites (e.g., γ-aminobutyric acid [GABA] in the NTS), suggest that externalizing behaviors in Sirt3-KO mice involve vagus nerve-dependent gut-brain axis signaling. Consistent with the involvement of vagal signaling, vagotomized Sirt3-KO mice were similar to WT mice in these measures, including GABA levels in the NTS and synaptic plasticity-related changes in the amygdala and BNST. Our findings support a model in which host genetic variation-associated microbiome alterations are sensed through sustained gut-vagal signaling under non-stressed conditions, correlating with NTS neurotransmitter alterations and externalizing behavioral phenotypes.
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Microbiota-targeted interventions and clinical implications for maternal-offspring health: An umbrella review of systematic reviews and meta-analyses of randomised controlled trials.
BACKGROUND: Microbes in the human body are the determinants of life-long health and disease. Microbiome acquisition starts in utero and matures during early childhood through breastfeeding. However, maternal gut dysbiosis affects the maternal-offspring microbiome interplay. Lines of evidence on dysbiosis-targeted interventions and their effect on maternal-offspring health and gut microbiome are inconsistent and inconclusive. Therefore, this study summarised studies to identify the most common microbiota-targeted intervention during pregnancy and lactation and to comprehensively evaluate its effects on maternal and offspring health. METHODS: This umbrella review was conducted by systematically searching databases such as PubMed and the Web of Science from inception to 2 September 2023. The quality was assessed using the Assessment of Multiple Systematic Reviews-2 checklist. The Grading of Recommendations Assessment, Development, and Evaluation was used for grading the strength and certainty of the studies. The overlap of primary studies was quantified by the corrected covered area score. RESULTS: A total of 17 systematic reviews and meta-analyses with 219 randomised controlled trials, 39 113 mothers, and 20 915 infants were included in this study. About 88% of studies had moderate and above certainty of evidence. Probiotics were the most common and effective interventions at reducing gestational diabetes risk (fasting blood glucose with the mean difference (MD) = -2.92, -0.05; I2 = 45, 98.97), fasting serum insulin (MD = -2.3, -2.06; I2 = 45, 77), glycated haemoglobin (Hb A1c) = -0.16; I2 = 0.00)), Homeostatic Model Assessment of insulin resistance (HOMA-IR) (MD = -20.55, -0.16; I2 = 0.00, 72.00), and lipid metabolism (MD = -5.47, 0.98; I2 = 0.00, 90.65). It was also effective in preventing and treating mastitis (risk ratio (RR) = 0.49; I2 = 2.00), relieving anxiety symptoms (MD = -0.99, 0.01; I2 = 0.00, 70.00), depression in lactation (MD = -0.46, -0.22; I2 = 0.00, 74.00) and reducing recto-vaginal bacterial colonisation (odds ratio (OR) = 0.62; I2 = 4.80), and with no adverse events. It also effectively remodelled the infant gut microbiome (MD = 0.89; I2 = 95.01) and prevented infant allergies. However, studies on pregnancy outcomes and preeclampsia incidences are limited. CONCLUSIONS: Our findings from high-quality studies identify that probiotics are the most common microbiome interventions during pregnancy and lactation. Probiotics have a strong impact on maternal and offspring health through maintaining gut microbiome homeostasis. However, further studies are needed on the effect of microbiota-targeted interventions on maternal cardiometabolic health, pregnancy, and neonatal outcomes. REGISTRATION: This umbrella review was registered with PROSPERO, CRD42023437098.
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Maternal gut microbiota disruption alters postpartum maternal behavior in association with modulation of stress responses and brain tryptophan metabolism in mice.
The maternal gut microbiota serves as a primary source of microbial transmission to offspring and plays a critical role in offspring development; however, its contribution to maternal mental states during the perinatal period remains poorly understood. In this study, we investigated how perturbation of maternal gut microbiota during pregnancy affects postpartum behavior using a mouse model treated with non-absorbable antibiotics. Antibiotic-treated dams exhibited increased offspring mortality and altered maternal behavior during the postpartum period. These behavioral alterations were accompanied by elevated plasma corticosterone and IL-6 levels, indicating enhanced stress and inflammatory responses. Plasma metabolomic and amino acid profiles in antibiotic-treated dams did not align with those typically observed in depression models or patients diagnosed with depressive disorders. Furthermore, tryptophan metabolism tended to shift towards the kynurenine pathway in key brain regions of antibiotic-treated dams. Together, these findings suggest that maternal gut microbiota contributes to the regulation of postpartum maternal behavior, which is associated with modulation of stress responses and brain tryptophan metabolism. This study highlights a previously underappreciated role of the maternal microbiota in maintaining maternal mental well-being and suggests potential targets for preventing maladaptive maternal behaviors that affect offspring development.
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The Microbiome and Host Behavior.
The microbiota is increasingly recognized for its ability to influence the development and function of the nervous system and several complex host behaviors. In this review, we discuss emerging roles for the gut microbiota in modulating host social and communicative behavior, stressor-induced behavior, and performance in learning and memory tasks. We summarize effects of the microbiota on host neurophysiology, including brain microstructure, gene expression, and neurochemical metabolism across regions of the amygdala, hippocampus, frontal cortex, and hypothalamus. We further assess evidence linking dysbiosis of the gut microbiota to neurobehavioral diseases, such as autism spectrum disorder and major depression, drawing upon findings from animal models and human trials. Finally, based on increasing associations between the microbiota, neurophysiology, and behavior, we consider whether investigating mechanisms underlying the microbiota-gut-brain axis could lead to novel approaches for treating particular neurological conditions.
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Gut microbes limit growth in house sparrow nestlings (Passer domesticus) but not through limitations in digestive capacity.
Recent research often lauds the services and beneficial effects of host-associated microbes on animals. However, hosting these microbes may come at a cost. For example, germ-free and antibiotic-treated birds generally grow faster than their conventional counterparts. In the wild, juvenile body size is correlated with survival, so hosting a microbiota may incur a fitness cost. Avian altricial nestlings represent an interesting study system in which to investigate these interactions, given that they exhibit the fastest growth rates among vertebrates, and growth is limited by their digestive capacity. We investigated whether reduction and restructuring of the microbiota by antibiotic treatment would: (i) increase growth and food conversion efficiency in nestling house sparrows (Passer domesticus); (ii) alter aspects of gut anatomy or function (particularly activities of digestive carbohydrases and their regulation in response to dietary change); and (iii) whether there were correlations between relative abundances of microbial taxa, digestive function and nestling growth. Antibiotic treatment significantly increased growth and food conversion efficiency in nestlings. Antibiotics did not alter aspects of gut anatomy that we considered but depressed intestinal maltase activity. There were no significant correlations between abundances of microbial taxa and aspects of host physiology. Overall, we conclude that microbial-induced growth limitation in developing birds is not driven by interactions with digestive capacity. Rather, decreased energetic and material costs of immune function or beneficial effects from microbes enriched under antibiotic treatment may underlie these effects. Understanding the costs and tradeoffs of hosting gut microbial communities represents an avenue of future research.
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Microbiome and metabolome reveal the metabolic and microbial variations induced by depression and constipation.
BACKGROUND: Depressed patients are often accompanied with constipation symptoms, and vice versa. However, the underlying mechanisms of such a bidirectional correlation have remained elusive. We aim to reveal the possible correlations between depression and constipation from the perspectives of gut microbiome and plasma metabolome. METHODS: We constructed the depressed model and the constipated model of rats, respectively. First, we measured the locomotor activity status and the gastrointestinal functions of rats. And then, nuclear magnetic resonance plasma metabolomics was applied to reveal the shared and the unique metabolites of depression and constipation. In addition, 16 S ribosomal RNA gene sequencing was used to detect the impacts of constipation and depression on gut microbiota of rats. Finally, a multiscale and multifactorial network, that is, the 'phenotypes - differential metabolites - microbial biomarkers' integrated network, was constructed to visualise the mechanisms of connections between depression and constipation. RESULTS: We found that spontaneous locomotor activity and gastrointestinal functions of both depressed rats and constipated rats significantly decreased. Further, eight metabolites and 14 metabolites were associated depression and constipation, respectively. Among them, seven metabolites and four metabolic pathways were shared by constipation and depression, mainly perturbing energy metabolism and amino acid metabolism. Additionally, depression and constipation significantly disordered the functions and the compositions of gut microbiota of rats, and decreased the ratio of Firmicutes to Bacteroidetes. CONCLUSION: The current findings provide multiscale and multifactorial perspectives for understanding the correlations between depression and constipation, and demonstrate new mechanisms of comorbidity of depression and constipation.
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Altered fecal microbiota composition in patients with major depressive disorder.
Studies using animal models have shown that depression affects the stability of the microbiota, but the actual structure and composition in patients with major depressive disorder (MDD) are not well understood. Here, we analyzed fecal samples from 46 patients with depression (29 active-MDD and 17 responded-MDD) and 30 healthy controls (HCs). High-throughput pyrosequencing showed that, according to the Shannon index, increased fecal bacterial α-diversity was found in the active-MDD (A-MDD) vs. the HC group but not in the responded-MDD (R-MDD) vs. the HC group. Bacteroidetes, Proteobacteria, and Actinobacteria strongly increased in level, whereas that of Firmicutes was significantly reduced in the A-MDD and R-MDD groups compared with the HC group. Despite profound interindividual variability, levels of several predominant genera were significantly different between the MDD and HC groups. Most notably, the MDD groups had increased levels of Enterobacteriaceae and Alistipes but reduced levels of Faecalibacterium. A negative correlation was observed between Faecalibacterium and the severity of depressive symptoms. These findings enable a better understanding of changes in the fecal microbiota composition in such patients, showing either a predominance of some potentially harmful bacterial groups or a reduction in beneficial bacterial genera. Further studies are warranted to elucidate the temporal and causal relationships between gut microbiota and depression and to evaluate the suitability of the microbiome as a biomarker.