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High-Altitude Drives the Convergent Evolution of Alpha Diversity and Indicator Microbiota in the Gut Microbiomes of Ungulates.

ABSTRACT: Convergent evolution is an important sector of evolutionary biology. High-altitude environments are one of the extreme environments for animals, especially in the Qinghai Tibet Plateau, driving the inquiry of whether, under broader phylogeny, high-altitude factors drive the convergent evolution of Artiodactyla and Perissodactyla gut microbiomes. Therefore, we profiled the gut microbiome of Artiodactyla and Perissodactyla at high and low altitudes using 16S rRNA gene sequencing. According to cluster analyses, the gut microbiome compositions of high-altitude Artiodactyla and Perissodactyla were not grouped together and were far from those of low-altitude Artiodactyla and Perissodactyla. The Wilcoxon's test in high-altitude ungulates showed significantly higher Sobs and Shannon indices than in low-altitude ungulates. At the phylum level, Firmicutes and Patescibacteria were significantly enriched in the gut microbiomes of high-altitude ungulates, which also displayed a higher Firmicutes/Bacteroidetes value than low-altitude ungulates. At the family level, Ruminococcaceae, Christensenellaceae, and Saccharimonadaceae were significantly enriched in the gut microbiomes of high-altitude ungulates. Our results also indicated that the OH and FH groups shared two significantly enriched genera, Christensenellaceae_R_7_group and Candidatus_Saccharimonas. These findings indicated that a high altitude cannot surpass the order level to drive the convergent evolution of ungulate gut microbiome composition but can drive the convergent evolution of alpha diversity and indicator microbiota in the gut microbiome of ungulates. Overall, this study provides a novel perspective for understanding the adaptation of ungulates to high-altitude environments.

SUBMITTER: Wang X

PROVIDER: S-EPMC9301279 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Animal gut microbiota plays an indispensable role in host adaptation to different altitude environments. At present, little is known about the mechanism of animal gut microbiota in host adaptation to high altitude environments. Here, we selected wild macaques, humans, and dogs with different levels of kinship and intimate relationships in high altitude and low altitude environments, and analyzed the response of their gut microbiota to the host diet and altitude environments. Alpha diversity analysis found that at high altitude, the gut microbiota diversity of wild macaques with more complex diet in the wild environments is much higher than that of humans and dogs with simpler diet (p < 0.05), and beta diversity analysis found that the UniFrac distance between humans and dogs was significantly lower than between humans and macaques (p < 0.05), indicating that diet strongly drive the convergence of gut microbiota among species. Meanwhile, alpha diversity analysis found that among three subjects, the gut microbiota diversity of high altitude population is higher than that of low altitude population (ACE index in three species, Shannon index in dog and macaque and Simpson index in dog, p < 0.05), and beta diversity analysis found that the UniFrac distances among the three subjects in the high altitude environments were significantly lower than in the low altitude environments (p < 0.05). Additionally, core shared ASVs analysis found that among three subjects, the number of core microbiota in high altitude environments is higher than in low altitude environments, up to 5.34 times (1,105/207), and the proportion and relative abundance of the core bacteria types in each species were significantly higher in high altitude environments than in low altitude environments (p < 0.05). The results showed that high altitude environments played an important role in driving the convergence of gut microbiota among species. Furthermore, the neutral community model trial found that the gut microbiota of the three subjects was dispersed much more at high altitude than at low altitude, implying that the gut microbiota convergence of animals at high altitudes may be partly due to the microbial transmission between hosts mediated by human activities.

Project description:BackgroundNeurological diseases are difficult to diagnose in time, and there is currently a lack of effective predictive methods. Previous studies have indicated that a variety of neurological diseases cause changes in the gut microbiota. Alpha diversity is a major indicator to describe the diversity of the gut microbiota. At present, the relationship between neurological diseases and the alpha diversity of the gut microbiota remains unclear.MethodsWe performed a systematic literature search of Pubmed and Bioproject databases up to January 2021. Six indices were used to measure alpha diversity, including community richness (observed species, Chao1 and ACE), community diversity (Shannon, Simpson), and phylogenetic diversity (PD). Random-effects meta-analyses on the standardized mean difference (SMD) were carried out on the alpha diversity indices. Subgroup analyses were performed to explore the sources of interstudy heterogeneity. Meta-analysis was performed on articles by matching the age, sex, and body mass index (BMI) of the disease group with the control group. Meanwhile, subgroup analysis was performed to control the variability of the sequencing region, platform, geographical region, instrument, and diseases. The area under the curve (AUC) value of the receiver operating characteristic (ROC) curve was calculated to assess the prediction effectiveness of the microbial alpha diversity indices.ResultsWe conducted a meta-analysis of 24 published studies on 16S rRNA gene amplified sequencing of the gut microbiota and neurological diseases from the Pubmed and Bioproject database (patients, n = 1,469; controls, n = 1,289). The pooled estimate demonstrated that there was no significant difference in the alpha diversity between patients and controls (P < 0.05). Alpha diversity decreased only in Parkinson's disease patients, while it increased in anorexia nervosa patients compared to controls. After adjusting for age, sex, BMI, and geographical region, none of the alpha diversity was associated with neurological diseases. In terms of Illumina HiSeq 2000 and the V3-V5 sequencing region, the results showed that alpha diversity increased significantly in comparison with the controls, while decreased in Illumina HiSeq 2500. ROC curves suggested that alpha diversity could be used as a biomarker to predict the AD (Simpson, AUC= 0.769, P = 0.0001), MS (observed species, AUC= 0.737, P = 0.001), schizophrenia (Chao1, AUC = 0.739, P = 0.002).ConclusionsOur review summarized the relationship between alpha diversity of the gut microbiota and neurological diseases. The alpha diversity of gut microbiota could be a promising predictor for AD, schizophrenia, and MS, but not for all neurological diseases.

Project description:Hypobaric hypoxia and dietary protein and fat intakes have been independently associated with an altered gastrointestinal (GI) environment and gut microbiota, but little is known regarding host-gut microbiota interactions at high altitude (HA) and the impact of diet macronutrient composition. This study aimed to determine the effect of dietary protein:fat ratio manipulation on the gut microbiota and GI barrier function during weight loss at high altitude (HA) and to identify associations between the gut microbiota and host responses to HA. Following sea-level (SL) testing, 17 healthy males were transported to HA (4,300 m) and randomly assigned to consume provided standard protein (SP; 1.1 g·kg-1·day-1, 39% fat) or higher protein (HP; 2.1 g·kg-1·day-1, 23% fat) carbohydrate-matched hypocaloric diets for 22 days. Fecal microbiota composition and metabolites, GI barrier function, GI symptoms, and acute mountain sickness (AMS) severity were measured. Macronutrient intake did not impact fecal microbiota composition, had only transient effects on microbiota metabolites, and had no effect on increases in small intestinal permeability, GI symptoms, and inflammation observed at HA. AMS severity was also unaffected by diet but in exploratory analyses was associated with higher SL-relative abundance of Prevotella, a known driver of interindividual variability in human gut microbiota composition, and greater microbiota diversity after AMS onset. Findings suggest that the gut microbiota may contribute to variability in host responses to HA independent of the dietary protein:fat ratio but should be considered preliminary and hypothesis generating due to the small sample size and exploratory nature of analyses associating the fecal microbiota and host responses to HA. NEW & NOTEWORTHY This study is the first to examine interactions among diet, the gut microbiota, and host responses to weight loss at high altitude (HA). Observed associations among the gut microbiota, weight loss at HA, and acute mountain sickness provide evidence that the microbiota may contribute to variability in host responses to HA. In contrast, dietary protein:fat ratio had only minimal, transient effects on gut microbiota composition and bacterial metabolites which were likely not of clinical consequence.

Project description:This study was conducted to investigate the effects of high-altitude hypoxic environments on the gut microbiota. Male Sprague-Dawley rats were randomly divided into three groups, namely, the plain, moderate-altitude hypoxic, and high-altitude hypoxic groups. On the 3rd, 7th, 15th, and 30th days of exposure, fecal samples were collected and analyzed via 16S rRNA gene sequencing technology. Fecal microbiota transplantation (FMT) experiments were also performed. The results showed significant differences between the gut microbiota structure and diversity of rats in the high-altitude hypoxic group and those of rats in the other groups. Further, compared with that of rats in the plain group, the gut microbiota of rats in the two hypoxic groups showed the most significant changes on day 7. Furthermore, the gut microbiota of the rats in the FMT groups exhibited changes and became increasingly similar to those of the rats in the hypoxic groups. We also identified the phylum Firmicutes, genus Akkermansia, and genus Lactobacillus as the core microbiota under hypoxic conditions. Phenotypic analysis indicated a decrease in the proportion of aerobic bacteria and an increase in that of anaerobic bacteria, possibly owing to the high-altitude hypoxic environment. Additionally, functional analysis showed significant differences between the different groups with respect to different metabolic pathways, including carbohydrate metabolism, energy metabolism, glycan biosynthesis, and metabolism. These findings indicated significant changes in gut microbiota structure and diversity under high-altitude hypoxia, establishing a foundation for further research on the pathogenesis and development of diseases, as well as drug metabolism, under high-altitude hypoxia. IMPORTANCE In this study, we investigated the effects of high-altitude hypoxic environments with low oxygen levels on the gut microbiota characteristics of rats. We observed that high-altitude hypoxia is an important environmental factor that can affect gut microbiota structure and diversity, thereby affecting homeostasis in the host intestinal environment. These findings provide a basis for further studies on disease initiation and development, as well as drug metabolism, in high-altitude hypoxic environments.

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High-Altitude Drives the Convergent Evolution of Alpha Diversity and Indicator Microbiota in the Gut Microbiomes of Ungulates.

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