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Diet-driven mercury contamination is associated with polar bear gut microbiota.

ABSTRACT: The gut microbiota may modulate the disposition and toxicity of environmental contaminants within a host but, conversely, contaminants may also impact gut bacteria. Such contaminant-gut microbial connections, which could lead to alteration of host health, remain poorly known and are rarely studied in free-ranging wildlife. The polar bear (Ursus maritimus) is a long-lived, wide-ranging apex predator that feeds on a variety of high trophic position seal and cetacean species and, as such, is exposed to among the highest levels of biomagnifying contaminants of all Arctic species. Here, we investigate associations between mercury (THg; a key Arctic contaminant), diet, and the diversity and composition of the gut microbiota of polar bears inhabiting the southern Beaufort Sea, while accounting for host sex, age class and body condition. Bacterial diversity was negatively associated with seal consumption and mercury, a pattern seen for both Shannon and Inverse Simpson alpha diversity indices (adjusted R² = 0.35, F_1,18 = 8.00, P = 0.013 and adjusted R² = 0.26, F_1,18 = 6.04, P = 0.027, respectively). No association was found with sex, age class or body condition of polar bears. Bacteria known to either be involved in THg methylation or considered to be highly contaminant resistant, including Lactobacillales, Bacillales and Aeromonadales, were significantly more abundant in individuals that had higher THg concentrations. Conversely, individuals with higher THg concentrations showed a significantly lower abundance of Bacteroidales, a bacterial order that typically plays an important role in supporting host immune function by stimulating intraepithelial lymphocytes within the epithelial barrier. These associations between diet-acquired mercury and microbiota illustrate a potentially overlooked outcome of mercury accumulation in polar bears.

SUBMITTER: Watson SE

PROVIDER: S-EPMC8642428 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Polar bears in captivity can be exposed to opportunistic pathogens not present in their natural environments. A 4-month-old polar bear (Ursus maritimus) living in an isolated enclosure with his mother in the Tierpark Berlin, Berlin, Germany, was suffering from severe abdominal pain, mild diarrhea, and loss of appetite and died in early 2017. Histopathology revealed severe hepatic degeneration and necrosis without evidence of inflammation or inclusion bodies, although a viral infection had been suspected on the basis of the clinical signs. We searched for nucleic acids of pathogens by shotgun high-throughput sequencing (HTS) from genomic DNA and cDNA extracted from tissue and blood. We identified a novel Mastadenovirus and assembled a nearly complete genome from the shotgun sequences. Quantitative PCR (qPCR) revealed that viral DNA was present in various concentrations in all tissues examined and that the highest concentrations were found in blood. Viral culture did not yield cytopathic effects, but qPCR suggested that virus replication was sustained for up to three passages. Positive immunofluorescence staining confirmed that the virus was able to replicate in the cells during early passage. Phylogenetic analysis demonstrated that the virus is highly divergent compared to other previously identified Mastadenovirus members and basal to most known viral clades. The virus was found only in the 4-month-old bear and not in other captive polar bears tested. We surmised, therefore, that the polar bear was infected from an unknown reservoir, illustrating that adenoviral diversity remains underestimated and that cross-species transmission of viruses can occur even under conditions of relative isolation.IMPORTANCE Cross-species transmission of viral pathogens is becoming an increasing problem for captive-animal facilities. This study highlights how animals in captivity are vulnerable to novel opportunistic pathogens, many of which do not result in straightforward diagnosis from symptoms and histopathology. In this study, a novel pathogen was suspected to have contributed to the death of a juvenile polar bear. HTS techniques were employed, and a novel Mastadenovirus was isolated. The virus was present in both the tissue and blood samples. Phylogenetic analysis of the virus at both the gene and genome levels revealed that it is highly divergent to other known mastadenoviruses. Overall, this study shows that animals in isolated conditions still come into contact with novel pathogens, and for many of these pathogens, the host reservoir and mode of transmission are yet to be determined.

Project description:There is increasing evidence for the interaction between gut microbiome, diet, and health. It is known that dysbiosis is related to disease and that most of the times this imbalances in gut microbial populations can be promoted through diet. Western dietary habits, which are characterized by high intakes of calories, animal proteins, saturated fats, and simple sugars have been linked with higher risk of obesity, diabetes, cancer, and cardiovascular disease. However, little is known about the impact of dietary patterns, dietary components, and nutrients on gut microbiota in healthy people. The aim of our study is to determine the effect of nutrient compounds as well as adherence to a dietary pattern, as the Mediterranean diet (MD) on the gut microbiome of healthy adults. Consequently, gut microbiota composition in healthy individuals, may be used as a potential biomarker to identify nutritional habits as well as risk of disease related to these habits. Dietary information from healthy volunteers (n = 27) was recorded using the Food Frequency Questionnaire. Adherence to the MD was measured using the PREDIMED test. Microbiota composition and diversity were obtained by 16S rRNA gene sequencing and specific quantitative polymerase chain reaction. Microbial metabolic activity was determined by quantification of short chain fatty acids (SCFA) on high performance liquid chromatography (HPLC). The results indicated that a higher ratio of Firmicutes-Bacteroidetes was related to lower adherence to the MD, and greater presence of Bacteroidetes was associated with lower animal protein intake. High consumption of animal protein, saturated fats, and sugars affected gut microbiota diversity. A significant higher presence of Christensenellaceae was found in normal-weight individuals compared to those who were overweight. This was also the case in volunteers with greater adherence to the MD compared to those with lower adherence. Butyricimonas, Desulfovibrio, and Oscillospira genera were associated with a BMI <25 and the genus Catenibacterium with a higher PREDIMED score. Higher bifidobacterial counts, and higher total SCFA were related to greater consumption of plant-based nutrients, such as vegetable proteins and polysaccharides. Better adherence to the MD was associated with significantly higher levels of total SCFA. Consequently, diet and specific dietary components could affect microbiota composition, diversity, and activity, which may have an effect on host metabolism by increasing the risk of Western diseases.

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Diet-driven mercury contamination is associated with polar bear gut microbiota.

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