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Enteric Viruses Nucleic Acids Distribution along the Digestive Tract of Rhesus Macaques with Idiopathic Chronic Diarrhea.

ABSTRACT: Idiopathic chronic diarrhea (ICD) is a little understood common clinical problem in captive rhesus macaques claiming 33% of medical culls unrelated to research. The eukaryotic virome in digestive tract tissues collected at necropsy from nine animals with ICD was characterized using viral metagenomics. We compared the distribution of viral reads in tissues and mucosal scrapings from the stomach, duodenum, jejunum, ileum, and the proximal, transverse, and distal colons. In situ hybridization (ISH) using viral probes were performed on fixed tissues. Deep sequencing revealed multiple viruses in the Parvoviridae and Picornaviridae family. Tissues and mucosal scraping from the same locations showed closely related viral reads contents while different gut tissues from the same animal varied widely. ISH showed punctuated staining for both RNA and DNA viruses in the distal colon. Parvovirus staining was also detected in the stomach/duodenum/jejunum in distinct oval-shaped structures. The location of enteric viral nucleic acid differed widely between different viral families and along the length of the digestive tract.

SUBMITTER: Delwart E

PROVIDER: S-EPMC8951234 | biostudies-literature | 2022 Mar

REPOSITORIES: biostudies-literature

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Enteric Viruses Nucleic Acids Distribution along the Digestive Tract of Rhesus Macaques with Idiopathic Chronic Diarrhea.

Delwart Eric E Merriam David D Ardeshir Amir A Altan Eda E Li Yanpeng Y Deng Xutao X Hartigan-O'Connor Dennis J DJ

Viruses 20220319 3

Idiopathic chronic diarrhea (ICD) is a little understood common clinical problem in captive rhesus macaques claiming 33% of medical culls unrelated to research. The eukaryotic virome in digestive tract tissues collected at necropsy from nine animals with ICD was characterized using viral metagenomics. We compared the distribution of viral reads in tissues and mucosal scrapings from the stomach, duodenum, jejunum, ileum, and the proximal, transverse, and distal colons. In situ hybridization (ISH) ...[more]

PMID: 35337045

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Project description:Diarrhea is the major cause of non-research-associated morbidity and mortality affecting the supply of rhesus macaques and, potentially, their responses to experimental treatments. Idiopathic chronic diarrhea (ICD) in rhesus macaques also resembles ulcerative colitis, one form of human inflammatory bowel disease. To test for viral etiologies, we characterized and compared the fecal viromes from 32 healthy animals, 31 animals with acute diarrhea, and 29 animals with ICD. The overall fractions of eukaryotic viral reads were 0.063% for the healthy group, 0.131% for the acute-diarrhea group, and 0.297% for the chronic-diarrhea group. Eukaryotic viruses belonging to 6 viral families, as well as numerous circular Rep-encoding single-stranded DNA (CRESS DNA) viral genomes, were identified. The most commonly detected sequences were from picornaviruses, making up 59 to 88% of all viral reads, followed by 9 to 17% for CRESS DNA virus sequences. The remaining 5 virus families, Adenoviridae, Astroviridae, Anelloviridae, Picobirnaviridae, and Parvoviridae, collectively made up 1 to 3% of the viral reads, except for parvoviruses, which made up 23% of the viral reads in the healthy group. Detected members of the families Picornaviridae and Parvoviridae were highly diverse, consisting of multiple genera, species, and genotypes. Coinfections with members of up to six viral families were detected. Complete and partial viral genomes were assembled and used to measure the number of matching short sequence reads in feces from the 92 animals in the two clinical and the healthy control groups. Several enterovirus genotypes and CRESS DNA genomes were associated with ICD relative to healthy animals. Conversely, higher read numbers from different parvoviruses were associated with healthy animals. Our study reveals a high level of enteric coinfections with diverse viruses in a captive rhesus macaque colony and identifies several viruses positively or negatively associated with ICD.

Project description:Diversity and composition of microbial communities was compared across the 13 major sections of the digestive tract (esophagus, reticulum, rumen, omasum, abomasum, duodenum, jejunum, ileum, cecum, ascending colon, transverse colon, descending colon, and rectum) in two captive populations of American bison (Bison bison), one of which was finished on forage, the other on grain.Microbial diversity fell to its lowest levels in the small intestine, with Bacteroidetes reaching their lowest relative abundance in that region, while Firmicutes and Euryarchaeota attained their highest relative abundances there. Gammaproteobacteria were most abundant in the esophagus, small intestine, and colon. The forage-finished bison population exhibited higher overall levels of diversity, as well as a higher relative abundance of Bacteroidetes in most gut sections. The grain-finished bison population exhibited elevated levels of Firmicutes and Gammaproteobacteria. Within each population, different sections of the digestive tract exhibited divergent microbial community composition, although it was essentially the same among sections within a given region of the digestive tract. Shannon diversity was lowest in the midgut. For each section of the digestive tract, the two bison populations differed significantly in microbial community composition.Similarities among sections indicate that the esophagus, reticulum, rumen, omasum, and abomasum may all be considered to house the foregut microbiota; the duodenum, jejunum, and ileum may all be considered to house the small intestine or midgut microbiota; and the cecum, ascending colon, transverse colon, descending colon, and rectum may all be considered to house the hindgut microbiota. Acid from the stomach, bile from the gall bladder, digestive enzymes from the pancreas, and the relatively low retention time of the small intestine may have caused the midgut's low microbial diversity. Differences in microbial community composition between populations may have been most strongly influenced by differences in diet (forage or grain). The clinical condition of the animals used in the present study was not evaluated, so further research is needed to establish whether the microbial profiles of some bison in this study are indeed indicative of dysbiosis, a predisposing factor to ruminal acidosis and its sequelae.

Project description:The strategy of adjusting the composition of gastrointestinal microbiota has shown great promise for the treatment of diseases. Currently, the relationship between gut microbes and human diseases is mainly presented by the fecal microbiota from the colon. Due to the limits of sampling, the healthy baseline of biogeographic microbiota in the human gastrointestinal tract remains blurry. Captive nonhuman primates (NHPs) present a "humanized" intestinal microbiome and may make up for the lack of atlas data for better understanding of the gut microbial composition and diseases. Therefore, the intestinal microbiota of 6 GIT regions of healthy rhesus monkeys were analyzed in this study; our results showed that Proteobacteria gradually decreased from the small intestine to the large intestine but Bacteroidetes gradually increased from the small intestine to the large intestine. Streptococcus and Lactobacillus can be used as markers to distinguish the small intestine from the large intestine. Sarcina is the most enriched in the middle site of the connection between the large intestine and the small intestine. Cyanobacteria are enriched in the small intestine, especially the duodenum and jejunum, and are absent in the large intestine. The lumenal microbiota of the small intestine is more susceptible to individual differences than is that of the large intestine. Metabolism and oxygen affect the distribution of the microbes, and the diversity of microbiota is the highest in the colon. Our results provide accurate comprehensive GIT microbiota data on nonhuman primates and will be beneficial for the better understanding of the composition of microbiota in the human gastrointestinal tract. IMPORTANCE For the study of upper gastrointestinal microbiota in humans, endoscopic sampling is the main source of information, which limits the understanding of healthy upper gastrointestinal microbiota. Rhesus monkeys show very close similarity to humans in physiology, genetics, and behavior and act as the most suitable animal models for human diseases. The present research made up for the lack of atlas data due to the ethical limitations of sampling in humans and provided baseline data on microbiota in 6 GIT regions of healthy NHPs. These important references will be beneficial for the better understanding of the regional organization and functions of gut microbial communities along the GIT and their relevance to conditions of health and disease.

Dataset Information

Enteric Viruses Nucleic Acids Distribution along the Digestive Tract of Rhesus Macaques with Idiopathic Chronic Diarrhea.

Publications

Enteric Viruses Nucleic Acids Distribution along the Digestive Tract of Rhesus Macaques with Idiopathic Chronic Diarrhea.

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