Gastrointestinal Biogeography of Luminal Microbiota and Short-Chain Fatty Acids in Sika Deer (Cervus nippon)

Abstract

Feces or specific segments of the gastrointestinal tract (in particular, the rumen) were sampled to explore the gut microbiome. The gastrointestinal biogeography of the luminal microbiota in ruminants, which is critical to guide accurate sampling for different purposes, is poorly understood at present.

Gut microbiome biogeography in reindeer supersedes millennia of ecological and evolutionary separation

“…Thus, GIT microbiome structuring is primarily driven by what seems to be a quasi-ubiquitous pattern of change in the relative abundance of the two dominant phyla—Bacteroidota and Firmicutes. This is in line with earlier studies on other ruminant species [Xie et al 2021 ; see also Li et al 2014 for Chinese roe deer ( Capreolus pygargus ); Kim et al 2019 for elk ( Cervus canadensis ); Hu et al 2022 for sika deer ( Cervus nippon )]. The higher Bacteroidota to Firmicutes ratio in the rumen has also been observed in reindeer across its distributional range (Pope et al 2012 , Glendinning et al 2021 ), and the opposite in faeces (Zielińska et al 2016 ).…”

“…ASV richness and Shannon diversity were also highly structured across the GIT in both reindeer subspecies, with the highest levels of diversity detected in the colon section, and the lowest in the small intestine. The observed patterns are comparable to other wild ruminants such as the Chinese roe deer (Li et al 2014 ) and the Sika deer (Hu et al 2022 ). However, only 30 to 40% of ASVs could be assigned to the genus level.…”

“…Overall, the catabolism of these sugars is known to result in the production of short-chain fatty acids—an essential energy source, providing up to 75% of the total metabolisable energy in ruminants (Bergman 1990 ), also important for a wider range of metabolic processes (Corrêa-Oliveira et al 2016 ; van der Hee and Wells 2021 ). Our results show the presence of enzymes important for the breakdown of carbohydrates in all regions along the GIT, also suggesting continuous production of various short-chain fatty acids in the small and large intestines as shown in the Sika deer (Hu et al 2022 ). Interestingly, the presence of sorbitol, known to be important for liveweight gain and milk production in domestic cattle (Geay et al 1992 , Hussian et al 2020 ) was observed in the Svalbard reindeer ( Fig.…”

“…However, comparatively little is known about the microbiomes of the other GIT compartments. Differences in pH levels and physiology (Kararli 1995 , Kohl et al 2013 ) together with documented structuring in the composition, diversity and function of microbial communities suggest a unique role in food digestion for each compartment (Xie et al 2021 , Hu et al 2022 ). Although several studies have indicated that structured microbial communities across the GIT may be a conserved trait across ruminant species (Li et al 2014 , Malmuthuge et al 2014 , Mao et al 2015 , Kim et al 2019 , Wang et al 2019 , Xie et al 2021 ), no studies have compared multiple sections of the GIT between subspecies subjected to differential selection pressures of diet, behaviour, and energy budgets.…”

Heterogeneity and Co-occurrence in the Luminal and Mucosal Gut Microbiomes and Metabolomes of Oriental Rat snake (Ptyas mucosus)

“…Short chain fatty acids (SCFAs), amino acids, bile acids, and other metabolites are important substances in microbe-mediated food digestion, nutrient absorption, energy metabolism, and immune homeostasis [3][4][5]. Most previous studies of the gut microbiome and/or metabolome in animals have involved analyses of feces [6][7][8][9], intestinal contents, and gastric luminal contents [10][11][12] by 16S rRNA gene sequencing, metagenomics, and metabolomics; however, mucosal microbiomes have not been extensively investigated. The mucosal microbiome is located in close proximity to the intestinal epithelium and have more direct interactions with the host immune system, compared with luminal/fecal bacteria; moreover, nutrient availability in the mucus layer of the epithelium considerably differs from the gut lumen environment [13].…”