The gut microbiome and metabolome of saddleback tamarins (Leontocebus weddelli): Insights into the foraging ecology of a small‐bodied primate

Abstract

Body mass is a strong predictor of diet and nutritional requirements across a wide range of mammalian taxa. In the case of small-bodied primates, because of their limited gut volume, rapid food passage rate, and high metabolic rate, they are hypothesized to maintain high digestive efficiency by exploiting foods rich in protein, fats, and readily available energy. However, our understanding of the dietary requirements of wild primates is limited because little is known concerning the contributions of their gut microbiome to the breakdown and assimilation of macronutrients and energy. To study how the gut microbiome contributes to the feeding ecology of a small-bodied primate, we analyzed the fecal microbiome composition and metabolome of 22 wild saddleback tamarins (adult body mass 360-390 g) in Northern Bolivia. Samples were analyzed using high-throughputIllumina sequencing of the 16 S rRNA gene V3-V5 regions, coupled with GC-MS metabolomic profiling. Our analysis revealed that the distal microbiome of Leontocebus weddelli is largely dominated by two main bacterial genera: Xylanibacter and Hallella (34.7 ± 14.7 and 22.6 ± 12.4%, respectively). A predictive analysis of functions likely carried out by bacteria in the tamarin gut demonstrated the dominance of membrane transport systems and carbohydrate metabolism as the predominant metabolic pathways. Moreover, given a fecal metabolome composed mainly of glucose, fructose, and lactic acid (21.7 ± 15.9%, 16.5 ± 10.7%, and 6.8 ± 5.5%, respectively), the processing of highly fermentable carbohydrates appears to play a central role in the nutritional ecology of these small-bodied primates. Finally, the results also show a potential influence of environmentally-derived bacteria in colonizing the tamarin gut. These results indicate high energetic turnover in the distal gut of Weddell's saddleback tamarin, likely influenced by dominant bacterial taxa that facilitate dietary dependence on highly digestible carbohydrates present in nectar, plant exudates, and ripe fruits.

Captive Common Marmosets (Callithrix jacchus) Are Colonized throughout Their Lives by a Community of Bifidobacterium Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches

“…Dominant genera included Bifidobacterium , Bacteroides , Collinsella , Prevotella , Alloprevotella , Parabacteroides , Phascolarctobacterium , Megamonas , Megasphaera , and Escherichia ( Table S1B ). In the majority of the animals, Bifidobacterium was the most abundant genus (range, 6 to 64%; median, 26%), and this characteristic has been reported in several other captive marmoset populations ( 31 , 40 – 43 ).…”

“…The marmoset is an emerging nonhuman primate model with several characteristics that make it a tractable model for studying the microbiome, and marmoset microbiomes are actively being studied in several different marmoset colonies and wild callitrichid populations ( 40 – 43 , 77 ). One of the most distinctive features shared by animals across multiple facilities, including the CRC, is the dominance of their microbiomes by species of Bifidobacterium ( 25 – 27 , 29 , 31 , 44 , 47 ) (see Fig.…”

The potential interplay between the glandular microbiome and scent marking behavior in owl monkeys (Aotus nancymaae)

“…The bacteria we identified are capable of producing some of the volatile compounds previously described in glandular secretions of A. nancymaae (MacDonald et al, 2008; Spence‐Aizenburg et al, 2018a). Many of the chemosignals in these secretions are volatile plant metabolite byproducts, alcohols, and short‐chain fatty acids (MacDonald et al, 2008) that could originate from their natural metabolome or diet (Garber et al, 2019). Given that the subcaudal glands rest directly under the anus, there is likely exposure to fecal flora.…”

Changes in the faecal microbiome of pied tamarins (Saguinus bicolor) associated with chronic, recurrent diarrhoea and weight loss

“…Species of Helicobacter are often reported to have been first isolated from callitrichids suffering from chronic colitis [ 49 , 53 ] and have been shown to cause enteritis in a mouse model [ 53 ]. However, studies of the intestinal microbiota of healthy adult callitrichids, both wild and captive, often yield a high relative abundance of Helicobacter [ 1 , 25 , 42 ]. Furthermore, to date no studies have identified a positive correlation between inflammatory lesions and the presence of Helicobacter [ 18 , 58 ].…”