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ARS Home » Midwest Area » Madison, Wisconsin » U.S. Dairy Forage Research Center » Cell Wall Biology and Utilization Research » Research » Publications at this Location » Publication #309946
Title: Diet specialization selects for an unusual and simplified gut microbiota in two- and three-toed sloths

Author
item DILL-MCFARLAND, KIMBERLEY - University Of Wisconsin
item Weimer, Paul
item PAULI, JONATHAN - University Of Wisconsin
item PEERY, M - University Of Wisconsin
item SUEN, GARRET - University Of Wisconsin

Submitted to: Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/12/2015
Publication Date: 5/6/2016
Publication URL: https://handle.nal.usda.gov/10113/62509
Citation: Dill-McFarland, K., Weimer, P.J., Pauli, J.N., Peery, M.Z., Suen, G. 2016. Diet specialization selects for an unusual and simplified gut microbiota in two- and three-toed sloths. Environmental Microbiology. 18(5):1391-1402.

Interpretive Summary: Three-toed sloths are one of the few tree-dwelling mammals that only rarely descend from their trees, and therefore, their diet consists almost exclusively of tree leaves. They also have a foregut containing microorganisms that are thought to aid in food digestion. Because of their specialized fibrous diet and their very slow rate of digestive passage, their foreguts could potentially harbor unusual bacteria capable of degrading plant biomass; these bacteria may have industrial use in biomass utilization. We used DNA sequencing to determine that three-toed sloths have a microbial community very different from the communities in two-toed sloths, which have a much less specialized diet. In addition, the foregut of three-toed sloths contains one of two acids produced by microbial fermentation (lactic acid or formic acid) that are not found in quantity in two-toed sloths, or in other mammalian species. This suggests that the foregut community members have unique metabolic characteristics. These data indicated that three-toed sloths contain a unique microbial community whose members should be investigated further for their fiber-degrading properties.

Technical Abstract: Herbivores are reliant on associated gut microorganisms for the conversion of indigestible dietary plant materials into accessible nutrients. Arboreal folivores are especially dependent on this symbiosis as their exploitation of treetop leaves places constraints on body size, and therefore, food intake. We postulated that strict arboreal folivores like three-toed sloths possess a specialized gut microbiota relative to that of more generalist foragers like two-toed sloths. We used next-generation sequencing to identify the bacteria present in the digesta and feces of wild two- (Choloepus hoffmanni) and three-toed sloths (Bradypus variegatus), and correlated these communities with diet and digesta short-chain organic acids (SCOAs). We showed that unlike most herbivores, sloths harbor gut communities dominated by phyla Proteobacteria and Firmicutes, and that digesta-associated communities (as well as SCOA profiles) differ between the two sloth species. Specifically, three-toed sloths consuming a low-diversity diet of mostly Cecropia leaves had digesta dominated by a single SCOA, either formate or lactate, and a highly conserved, low-diversity bacterial community. In contrast, two-toed animals consuming a more diverse diet had correspondingly more diverse bacterial communities and SCOA profiles. Compared to two-toed sloths, three-toed digesta had more highly abundant families (Neisseriaceae, Porphyromonadaceae, and Veillonellaceae) with a single Neisseria species making up roughly one-quarter of the community. Our results suggested that the limited diet of three-toed sloths selects for a conserved microbial community with narrow SCOA production abilities, and that the sloth lifestyle, particularly that of three-toed species, selects for gut communities dissimilar to those in other herbivores.