Diet specialization selects for an unusual and simplified gut microbiota in two- and three-toed sloths

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 int...

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Veröffentlicht in:Environmental microbiology Jg. 18; H. 5; S. 1391 - 1402
Hauptverfasser: Dill-McFarland, Kimberly A., Weimer, Paul J., Pauli, Jonathan N., Peery, M. Zachariah, Suen, Garret
Format: Journal Article
Sprache:Englisch
Veröffentlicht: England Blackwell Publishing Ltd 01.05.2016
Wiley Subscription Services, Inc
Schlagworte:
Animals
bacteria
Bacteria - classification
Bacteria - isolation & purification
bacterial communities
Body size
Bradypus variegatus
Cecropia
Choloepus hoffmanni
Diet
digesta
feces
Feeding Behavior
Female
Firmicutes
food intake
foregut
formates
Gastrointestinal Microbiome
habitat destruction
Habitat loss
Herbivores
Herbivory
high-throughput nucleotide sequencing
intestinal microorganisms
lactic acid
leaves
lifestyle
Male
mammals
Microbial activity
Microorganisms
Neisseria
nutrients
Organic acids
Proteobacteria
Sloths - microbiology
Symbiosis
tree crown
trees
ISSN:1462-2912, 1462-2920, 1462-2920
Online-Zugang:Volltext
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Zusammenfassung: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.
Bibliographie:http://handle.nal.usda.gov/10113/62509
http://dx.doi.org/10.1111/1462-2920.13022
istex:7BB4BF063F2121056DB7891B5CE9F7E76876F0AD
ArticleID:EMI13022
Fig. S1. Nearest neighbour rarefaction curves of 97 % OTUs in (A) digesta and (B) feces. Two-toed: grey; three-toed: black.Fig. S2. Total bacterial communities of digesta and feces differ in two- and three-toed sloths. Non-metric multidimensional scaling (nMDS) plot of gut-associated bacterial community structure (Bray-Curtis index) in two- (∆) and three-toed (□) sloths. Digesta (■▲) and feces (□∆). Ellipses represent 95 % confidence intervals.Fig. S3. Standard curves for acetate, propionate, butyrate and valerate concentrations determined by HPLC. Standards at 0, 10, 50, 100, 200 and 300 nM (except for valerate which is non-linear after 200 nM) were run for each acid. Each standard was run twice and the best fit linear regression was determined for each acid.Table S1. Metadata as well as coverage and diversity metrics of all digesta and feces samples from two- and three-toed sloths.Table S2. OTU counts and classifications in all samples (no subsampling).Table S3. P values associated with PERMANOVA, ANOSIM and ANOVA.Table S4. Similarity percentage (SIMPER) analyses.Table S5. Consensus sequence and top blast results* for full-length OTU3 and OTU4 sequences.Table S6. Relative abundance of OTUs shared by two- and/or three-toed sloths.Table S7. All tree observations.Table S8. SCOAs detected in sloth digesta in mM (molar fraction, %).Table S9. Linear correlations between contributing OTUs (SIMPER) and trees or SCOAs.Appendix S1. Sequence data processing code in mothur.
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ISSN:1462-2912
1462-2920
1462-2920
DOI:10.1111/1462-2920.13022