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Patterns of gut bacterial colonization in three primate species.

McKenney EA, Rodrigo A, Yoder AD - PLoS ONE (2015)

Bottom Line: Here, we show that colonization proceeds along different successional trajectories in developing infants from species with differing dietary regimes and ecological profiles: frugivorous (fruit-eating) Varecia variegata, generalist Lemur catta, and folivorous (leaf-eating) Propithecus coquereli.Our analyses reveal community membership and succession patterns consistent with previous studies of human infants, suggesting that lemurs may serve as a useful model of microbial ecology in the primate gut.Each lemur species exhibits distinct species-specific bacterial diversity signatures correlating to life stages and life history traits, implying that gut microbial community assembly primes developing infants at species-specific rates for their respective adult feeding strategies.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Duke University, Durham, North Carolina, United States of America.

ABSTRACT
Host fitness is impacted by trillions of bacteria in the gastrointestinal tract that facilitate development and are inextricably tied to life history. During development, microbial colonization primes the gut metabolism and physiology, thereby setting the stage for adult nutrition and health. However, the ecological rules governing microbial succession are poorly understood. In this study, we examined the relationship between host lineage, captive diet, and life stage and gut microbiota characteristics in three primate species (infraorder, Lemuriformes). Fecal samples were collected from captive lemur mothers and their infants, from birth to weaning. Microbial DNA was extracted and the v4 region of 16S rDNA was sequenced on the Illumina platform using protocols from the Earth Microbiome Project. Here, we show that colonization proceeds along different successional trajectories in developing infants from species with differing dietary regimes and ecological profiles: frugivorous (fruit-eating) Varecia variegata, generalist Lemur catta, and folivorous (leaf-eating) Propithecus coquereli. Our analyses reveal community membership and succession patterns consistent with previous studies of human infants, suggesting that lemurs may serve as a useful model of microbial ecology in the primate gut. Each lemur species exhibits distinct species-specific bacterial diversity signatures correlating to life stages and life history traits, implying that gut microbial community assembly primes developing infants at species-specific rates for their respective adult feeding strategies.

No MeSH data available.


Related in: MedlinePlus

GIT diagrams [49] and feeding strategies for (A) Varecia variegata, (B) Lemur catta, and (C) Propithecus sifaka, projected onto a phylogenetic tree [28].H: If the succession process in lemurs is similar to that described in humans, then microbial diversity should be lowest in samples from birth and increase with age until weaning, with decreasing intraspecific variability as individuals approach adulthood and their GMs approach the climax community. We refer to this as the “life stage” hypothesis.
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pone.0124618.g001: GIT diagrams [49] and feeding strategies for (A) Varecia variegata, (B) Lemur catta, and (C) Propithecus sifaka, projected onto a phylogenetic tree [28].H: If the succession process in lemurs is similar to that described in humans, then microbial diversity should be lowest in samples from birth and increase with age until weaning, with decreasing intraspecific variability as individuals approach adulthood and their GMs approach the climax community. We refer to this as the “life stage” hypothesis.

Mentions: We examine GM assembly in Varecia variegata, Lemur catta, and Propithecus coquereli (see Fig 1). Estimated divergence times are ~32mya for the divergence of V. variegata and L. catta and ~ 42mya for the divergence of P. coquereli from the Lemuridae (V. variegata, L. catta; [28]). Each species has evolved unique and differing life histories, ecological constraints, and distinct GIT morphologies. In our study system, however, V. variegata and L. catta are fed similar diets in captivity. We analyzed bacterial 16S rDNA reads amplified from fecal samples collected from positively identified individuals to resolve GM membership at the genus level and to compare succession patterns between individuals and across species. By controlling certain environmental variables such as dietary intake and recording relevant long-term metadata, we investigate the contributions of host life stage, captive diet, and GIT morphology to the host-gut microbial relationship and the process of community assembly. We use summary statistics of taxonomic richness, membership, and diversity to test the following hypotheses.


Patterns of gut bacterial colonization in three primate species.

McKenney EA, Rodrigo A, Yoder AD - PLoS ONE (2015)

GIT diagrams [49] and feeding strategies for (A) Varecia variegata, (B) Lemur catta, and (C) Propithecus sifaka, projected onto a phylogenetic tree [28].H: If the succession process in lemurs is similar to that described in humans, then microbial diversity should be lowest in samples from birth and increase with age until weaning, with decreasing intraspecific variability as individuals approach adulthood and their GMs approach the climax community. We refer to this as the “life stage” hypothesis.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4430486&req=5

pone.0124618.g001: GIT diagrams [49] and feeding strategies for (A) Varecia variegata, (B) Lemur catta, and (C) Propithecus sifaka, projected onto a phylogenetic tree [28].H: If the succession process in lemurs is similar to that described in humans, then microbial diversity should be lowest in samples from birth and increase with age until weaning, with decreasing intraspecific variability as individuals approach adulthood and their GMs approach the climax community. We refer to this as the “life stage” hypothesis.
Mentions: We examine GM assembly in Varecia variegata, Lemur catta, and Propithecus coquereli (see Fig 1). Estimated divergence times are ~32mya for the divergence of V. variegata and L. catta and ~ 42mya for the divergence of P. coquereli from the Lemuridae (V. variegata, L. catta; [28]). Each species has evolved unique and differing life histories, ecological constraints, and distinct GIT morphologies. In our study system, however, V. variegata and L. catta are fed similar diets in captivity. We analyzed bacterial 16S rDNA reads amplified from fecal samples collected from positively identified individuals to resolve GM membership at the genus level and to compare succession patterns between individuals and across species. By controlling certain environmental variables such as dietary intake and recording relevant long-term metadata, we investigate the contributions of host life stage, captive diet, and GIT morphology to the host-gut microbial relationship and the process of community assembly. We use summary statistics of taxonomic richness, membership, and diversity to test the following hypotheses.

Bottom Line: Here, we show that colonization proceeds along different successional trajectories in developing infants from species with differing dietary regimes and ecological profiles: frugivorous (fruit-eating) Varecia variegata, generalist Lemur catta, and folivorous (leaf-eating) Propithecus coquereli.Our analyses reveal community membership and succession patterns consistent with previous studies of human infants, suggesting that lemurs may serve as a useful model of microbial ecology in the primate gut.Each lemur species exhibits distinct species-specific bacterial diversity signatures correlating to life stages and life history traits, implying that gut microbial community assembly primes developing infants at species-specific rates for their respective adult feeding strategies.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Duke University, Durham, North Carolina, United States of America.

ABSTRACT
Host fitness is impacted by trillions of bacteria in the gastrointestinal tract that facilitate development and are inextricably tied to life history. During development, microbial colonization primes the gut metabolism and physiology, thereby setting the stage for adult nutrition and health. However, the ecological rules governing microbial succession are poorly understood. In this study, we examined the relationship between host lineage, captive diet, and life stage and gut microbiota characteristics in three primate species (infraorder, Lemuriformes). Fecal samples were collected from captive lemur mothers and their infants, from birth to weaning. Microbial DNA was extracted and the v4 region of 16S rDNA was sequenced on the Illumina platform using protocols from the Earth Microbiome Project. Here, we show that colonization proceeds along different successional trajectories in developing infants from species with differing dietary regimes and ecological profiles: frugivorous (fruit-eating) Varecia variegata, generalist Lemur catta, and folivorous (leaf-eating) Propithecus coquereli. Our analyses reveal community membership and succession patterns consistent with previous studies of human infants, suggesting that lemurs may serve as a useful model of microbial ecology in the primate gut. Each lemur species exhibits distinct species-specific bacterial diversity signatures correlating to life stages and life history traits, implying that gut microbial community assembly primes developing infants at species-specific rates for their respective adult feeding strategies.

No MeSH data available.


Related in: MedlinePlus