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

Paul A. Garber, Elizabeth K. Mallott, Leila M. Porter, Andres Gomez

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

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-throughput Illumina 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.

Original languageEnglish (US)
Article numbere23003
JournalAmerican journal of primatology
Volume81
Issue number10-11
DOIs
StatePublished - Oct 1 2019

Bibliographical note

Funding Information:
Thank you to Ripan Malhi for allowing us to use his lab facilities and for his methodological expertise. At the Roy J. Carver Biotechnology Center at the University of Illinois Urbana‐Champaign, we would like to thank Mark Band and Chris Wright for their help with next‐generation sequencing and Alex Ulanov for his help with the metabolite analysis. We would also like to thank Chris Fields and Kiran Donthu at the High‐Performance Biological Computing facility at the University of Illinois Urbana‐Champaign. PAG wishes to thank Chrissie, Sara, and Jenni for their inspiration, love, and support. We would like to thank Antonio Salazar and Lucero Hernani Lineros for their help with data collection and the Leakey Foundation for their funding support. We also thank the Colección Boliviana de Fauna, Bolivia for their help securing permits for this research and for the Minesterio de Medio Ambiente, Bolivia for granting permission to conduct this project. AG wishes to thank Bryan White at the University of Illinois Urbana‐Champaign and Steve Leigh at University of Colorado, and Anna and Martina for their love and support. AG was supported with funds of the University of Minnesota's Agricultural Research, Education, Extension and Technology Transfer Program (AGREETT). PAG was supported by research funds provided by the University of Illinois.

Funding Information:
Thank you to Ripan Malhi for allowing us to use his lab facilities and for his methodological expertise. At the Roy J. Carver Biotechnology Center at the University of Illinois Urbana-Champaign, we would like to thank Mark Band and Chris Wright for their help with next-generation sequencing and Alex Ulanov for his help with the metabolite analysis. We would also like to thank Chris Fields and Kiran Donthu at the High-Performance Biological Computing facility at the University of Illinois Urbana-Champaign. PAG wishes to thank Chrissie, Sara, and Jenni for their inspiration, love, and support. We would like to thank Antonio Salazar and Lucero Hernani Lineros for their help with data collection and the Leakey Foundation for their funding support. We also thank the Colección Boliviana de Fauna, Bolivia for their help securing permits for this research and for the Minesterio de Medio Ambiente, Bolivia for granting permission to conduct this project. AG wishes to thank Bryan White at the University of Illinois Urbana-Champaign and Steve Leigh at University of Colorado, and Anna and Martina for their love and support. AG was supported with funds of the University of Minnesota's Agricultural Research, Education, Extension and Technology Transfer Program (AGREETT). PAG was supported by research funds provided by the University of Illinois.

Publisher Copyright:
© 2019 Wiley Periodicals, Inc.

Keywords

  • Leontocebus weddelli
  • gut microbiome
  • metabolome

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