The primate gut mycobiome-bacteriome interface is impacted by environmental and subsistence factors

Ashok Kumar Sharma, Sam Davison, Barbora Pafco, Jonathan B Clayton, Jessica M. Rothman, Matthew R. McLennan, Marie Cibot, Terence Fuh, Roman Vodicka, Carolyn Jost Robinson, Klara Petrzelkova, Andres Gomez

Research output: Contribution to journalArticlepeer-review

Abstract

The gut microbiome of primates is known to be influenced by both host genetic background and subsistence strategy. However, these inferences have been made mainly based on adaptations in bacterial composition - the bacteriome and have commonly overlooked the fungal fraction - the mycobiome. To further understand the factors that shape the gut mycobiome of primates and mycobiome-bacteriome interactions, we sequenced 16 S rRNA and ITS2 markers in fecal samples of four different nonhuman primate species and three human groups under different subsistence patterns (n = 149). The results show that gut mycobiome composition in primates is still largely unknown but highly plastic and weakly structured by primate phylogeny, compared with the bacteriome. We find significant gut mycobiome overlap between captive apes and human populations living under industrialized subsistence contexts; this is in contrast with contemporary hunter-gatherers and agriculturalists, who share more mycobiome traits with diverse wild-ranging nonhuman primates. In addition, mycobiome-bacteriome interactions were specific to each population, revealing that individual, lifestyle and intrinsic ecological factors affect structural correspondence, number, and kind of interactions between gut bacteria and fungi in primates. Our findings indicate a dominant effect of ecological niche, environmental factors, and diet over the phylogenetic background of the host, in shaping gut mycobiome composition and mycobiome-bacteriome interactions in primates.

Original languageEnglish (US)
Article number12
JournalNPJ biofilms and microbiomes
Volume8
Issue number1
DOIs
StatePublished - Dec 2022

Bibliographical note

Funding Information:
This study was supported with funds from the University of Minnesota-NIFA agricultural experimental station (project number MN-16-122s) and the Agricultural Research, Education, Extension and Technology Transfer Program (AGREETT), also from the University of Minnesota granted the Andres Gomez. The study was also supported by the Czech-American Scientific cooperation (INTER-ACTION, INTER-EXCELLENCE, LTAUSA18209) from the Ministry of Education, Youth and Sports of The Czech Republic. Klara Petrželková and Barbora Pafčo were supported by institutional support from the Institute of Vertebrate Biology, Czech Academy of Sciences (RVO:68081766). We thank the World Wildlife Fund and the Administration of Dzanga-Sangha Protected Areas in the Central African Republic for assistance with obtaining permits and for collaborative research support, and the Ministre de l’Education Nationale, de l’Alphabetisation, de l’Enseignement Superieur, et de la Recherche for granting research permission and sample transport permits. Special thanks to all the staff of the Primate Habituation Program for logistical support and assistance, and especially the BaAka trackers in the field. We thank Tom Sabiiti for helping collect samples at Bulindi, Uganda. We thank the Uganda Wildlife Authority and the Uganda National Council for Science and Technology for permission to conduct this research in Uganda. Simplicious Gessa and Pontius Ezuma provided logistical support in Uganda. We would like to express our most sincere gratitude to the staff of Como Zoo (St. Paul, MN, USA), and Ostrava Zoo (Czech Republic), particularly to Tami Murphy and Jana Pluhackova respectively; for providing assistance with sample collection from captive primates. This work was completed, in part, with resources from The Minnesota Supercomputing Institute (MSI).

Funding Information:
This study was supported with funds from the University of Minnesota-NIFA agricultural experimental station (project number MN-16-122s) and the Agricultural Research, Education, Extension and Technology Transfer Program (AGREETT), also from the University of Minnesota granted the Andres Gomez. The study was also supported by the Czech-American Scientific cooperation (INTER-ACTION, INTER-EXCELLENCE, LTAUSA18209) from the Ministry of Education, Youth and Sports of The Czech Republic. Klara Petrželková and Barbora Pafčo were supported by institutional support from the Institute of Vertebrate Biology, Czech Academy of Sciences (RVO:68081766). We thank the World Wildlife Fund and the Administration of Dzanga-Sangha Protected Areas in the Central African Republic for assistance with obtaining permits and for collaborative research support, and the Ministre de l’Education Nationale, de l’Alphabetisation, de l’Enseignement Superieur, et de la Recherche for granting research permission and sample transport permits. Special thanks to all the staff of the Primate Habituation Program for logistical support and assistance, and especially the BaAka trackers in the field. We thank Tom Sabiiti for helping collect samples at Bulindi, Uganda. We thank the Uganda Wildlife Authority and the Uganda National Council for Science and Technology for permission to conduct this research in Uganda. Simplicious Gessa and Pontius Ezuma provided logistical support in Uganda. We would like to express our most sincere gratitude to the staff of Como Zoo (St. Paul, MN, USA), and Ostrava Zoo (Czech Republic), particularly to Tami Murphy and Jana Pluhackova respectively; for providing assistance with sample collection from captive primates. This work was completed, in part, with resources from The Minnesota Supercomputing Institute (MSI).

Publisher Copyright:
© 2022, The Author(s).

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