Anaerobic Fungi in Gorilla (Gorilla gorilla gorilla) Feces: an Adaptation to a High-Fiber Diet?
Many studies have demonstrated the importance of symbiotic microbial communities for the host with beneficial effects for nutrition, development, and the immune system. The majority of these studies have focused on bacteria residing in the gastrointestinal tract, while the fungal community has often been neglected. Gut anaerobic fungi of the class Neocallimastigomycetes are a vital part of the intestinal microbiome in many herbivorous animals and their exceptional abilities to degrade indigestible plant material means that they contribute significantly to fermentative processes in the enteric tract. Gorillas rely on a highly fibrous diet and depend on fermentative microorganisms to meet their daily energetic demands. To assess whether Neocallimastigomycetes occur in gorillas we analyzed 12 fecal samples from wild Western lowland gorillas (Gorilla gorilla gorilla) from Dzanga–Sangha Protected Areas, Central African Republic, and subjected potential anaerobic fungi sequences to phylogenetic analysis. The clone library contained ITS1 fragments that we related to 45 different fungi clones. Of these, 12 gastrointestinal fungi in gorillas are related to anaerobic fungi and our phylogenetic analyses support their assignment to the class Neocallimastigomycetes. As anaerobic fungi play a pivotal role in plant fiber degradation in the herbivore gut, gorillas might benefit from harboring these particular fungi with regard to their nutritional status. Future studies should investigate whether Neocallimastigomycetes are also found in other nonhuman primates with high fiber intake, which would also benefit from having such highly efficient fermentative microbes.
KeywordsDiet Gorillas Gut microbiome Neocallimastigales
We are grateful to the government of the Central African Republic as well as the Ministre de l’Education Nationale, de l’Alphabetisation, de l’Enseignement Superieur, et de la Recherche for granting permission to conduct our research within the Dzanga–Sangha Protected Areas, Central African Republic. We further thank the World Wildlife Fund and the Primate Habituation Project for administrative and logistical support on side. Last, we are very grateful to the associate editor and the two anonymous reviewers for their valuable comments. The project was supported by the Leakey Foundation (D. Schulz, K. J. Petrzelkova, K. Fliegerová), by the project CEITEC (Central European Institute of Technology, CZ.1·05/1·1·00/02·0068) from the European Regional Development Fund (D. Modry), by project CZ.02.1.01/0.0/0.0/15_003/0000460 OP RDE (K. Fliegerová), by institutional support of Institute of Vertebrate Biology, Czech Academy of Sciences (RVO: 68081766) (K. J. Petrzelkova) and cofinanced from the European Social Fund and the state budget of the Czech Republic (CZ.1·07/2·3·00/20·0300) (D. Schulz, I. Profousova-Psenkova, M. A. Qablan, D. Modry, K. J. Petrzelkova).
- Ariyawansa, H. A., Hyde, K. D., Jayasiri, S. C., Buyck, B., Chethana, K. W. T., et al. (2015). Fungal diversity notes 111–252: Taxonomic and phylogenetic contributions to fungal taxa. Fungal Diversity, 75(1), 27–274.Google Scholar
- Cheng, Y. F., Edwards, J. E., Allison, G. G., Zhu, W.-Y., & Theodorou, M. K. (2009). Diversity and activity of enriched ruminal cultures of anaerobic fungi and methanogens grown together on lignocellulose in consecutive batch culture. Bioresource Technology, 100(20), 4821–4828.CrossRefPubMedGoogle Scholar
- Conklin-Brittain, N. L., Knott, C. D., & Wrangham, R. W. (2006). Energy intake by wild chimpanzees and orangutans: Methodological considerations and a preliminary comparison. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 445–471). Cambridge: Cambridge University Press.Google Scholar
- Doran-Sheehy, D., Mongo, P., Lodwick, J., & Conklin-Brittain, N. l. (2009). Male and female western gorilla diet: Preferred foods, use of fallback resources, and implications for ape versus old world monkey foraging strategies. American Journal of Physical Anthropology, 140(4), 727–738.CrossRefPubMedGoogle Scholar
- Edwards, J. E., Forster, R. J., Callaghan, T. M., Dollhofer, V., Dagar, S. S., et al. (2017). PCR and omics based techniques to study the diversity, ecology and biology of anaerobic fungi: Insights, challenges and opportunities. Frontiers in Microbiology, 8, doi: https://doi.org/10.3389/fmicb.2017.01657
- Edwards, J. E., Kingston-Smith, A. H., Jimenez, H. R., Huws, S. A., Skøt, K. P., et al. (2008). Dynamics of initial colonization of nonconserved perennial ryegrass by anaerobic fungi in the bovine rumen: Initial colonization of forage by ruminal anaerobic fungi. FEMS Microbiology Ecology, 66(3), 537–545.CrossRefPubMedGoogle Scholar
- Goudarzi, A. M., Chamani, M., Maheri-Sis, N., Afshar, M. A., & Salamatdoost-Nobar, R. (2015). Genetic diversity of gastrointestinal tract fungi in buffalo by molecular methods on the basis of polymerase chain reaction. Biological Forum, 7(1), 20–25.Google Scholar
- Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar
- Mackie, R. I., Rycyk, M., Ruemmler, R. L., Aminov, R. I., & Wikelski, M. (2004). Biochemical and microbiological evidence for fermentative digestion in free-living land iguanas (Conolophus pallidus) and marine iguanas (Amblyrhynchus cristatus) on the Galapagos archipelago. Physiological and Biochemical Zoology, 77(1), 127–138.CrossRefPubMedGoogle Scholar
- Masi, S. (2007). Seasonal influence on foraging strategies, activity and energy budgets of western lowland gorillas (Gorilla gorilla gorilla) in Bai Hokou, Central African Republic. PhD thesis, La Sapienza - Università di Roma.Google Scholar
- Orpin, C. G. (1975). Studies on the rumen flagellate Neocallimastix frontalis. Microbiology, 91(2), 249–262.Google Scholar
- Remis, M. J. (2003). Are gorillas vacuum cleaners of the forest floor? The roles of gorilla body size, habitat and food preferences on dietary flexibility and nutrition. In A. B. Taylor & M. L. Goldsmith (Eds.), Gorilla biology: A multidisciplinary perspective (pp. 385–404). Cambridge: Cambridge University Press.Google Scholar
- Song, S. J., Amir, A., Metcalf, J. L., Amato, K. R., Xu, Z. Z., et al. (2016). Preservation methods differ in fecal microbiome stability, affecting suitability for field studies. mSystems, 1(3), e00021-16, e00021, e00016.Google Scholar
- Tuckwell, D. S., Nicholson, M. J., McSweeney, C. S., Theodorou, M. K., & Brookman, J. L. (2005). The rapid assignment of ruminal fungi to presumptive genera using ITS1 and ITS2 RNA secondary structures to produce group-specific fingerprints. Microbiology, 151(5), 1557–1567.CrossRefPubMedGoogle Scholar
- Ungar, P. S. (2007). Dental functional morphology: The known, the unknown and the unknowable. In P. S. Ungar (Ed.), Evolution of the human diet: The known, the unknown, and the unknowable (pp. 39–55). Oxford: Oxford University Press.Google Scholar