Background

Anaerobic gut fungi (AGF, phylum Neocallimastigomycota) are a group of microscopic fungi that inhabit the digestive tracts of herbivorous animals. These fungi play a critical role in the breakdown of the complex plant material in their hosts' diets, making them of particular interest to the biofuel industry. However, their exclusive anaerobic lifestyle presents a challenge to lab cultivation and study, resulting in limited knowledge of their distribution, diversity, and community structure. Our group aimed to assess the diversity of anaerobic gut fungi on a global scale and evaluate some of the ecological and evolutionary factors that influence AGF communities within the gut.

Approach

Researchers at Oklahoma State University assembled and lead a team of scientists from 17 institutions, 12 countries, and 6 continents. Together we obtained 661 fecal samples from different types of animals, including ruminants, pseudoruminants, and hindgut fermenters as well as both wild and domesticated animals. These samples belonged to 34 species and 9 families, providing a diverse range of animals for analysis.

Discovery of 56 novel fungal genera

The newly discovered genera in this study more than doubles the known AGF diversity previously uncovered in the previous half-century. The abundance of these new genera was higher in specific types of animals, particularly in hosts that have never been investigated for AGF like the mara (a species of rodent) and the rhinoceros. Phylogenetic analysis placed the new genera within known families or suggested novel family-level lineages.

Host identity has the greatest influence on AGF communities.

Interestingly, we found a pattern where animals that are more genetically related to each other (for example goats and sheep or horses and mules) harbor fungal communities that are also more similar to each other than to the communities in less related hosts. Host identity appeared to be the most important factor in determining anaerobic gut fungal community structure. On the other hand, domestication, geography, and diet appear to play more minor roles in shaping communities.

 Fungal-host preferences are correlated with evolutionary dynamics.

By combining transcriptomics and fossil dating with the ecological insights obtained from our dataset, we uncovered an interesting evolutionary finding: many AGF genera appear to have coevolved with their preferred host. For example, the evolution of the horse family Equidae occurred at roughly the same time (55 million years ago) as the emergence of their preferred fungal genus Khoyollomyces. Similarly, foregut fermenters appear to harbor AGF genera that evolved more recently. This coincides with the emergence of the functional rumen about 40 million years ago). Therefore, it seems that AGF and their preferred hosts stayed together and evolved together. Such evolutionary-based associations appear to be retained today, meaning that studying present distribution patterns could be a valuable way to better understand the evolutionary relationships of the past.

Conclusion

The discovery of 56 novel genera sheds light on the global distribution of AGF and provides potential new candidates for biotechnological applications, such as the production of biofuels and other useful compounds. We are hopeful that these genera will be isolated in the lab, allowing scientists to learn more about their unique characteristics like the production of carbohydrate-active enzymes and antibiotics. The discovery that host identity shapes AGF communities more than factors like biogeography and domestication provides a better understanding of the mechanisms that underlie AGF evolution and their relationship with their hosts.