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1. Patterns and determinants of the global herbivorous mycobiome

   Casey H. Meili, Adrienne L. (April 2023, Nature communications)

   In spite of their indispensable role in host nutrition, the anaerobic gut fungal (AGF) component of the herbivorous gut microbiome remains poorly characterized. To examine global patterns and determinants of AGF diversity, we generated and analyzed an amplicon dataset from 661 fecal samples from 34 animal species, 9 families, and 6 continents. We identified 56 novel genera, greatly expanding AGF diversity beyond current estimates. Both stochastic (homogenizing dispersal and drift) and deterministic (homogenizing selection) processes played an integral role in shaping AGF communities, with a higher level of stochasticity observed in foregut fermenters. Community structure analysis revealed a distinct pattern of phylosymbiosis, where host-associated (animal species, family, and gut type), rather than ecological (domestication status and biogeography) factors predominantly shaped the community. Hindgut fermenters exhibited stronger and more specific fungal-host associations, compared to broader mostly non-host specific associations in foregut fermenters. Transcriptomics-enabled phylogenomic and molecular clock analyses of 52 strains from 14 genera indicated that most genera with preferences for hindgut hosts evolved earlier (44-58 Mya), while those with preferences for foregut hosts evolved more recently (22-32 Mya). This pattern is in agreement with the sole dependence of herbivores on hindgut fermentation past the Cretaceous-Paleogene (K-Pg) extinction event through the Paleocene and Eocene, and the later rapid evolution of animals employing foregut fermentation strategy during the early Miocene. Only a few AGF genera deviated from this pattern of co-evolutionary phylosymbiosis, by exhibiting preferences suggestive of post-evolutionary environmental filtering. Our results greatly expand the documented scope of AGF diversity and provide an ecologically and evolutionary-grounded model to explain the observed patterns of AGF diversity in extant animal hosts. 

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2. Temporal progression of anaerobic fungal communities in dairy calves from birth to maturity

   https://doi.org/10.1111/1462-2920.16443  

   Jones, Adrienne_L; Clayborn, Jordan; Pribil, Elizabeth; Foote, Andrew_P; Montogomery, Dagan; Elshahed, Mostafa_S; Youssef, Noha_H (June 2023, Environmental Microbiology)

   Abstract Establishment of microbial communities in neonatal calves is vital for their growth and overall health. While this process has received considerable attention for bacteria, our knowledge on temporal progression of anaerobic gut fungi (AGF) in calves is lacking. Here, we examined AGF communities in faecal samples from six dairy cattle collected at 24 different time points during the pre‐weaning (days 1–48), weaning (days 48–60), and post‐weaning (days 60–360) phases. Quantitative polymerase chain reaction indicated that AGF colonisation occurs within 24 h after birth, with loads slowly increasing during pre‐weaning and weaning, then drastically increasing post‐weaning. Culture‐independent amplicon surveys identified higher alpha diversity during pre‐weaning/weaning, compared to post‐weaning. AGF community structure underwent a drastic shift post‐weaning, from a community enriched in genera commonly encountered in hindgut fermenters to one enriched in genera commonly encountered in adult ruminants.Comparison of AGF community between calves day 1 post‐birth and their mothers suggest a major role for maternal transmission, with additional input from cohabitating subjects. This distinct pattern of AGF progression could best be understood in‐light of their narrower niche preferences, metabolic specialisation, and physiological optima compared to bacteria, hence eliciting a unique response to changes in feeding pattern and associated structural GIT development during maturation. 

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3. Anaerobic fungi in the tortoise alimentary tract illuminate early stages of host-fungal symbiosis and Neocallimastigomycota evolution

   https://doi.org/10.1038/s41467-024-47047-4  

   Pratt, Carrie J.; Meili, Casey H.; Jones, Adrienne L.; Jackson, Darian K.; England, Emma E.; Wang, Yan; Hartson, Steve; Rogers, Janet; Elshahed, Mostafa S.; Youssef, Noha H. (March 2024, Nature Communications)

   Abstract Anaerobic gut fungi (AGF,Neocallimastigomycota) reside in the alimentary tract of herbivores. While their presence in mammals is well documented, evidence for their occurrence in non-mammalian hosts is currently sparse. Culture-independent surveys of AGF in tortoises identified a unique community, with three novel deep-branching genera representing >90% of sequences in most samples. Representatives of all genera were successfully isolated under strict anaerobic conditions. Transcriptomics-enabled phylogenomic and molecular dating analyses indicated an ancient, deep-branching position in the AGF tree for these genera, with an evolutionary divergence time estimate of 104-112 million years ago (Mya). Such estimates push the establishment of animal-Neocallimastigomycotasymbiosis from the late to the early Cretaceous. Further, tortoise-associated isolates (T-AGF) exhibited limited capacity for plant polysaccharides metabolism and lacked genes encoding several carbohydrate-active enzyme (CAZyme) families. Finally, we demonstrate that the observed curtailed degradation capacities and reduced CAZyme repertoire is driven by the paucity of horizontal gene transfer (HGT) in T-AGF genomes, compared to their mammalian counterparts. This reduced capacity was reflected in an altered cellulosomal production capacity in T-AGF. Our findings provide insights into the phylogenetic diversity, ecological distribution, evolutionary history, evolution of fungal-host nutritional symbiosis, and dynamics of genes acquisition inNeocallimastigomycota. 

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4. Diversity and community structure of anaerobic gut fungi in the rumen of wild and domesticated herbivores

   https://doi.org/10.1128/aem.01492-23  

   Meili, Casey H; TagElDein, Moustafa A; Jones, Adrienne L; Moon, Christina D; Andrews, Catherine; Kirk, Michelle R; Janssen, Peter H; J_Yeoman, Carl; Grace, Savannah; Borgogna, Joanna-Lynn C; et al (February 2024, Applied and Environmental Microbiology)

   Reguera, Gemma (Ed.)

   ABSTRACT The rumen houses a diverse community that plays a major role in the digestion process in ruminants. Anaerobic gut fungi (AGF) are key contributors to plant digestion in the rumen. Here, we present a global amplicon-based survey of the rumen AGF mycobiome by examining 206 samples from 15 animal species, 15 countries, and 6 continents. The rumen AGF mycobiome was highly diverse, with 81 out of 88 currently recognized AGF genera or candidate genera identified. However, only six genera (Neocallimastix, Orpinomyces, Caecomyces, Cyllamyces,NY9, andPiromyces) were present at >4% relative abundance. AGF diversity was higher in members of the familiesAntilocapridaeandCervidaecompared toBovidae. Community structure analysis identified a pattern of phylosymbiosis, where host family (10% of total variance) and species (13.5%) partially explained the rumen mycobiome composition. As well, diet composition (9%–19%), domestication (11.14%), and biogeography (14.1%) also partially explained AGF community structure; although sampling limitation, geographic range restrictions, and direct association between different factors hindered accurate elucidation of the relative contribution of each factor. Pairwise comparison of rumen and fecal samples obtained from the same subject (n= 13) demonstrated greater diversity and inter-sample variability in rumen versus fecal samples. The generaNeocallimastixandOrpinomyceswere present in higher abundance in rumen samples, whileCyllamycesandCaecomyceswere enriched in fecal samples. Comparative analysis of global rumen and feces data sets revealed a similar pattern. Our results provide a global view of AGF community in the rumen and identify patterns of AGF variability between rumen and feces in herbivores Gastrointestinal (GI) tract. IMPORTANCERuminants are highly successful and economically important mammalian suborder. Ruminants are herbivores that digest plant material with the aid of microorganisms residing in their GI tract. In ruminants, the rumen compartment represents the most important location where microbially mediated plant digestion occurs, and is known to house a bewildering array of microbial diversity. An important component of the rumen microbiome is the anaerobic gut fungi (AGF), members of the phylumNeocallimastigomycota. So far, studies examining AGF diversity have mostly employed fecal samples, and little is currently known regarding the identity of AGF residing in the rumen compartment, factors that impact the observed patterns of diversity and community structure of AGF in the rumen, and how AGF communities in the rumen compare to AGF communities in feces. Here, we examined the rumen AGF diversity using an amplicon-based survey targeting a wide range of wild and domesticated ruminants (n= 206, 15 different animal species) obtained from 15 different countries. Our results demonstrate that while highly diverse, no new AGF genera were identified in the rumen mycobiome samples examined. Our analysis also indicate that animal host phylogeny, diet, biogeography, and domestication status could play a role in shaping AGF community structure. Finally, we demonstrate that a greater level of diversity and higher inter-sample variability was observed in rumen compared to fecal samples, with two genera (NeocallimastixandOrpinomyces) present in higher abundance in rumen samples, and two others (CyllamycesandCaecomyces) enriched in fecal samples. Our results provide a global view of the identity, diversity, and community structure of AGF in ruminants, elucidate factors impacting diversity and community structure of the rumen mycobiome, and identify patterns of AGF community variability between the rumen and feces in the herbivorous GI tract. 

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5. CH4/CO2 Ratios and Carbon Isotope Enrichment Between Diet and Breath in Herbivorous Mammals

   https://doi.org/10.3389/fevo.2021.638568  

   Cerling, Thure E.; Bernasconi, Stefano M.; Hofstetter, Lino S.; Jaggi, Madalina; Wyss, Fabia; Rudolf von Rohr, Claudia; Clauss, Marcus (May 2021, Frontiers in Ecology and Evolution)

   Breath and diet samples were collected from 29 taxa of animals at the Zurich and Basel Zoos to characterize the carbon isotope enrichment between breath and diet. Diet samples were measured for δ 13 C and breath samples for CH 4 /CO 2 ratios and for the respired component of δ 13 C using the Keeling plot approach. Different digestive physiologies included coprophagous and non-coprophagous hindgut fermenters, and non-ruminant and ruminant foregut fermenters. Isotope enrichments from diet to breath were 0.8 ± 0.9‰, 3.5 ± 0.8‰, 2.3 ± 0.4‰, and 4.1 ± 1.0‰, respectively. CH 4 /CO 2 ratios were strongly correlated with isotope enrichments for both hindgut and foregut digestive strategies, although CH 4 production was not the sole reason for isotope enrichment. Average CH 4 /CO 2 ratios per taxon ranged over several orders of magnitude from 10 –5 to 10 –1 . The isotope enrichment values for diet-breath can be used to further estimate the isotope enrichment from diet-enamel because Passey et al. (2005b) found a nearly constant isotope enrichment for breath-enamel for diverse mammalian taxa. The understanding of isotope enrichment factors from diet to breath and diet to enamel will have important applications in the field of animal physiology, and possibly also for wildlife ecology and paleontology. 

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