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1. Gut microbiome composition of wild western lowland gorillas is associated with individual age and sex factors

   https://doi.org/10.1002/ajpa.23842  

   Pafčo, Barbora ; Sharma, Ashok K. ; Petrželková, Klára J. ; Vlčková, Klára ; Todd, Angelique ; Yeoman, Carl J. ; Wilson, Brenda A. ; Stumpf, Rebecca ; White, Bryan A. ; Nelson, Karen E. ; et al ( April 2019 , American Journal of Physical Anthropology)

   Environmental and ecological factors, such as geographic range, anthropogenic pressure, group identity, and feeding behavior are known to influence the gastrointestinal microbiomes of great apes. However, the influence of individual host traits such as age and sex, given specific dietary and social constraints, has been less studied. The objective of this investigation was to determine the associations between an individual's age and sex on the diversity and composition of the gut microbiome in wild western lowland gorillas.

   Publicly available 16S rRNA data generated from fecal samples of different groups ofGorilla gorillagorillain the Central African Republic were downloaded and bioinformatically processed. The groups analyzed included habituated, partially habituated and unhabituated gorillas, sampled during low fruit (dry,n = 28) and high fruit (wet,n = 82) seasons. Microbial community analyses (alpha and beta diversity and analyses of discriminant taxa), in tandem with network‐wide approaches, were used to (a) mine for specific age and sex based differences in gut bacterial community composition and to (b) asses for gut community modularity and bacterial taxa with potential functional roles, in the context of seasonal food variation, and social group affiliation.

   Both age and sex significantly influenced gut microbiome diversity and composition in wild western lowland gorillas. However, the largest differences were observed between infants and adults in habituated groups and between adults and immature gorillas within all groups, and across dry and wet seasons. Specifically, although adults always showed greater bacterial richness than infants and immature gorillas, network‐wide analyses showed higher microbial community complexity and modularity in the infant gorilla gut. Sex‐based microbiome differences were not evident among adults, being only detected among immature gorillas.

   The results presented point to a dynamic gut microbiome inGorillaspp., associated with ontogeny and individual development. Of note, the gut microbiomes of breastfeeding infants seemed to reflect early exposure to complex, herbaceous vegetation. Whether increased compositional complexity of the infant gorilla gut microbiome is an adaptive response to an energy‐limited diet and an underdeveloped gut needs to be further tested. Overall, age and sex based gut microbiome differences, as shown here, maybe mainly attributed to access to specific feeding sources, and social interactions between individuals within groups.

    

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2. Taxonomic, Genomic, and Functional Variation in the Gut Microbiomes of Wild Spotted Hyenas Across 2 Decades of Study

   https://doi.org/10.1128/msystems.00965-22  

   Rojas, Connie A. ; Holekamp, Kay E. ; Viladomat Jasso, Mariette ; Souza, Valeria ; Eisen, Jonathan A. ; Theis, Kevin R. ( January 2022 , mSystems)

   Hird, Sarah M. (Ed.)

   The gut microbiome provides vital functions for mammalian hosts, yet research on its variability and function across adult life spans and multiple generations is limited in large mammalian carnivores. Here, we used 16S rRNA gene and metagenomic high-throughput sequencing to profile the bacterial taxonomic composition, genomic diversity, and metabolic function of fecal samples collected from 12 wild spotted hyenas ( Crocuta crocuta ) residing in the Masai Mara National Reserve, Kenya, over a 23-year period spanning three generations. The metagenomic data came from four of these hyenas and spanned two 2-year periods. With these data, we determined the extent to which host factors predicted variation in the gut microbiome and identified the core microbes present in the guts of hyenas. We also investigated novel genomic diversity in the mammalian gut by reporting the first metagenome-assembled genomes (MAGs) for hyenas. We found that gut microbiome taxonomic composition varied temporally, but despite this, a core set of 14 bacterial genera were identified. The strongest predictors of the microbiome were host identity and age, suggesting that hyenas possess individualized microbiomes and that these may change with age during adulthood. The gut microbiome functional profiles of the four adult hyenas were also individual specific and were associated with prey abundance, indicating that the functions of the gut microbiome vary with host diet. We recovered 149 high-quality MAGs from the hyenas’ guts; some MAGs were classified as taxa previously reported for other carnivores, but many were novel and lacked species-level matches to genomes in existing reference databases. IMPORTANCE There is a gap in knowledge regarding the genomic diversity and variation of the gut microbiome across a host’s life span and across multiple generations of hosts in wild mammals. Using two types of sequencing approaches, we found that although gut microbiomes were individualized and temporally variable among hyenas, they correlated similarly to large-scale changes in the ecological conditions experienced by their hosts. We also recovered 149 high-quality MAGs from the hyena gut, greatly expanding the microbial genome repertoire known for hyenas, carnivores, and wild mammals in general. Some MAGs came from genera abundant in the gastrointestinal tracts of canid species and other carnivores, but over 80% of MAGs were novel and from species not previously represented in genome databases. Collectively, our novel body of work illustrates the importance of surveying the gut microbiome of nonmodel wild hosts, using multiple sequencing methods and computational approaches and at distinct scales of analysis. 

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3. Plant neighborhood shapes diversity and reduces interspecific variation of the phyllosphere microbiome

   https://doi.org/10.1038/s41396-021-01184-6  

   Meyer, Kyle M. ; Porch, Robert ; Muscettola, Isabella E. ; Vasconcelos, Ana Luisa S. ; Sherman, Julia K. ; Metcalf, C. Jessica E. ; Lindow, Steven E. ; Koskella, Britt ( January 2022 , The ISME Journal)

   Microbial communities associated with plant leaf surfaces (i.e., the phyllosphere) are increasingly recognized for their role in plant health. While accumulating evidence suggests a role for host filtering of its microbiota, far less is known about how community composition is shaped by dispersal, including from neighboring plants. We experimentally manipulated the local plant neighborhood within which tomato, pepper, or bean plants were grown in a 3-month field trial. Focal plants were grown in the presence of con- or hetero-specific neighbors (or no neighbors) in a fully factorial combination. At 30-day intervals, focal plants were harvested and replaced with a new age- and species-matched cohort while allowing neighborhood plants to continue growing. Bacterial community profiling revealed that the strength of host filtering effects (i.e., interspecific differences in composition) decreased over time. In contrast, the strength of neighborhood effects increased over time, suggesting dispersal from neighboring plants becomes more important as neighboring plant biomass increases. We next implemented a cross-inoculation study in the greenhouse using inoculum generated from the field plants to directly test host filtering of microbiomes while controlling for directionality and source of dispersal. This experiment further demonstrated that focal host species, the host from which the microbiome came, and in one case the donor hosts’ neighbors, contribute to variation in phyllosphere bacterial composition. Overall, our results suggest that local dispersal is a key factor in phyllosphere assembly, and that demographic factors such as nearby neighbor identity and biomass or age are important determinants of phyllosphere microbiome diversity.

    

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4. Social environment and genetics underlie body site‐specific microbiomes of Yellowstone National Park gray wolves ( Canis lupus )

   https://doi.org/10.1002/ece3.7767  

   DeCandia, Alexandra L. ; Cassidy, Kira A. ; Stahler, Daniel R. ; Stahler, Erin A. ; vonHoldt, Bridgett M. ( June 2021 , Ecology and Evolution)

   The host‐associated microbiome is an important player in the ecology and evolution of species. Despite growing interest in the medical, veterinary, and conservation communities, there remain numerous questions about the primary factors underlying microbiota, particularly in wildlife. We bridged this knowledge gap by leveraging microbial, genetic, and observational data collected in a wild, pedigreed population of gray wolves (Canis lupus) inhabiting Yellowstone National Park. We characterized body site‐specific microbes across six haired and mucosal body sites (and two fecal samples) using 16S rRNA amplicon sequencing. At the phylum level, we found that the microbiome of gray wolves primarily consists of Actinobacteria, Bacteroidetes, Firmicutes, Fusobacteria, and Proteobacteria, consistent with previous studies within Mammalia and Canidae. At the genus level, we documented body site‐specific microbiota with functions relevant to microenvironment and local physiological processes. We additionally employed observational and RAD sequencing data to examine genetic, demographic, and environmental correlates of skin and gut microbiota. We surveyed individuals across several levels of pedigree relationships, generations, and social groups, and found that social environment (i.e., pack) and genetic relatedness were two primary factors associated with microbial community composition to differing degrees between body sites. We additionally reported body condition and coat color as secondary factors underlying gut and skin microbiomes, respectively. We concluded that gray wolf microbiota resemble similar host species, differ between body sites, and are shaped by numerous endogenous and exogenous factors. These results provide baseline information for this long‐term study population and yield important insights into the evolutionary history, ecology, and conservation of wild wolves and their associated microbes.

    

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5. Geography and elevation as drivers of cloacal microbiome assemblages of a passerine bird distributed across Sulawesi, Indonesia

   https://doi.org/10.1186/s42523-022-00219-3  

   Joakim, Rachael L. ; Irham, Mohammad ; Haryoko, Tri ; Rowe, Karen M. C. ; Dalimunthe, Yohanna ; Anita, Syahfitri ; Achmadi, Anang S. ; McGuire, Jimmy A. ; Perkins, Susan ; Bowie, Rauri C. K. ( January 2023 , Animal Microbiome)

   Empirical field studies allow us to view how ecological and environmental processes shape the biodiversity of our planet, but collecting samples in situ creates inherent challenges. The majority of empirical vertebrate gut microbiome research compares multiple host species against abiotic and biotic factors, increasing the potential for confounding environmental variables. To minimize these confounding factors, we focus on a single species of passerine bird found throughout the geologically complex island of Sulawesi, Indonesia. We assessed the effects of two environmental factors, geographic Areas of Endemism (AOEs) and elevation, as well as host sex on the gut microbiota assemblages of the Sulawesi Babbler,Pellorneum celebense,from three different mountains across the island. Using cloacal swabs, high-throughput-amplicon sequencing, and multiple statistical models, we identified the core microbiome and determined the signal of these three factors on microbial composition.

   The five most prevalent bacterial phyla within the gut microbiome ofP. celebensewereProteobacteria(32.6%),Actinobacteria(25.2%),Firmicutes(22.1%),Bacteroidetes(8.7%), andPlantomycetes(2.6%). These results are similar to those identified in prior studies of passeriform microbiomes. Overall, microbiota diversity decreased as elevation increased, irrespective of sex or AOE. A single ASV ofClostridiumwas enriched in higher elevation samples, while lower elevation samples were enriched with the generaPerlucidibaca(FamilyMoraxellaceae),Lachnoclostridium(FamilyLachnospiraceae), and an unidentified species in the FamilyPseudonocardiaceae.

   While the core microbiota families recovered here are consistent with other passerine studies, the decreases in diversity as elevation increases has only been seen in non-avian hosts. Additionally, the increased abundance ofClostridiumat high elevations suggests a potential microbial response to lower oxygen levels. This study emphasizes the importance of incorporating multiple statistical models and abiotic factors such as elevation in empirical microbiome research, and is the first to describe an avian gut microbiome from the island of Sulawesi.

    

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