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1. Microbial rewilding in the gut microbiomes of captive ring-tailed lemurs (Lemur catta) in Madagascar

   https://doi.org/10.1038/s41598-022-26861-0  

   Bornbusch, Sally_L; Clarke, Tara_A; Hobilalaina, Sylvia; Reseva, Honore_Soatata; LaFleur, Marni; Drea, Christine_M (December 2022, Scientific Reports)

   Abstract Microbial rewilding, whereby exposure to naturalistic environments can modulate or augment gut microbiomes and improve host-microbe symbiosis, is being harnessed as an innovative approach to human health, one that may also have significant value to animal care and conservation. To test for microbial rewilding in animal microbiomes, we used a unique population of wild-born ring-tailed lemurs (Lemur catta) that were initially held as illegal pets in unnatural settings and, subsequently, relocated to a rescue center in Madagascar where they live in naturalistic environments. Using amplicon and shotgun metagenomic sequencing of lemur and environmental microbiomes, we found multiple lines of evidence for microbial rewilding in lemurs that were transitioned from unnatural to naturalistic environments: A lemur’s duration of exposure to naturalistic settings significantly correlated with (a) increased compositional similarly to the gut communities of wild lemurs, (b) decreased proportions of antibiotic resistance genes that were likely acquired via human contact during pethood, and (c) greater covariation with soil microbiomes from natural habitats. Beyond the inherent psychosocial value of naturalistic environments, we find that actions, such as providing appropriate diets, minimizing contact with humans, and increasing exposure to natural environmental consortia, may assist in maximizing host-microbe symbiosis in animals under human care. 

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2. The meta-gut: community coalescence of animal gut and environmental microbiomes

   https://doi.org/10.1038/s41598-021-02349-1  

   Dutton, Christopher L.; Subalusky, Amanda L.; Sanchez, Alvaro; Estrela, Sylvie; Lu, Nanxi; Hamilton, Stephen K.; Njoroge, Laban; Rosi, Emma J.; Post, David M. (November 2021, Scientific Reports)

   Abstract All animals carry specialized microbiomes, and their gut microbiota are continuously released into the environment through excretion of waste. Here we propose themeta-gutas a novel conceptual framework that addresses the ability of the gut microbiome released from an animal to function outside the host and alter biogeochemical processes mediated by microbes. We demonstrate this dynamic in the hippopotamus (hippo) and the pools they inhabit. We used natural field gradients and experimental approaches to examine fecal and pool water microbial communities and aquatic biogeochemistry across a range of hippo inputs. Sequencing using 16S RNA methods revealed community coalescence between hippo gut microbiomes and the active microbial communities in hippo pools that received high inputs of hippo feces. The shared microbiome between the hippo gut and the waters into which they excrete constitutes ameta-gutsystem that could influence the biogeochemistry of recipient ecosystems and provide a reservoir of gut microbiomes that could influence other hosts. We propose thatmeta-gutdynamics may also occur where other animal species congregate in high densities, particularly in aquatic environments. 

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3. The reproductive microbiome and maternal transmission of microbiota via eggs in Sceloporus virgatus

   https://doi.org/10.1093/femsec/fiae011  

   Bunker, Marie E.; Weiss, Stacey L. (February 2024, FEMS Microbiology Ecology)

   Abstract Maternal transmission of microbes occurs across the animal kingdom and is vital for offspring development and long-term health. The mechanisms of this transfer are most well-studied in humans and other mammals but are less well-understood in egg-laying animals, especially those with no parental care. Here, we investigate the transfer of maternal microbes in the oviparous phrynosomatid lizard, Sceloporus virgatus. We compared the microbiota of three maternal tissues—oviduct, cloaca, and intestine—to three offspring sample types: egg contents and eggshells on the day of oviposition, and hatchling intestinal tissue on the day of hatching. We found that maternal identity is an important factor in hatchling microbiome composition, indicating that maternal transmission is occurring. The maternal cloacal and oviductal communities contribute to offspring microbiota in all three sample types, with minimal microbes sourced from maternal intestines. This indicates that the maternal reproductive microbiome is more important for microbial inheritance than the gut microbiome, and the tissue-level variation of the adult S. virgatus microbiota must develop as the hatchling matures. Despite differences between adult and hatchling communities, offspring microbiota were primarily members of the Enterobacteriaceae and Yersiniaceae families (Phylum Proteobacteria), consistent with this and past studies of adult S. virgatus microbiomes. 

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4. Macrobdella decora : Old World Leech Gut Microbial Community Structure Conserved in a New World Leech

   https://doi.org/10.1128/AEM.02082-20  

   McClure, Emily Ann; Nelson, Michael C.; Lin, Amy; Graf, Joerg (April 2021, Applied and Environmental Microbiology)

   Johnson, Karyn N. (Ed.)

   ABSTRACT Leeches are found in terrestrial, aquatic, and marine habitats on all continents. Sanguivorous leeches have been used in medicine for millennia. Modern scientific uses include studies of neurons, anticoagulants, and gut microbial symbioses. Hirudo verbana , the European medicinal leech, maintains a gut community dominated by two bacterial symbionts, Aeromonas veronii and Mucinivorans hirudinis , which sometimes account for as much as 97% of the total crop microbiota. The highly simplified gut anatomy and microbiome of H. verbana make it an excellent model organism for studying gut microbial dynamics. The North American medicinal leech, Macrobdella decora , is a hirudinid leech native to Canada and the northern United States. In this study, we show that M. decora symbiont communities are very similar to those in H. verbana. We performed an extensive study using field-caught M. decora and purchased H. verbana from two suppliers. Deep sequencing of the V4 region of the 16S rRNA gene allowed us to determine that the core microbiome of M. decora consists of Bacteroides , Aeromonas, Proteocatella , and Butyricicoccus. The analysis revealed that the compositions of the gut microbiomes of the two leech species were significantly different at all taxonomic levels. The R 2 value was highest at the genus and amplicon sequence variant (ASV) levels and much lower at the phylum, class, and order levels. The gut and bladder microbial communities were distinct. We propose that M. decora is an alternative to H. verbana for studies of wild-caught animals and provide evidence for the conservation of digestive-tract and bladder symbionts in annelid models. IMPORTANCE Building evidence implicates the gut microbiome in critical animal functions such as regulating digestion, nutrition, immune regulation, and development. Simplified, phylogenetically diverse models for hypothesis testing are necessary because of the difficulty of assigning causative relationships in complex gut microbiomes. Previous research used Hirudo verbana as a tractable animal model of digestive-tract symbioses. Our data show that Macrobdella decora may work just as well without the drawback of being an endangered organism and with the added advantage of easy access to field-caught specimens. The similarity of the microbial community structures of species from two different continents reveals the highly conserved nature of the microbial symbionts in sanguivorous leeches. 

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5. Large Comparative Analyses of Primate Body Site Microbiomes Indicate that the Oral Microbiome Is Unique among All Body Sites and Conserved among Nonhuman Primates

   https://doi.org/10.1128/spectrum.01643-21  

   Asangba, Abigail E.; Mugisha, Lawrence; Rukundo, Joshua; Lewis, Rebecca J.; Halajian, Ali; Cortés-Ortiz, Liliana; Junge, Randall E.; Irwin, Mitchell T.; Karlson, Johan; Perkin, Andrew; et al (June 2022, Microbiology Spectrum)

   Kormas, Konstantinos Aristomenis (Ed.)

   ABSTRACT The study of the mammalian microbiome serves as a critical tool for understanding host-microbial diversity and coevolution and the impact of bacterial communities on host health. While studies of specific microbial systems (e.g., in the human gut) have rapidly increased, large knowledge gaps remain, hindering our understanding of the determinants and levels of variation in microbiomes across multiple body sites and host species. Here, we compare microbiome community compositions from eight distinct body sites among 17 phylogenetically diverse species of nonhuman primates (NHPs), representing the largest comparative study of microbial diversity across primate host species and body sites. Analysis of 898 samples predominantly acquired in the wild demonstrated that oral microbiomes were unique in their clustering, with distinctive divergence from all other body site microbiomes. In contrast, all other body site microbiomes clustered principally by host species and differentiated by body site within host species. These results highlight two key findings: (i) the oral microbiome is unique compared to all other body site microbiomes and conserved among diverse nonhuman primates, despite their considerable dietary and phylogenetic differences, and (ii) assessments of the determinants of host-microbial diversity are relative to the level of the comparison (i.e., intra-/inter-body site, -host species, and -individual), emphasizing the need for broader comparative microbial analyses across diverse hosts to further elucidate host-microbial dynamics, evolutionary and biological patterns of variation, and implications for human-microbial coevolution. IMPORTANCE The microbiome is critical to host health and disease, but much remains unknown about the determinants, levels, and evolution of host-microbial diversity. The relationship between hosts and their associated microbes is complex. Most studies to date have focused on the gut microbiome; however, large gaps remain in our understanding of host-microbial diversity, coevolution, and levels of variation in microbiomes across multiple body sites and host species. To better understand the patterns of variation and evolutionary context of host-microbial communities, we conducted one of the largest comparative studies to date, which indicated that the oral microbiome was distinct from the microbiomes of all other body sites and convergent across host species, suggesting conserved niche specialization within the Primates order. We also show the importance of host species differences in shaping the microbiome within specific body sites. This large, comparative study contributes valuable information on key patterns of variation among hosts and body sites, with implications for understanding host-microbial dynamics and human-microbial coevolution. 

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