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1. Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota

   https://doi.org/10.1186/s42523-022-00176-x  

   Bornbusch, Sally L. ; Greene, Lydia K. ; Rahobilalaina, Sylvia ; Calkins, Samantha ; Rothman, Ryan S. ; Clarke, Tara A. ; LaFleur, Marni ; Drea, Christine M. ( April 2022 , Animal Microbiome)

   Inter-population variation in host-associated microbiota reflects differences in the hosts’ environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes—an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur (Lemur catta; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used microbial source tracking to examine covariation between the two types of consortia.

   The diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or environmental condition. Variation in microbial composition was inconsistent both withmore »a single, representative gut community for wild conspecifics and with a universal ‘signal of captivity’ that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemur gut microbiomes within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities varied across geographic locations, with the few samples from different continents being the most distinct, and there was significant and context-specific covariation between gut and soil microbiota.

   As one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple ‘captive vs. wild’ dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.

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2. Variations in the microbiome due to storage preservatives are not large enough to obscure variations due to factors such as host population, host species, body site, and captivity

   https://doi.org/10.1002/ajp.23045  

   Asangba, Abigail E. ; Donohue, Mariah E. ; Lamb, Alicia ; Wright, Patricia C. ; Halajian, Ali ; Leigh, Steven R. ; Stumpf, Rebecca M. ( August 2019 , American Journal of Primatology)

   The study of the primate microbiome is critical in understanding the role of the microbial community in the host organism. To be able to isolate the main factors responsible for the differences observed in microbiomes within and between individuals, confounding factors due to technical variations need to be removed. To determine whether alterations due to preservatives outweigh differences due to factors such as host population, host species, body site, and habitat, we tested three methods (no preservative, 96% ethanol, and RNAlater) for preserving wild chimpanzee (fecal), wild lemur (fecal), wild vervet monkey (rectal, oral, nasal, otic, vaginal, and penile), and captive vervet monkey (rectal) samples. All samples were stored below − 20°C (short term) at the end of the field day and then at − 80°C until DNA extraction. Using 16S rRNA gene sequencing, we show a significant preservative effect on microbiota composition and diversity. Samples stored in ethanol and RNAlater appear to be less different compared with samples not stored in any preservative (none). Our differential analysis revealed significantly higher amounts of Enterococcaceae and Family XI in no preservative samples, Prevotellaceae and Spirochaetaceae in ethanol and RNAlater preserved samples, Oligosphaeraceae in ethanol‐preserved samples, and Defluviitaleaceae in RNAlater preserved samples. Whilemore »these preservative effects on the microbiome are not large enough to remove or outweigh the differences arising from biological factors (e.g., host species, body site, and habitat differences) they may promote misleading interpretations if they have large enough effect sizes compared to the biological factors (e.g., host population).

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3. Wild microbiomes of striped plateau lizards vary with reproductive season, sex, and body size

   https://doi.org/10.1038/s41598-022-24518-6  

   Bunker, Marie E. ; Arnold, A. Elizabeth ; Weiss, Stacey L. ( December 2022 , Scientific Reports)

   Abstract Long-term studies of animal microbiomes under natural conditions are valuable for understanding the effects of host demographics and environmental factors on host-associated microbial communities, and how those effects interact and shift over time. We examined how the cloacal microbiome of wild Sceloporus virgatus (the striped plateau lizard) varies under natural conditions in a multi-year study. Cloacal swabs were collected from wild-caught lizards across their entire active season and over three years in southeastern Arizona, USA. Analyses of 16S rRNA data generated on the Illumina platform revealed that cloacal microbiomes of S. virgatus vary as a function of season, sex, body size, and reproductive state, and do so independently of one another. Briefly, microbial diversity was lowest in both sexes during the reproductive season, was higher in females than in males, and was lowest in females when they were vitellogenic, and microbiome composition varied across seasons, sexes, and sizes. The pattern of decreased diversity during reproductive periods with increased sociality is surprising, as studies in other systems often suggest that microbial diversity generally increases with sociality. The cloacal microbiome was not affected significantly by hibernation and was relatively stable from year to year. This study highlights the importance of longmore »term, wide-scale microbiome studies for capturing accurate perspectives on microbiome diversity and composition in animals. It also serves as a warning for comparisons of microbiomes across species, as each may be under a different suite of selective pressures or exhibit short-term variation from external or innate factors, which may differ in a species-specific manner.« less
4. Antibiotics and fecal transfaunation differentially affect microbiota recovery, associations, and antibiotic resistance in lemur guts

   https://doi.org/10.1186/s42523-021-00126-z  

   Bornbusch, Sally L. ; Harris, Rachel L. ; Grebe, Nicholas M. ; Roche, Kimberly ; Dimac-Stohl, Kristin ; Drea, Christine M. ( October 2021 , Animal Microbiome)

   Antibiotics alter the diversity, structure, and dynamics of host-associated microbial consortia, including via development of antibiotic resistance; however, patterns of recovery from microbial imbalances and methods to mitigate associated negative effects remain poorly understood, particularly outside of human-clinical and model-rodent studies that focus on outcome over process. To improve conceptual understanding of host-microbe symbiosis in more naturalistic contexts, we applied an ecological framework to a non-traditional, strepsirrhine primate model via long-term, multi-faceted study of microbial community structure before, during, and following two experimental manipulations. Specifically, we administered a broad-spectrum antibiotic, either alone or with subsequent fecal transfaunation, to healthy, male ring-tailed lemurs (Lemur catta), then used 16S rRNA and shotgun metagenomic sequencing to longitudinally track the diversity, composition, associations, and resistomes of their gut microbiota both within and across baseline, treatment, and recovery phases.

   Antibiotic treatment resulted in a drastic decline in microbial diversity and a dramatic alteration in community composition. Whereas microbial diversity recovered rapidly regardless of experimental group, patterns of microbial community composition reflected long-term instability following treatment with antibiotics alone, a pattern that was attenuated by fecal transfaunation. Covariation analysis revealed that certain taxa dominated bacterial associations, representing potential keystone species in lemur gut microbiota. Antibioticmore »resistance genes, which were universally present, including in lemurs that had never been administered antibiotics, varied across individuals and treatment groups.

   Long-term, integrated study post antibiotic-induced microbial imbalance revealed differential, metric-dependent evidence of recovery, with beneficial effects of fecal transfaunation on recovering community composition, and potentially negative consequences to lemur resistomes. Beyond providing new perspectives on the dynamics that govern host-associated communities, particularly in the Anthropocene era, our holistic study in an endangered species is a first step in addressing the recent, interdisciplinary calls for greater integration of microbiome science into animal care and conservation.

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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,more »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.« less