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1. Antibiotic Resistance Genes in Lemur Gut and Soil Microbiota Along a Gradient of Anthropogenic Disturbance

   https://doi.org/10.3389/fevo.2021.704070  

   Bornbusch, Sally L. ; Drea, Christine M. ( August 2021 , Frontiers in Ecology and Evolution)

   The overuse of man-made antibiotics has facilitated the global propagation of antibiotic resistance genes in animals, across natural and anthropogenically disturbed environments. Although antibiotic treatment is the most well-studied route by which resistance genes can develop and spread within host-associated microbiota, resistomes also can be acquired or enriched via more indirect routes, such as via transmission between hosts or via contact with antibiotic-contaminated matter within the environment. Relatively little is known about the impacts of anthropogenic disturbance on reservoirs of resistance genes in wildlife and their environments. We therefore tested for (a) antibiotic resistance genes in primate hosts experiencing different severities and types of anthropogenic disturbance (i.e., non-wildlife animal presence, human presence, direct human contact, and antibiotic treatment), and (b) covariation between host-associated and environmental resistomes. We used shotgun metagenomic sequencing of ring-tailed lemur ( Lemur catta ) gut resistomes and associated soil resistomes sampled from up to 10 sites: seven in the wilderness of Madagascar and three in captivity in Madagascar or the United States. We found that, compared to wild lemurs, captive lemurs harbored greater abundances of resistance genes, but not necessarily more diverse resistomes. Abundances of resistance genes were positively correlated with our assessments of anthropogenic disturbance,more »a pattern that was robust across all ten lemur populations. The composition of lemur resistomes was site-specific and the types of resistance genes reflected antibiotic usage in the country of origin, such as vancomycin use in Madagascar. We found support for multiple routes of ARG enrichment (e.g., via human contact, antibiotic treatment, and environmental acquisition) that differed across lemur populations, but could result in similar degrees of enrichment. Soil resistomes varied across natural habitats in Madagascar and, at sites with greater anthropogenic disturbance, lemurs and soil resistomes covaried. As one of the broadest, single-species investigations of wildlife resistomes to date, we show that the transmission and enrichment of antibiotic resistance genes varies across environments, thereby adding to the mounting evidence that the resistance crisis extends outside of traditional clinical settings.« less
2. 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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3. An examination of the use of antibiotics as a method to experimentally perturb the microbiota of suspension‐feeding bivalves

   https://doi.org/10.1111/ivb.12352  

   Griffin, Tyler W. ; Pierce, Melissa L. ; Nigro, Lisa M. ; Holohan, Bridget A. ; Ward, J. Evan ( November 2021 , Invertebrate Biology)

   Suspension‐feeding bivalves are critical members of aquatic ecosystems worldwide, which is why research into their host‐associated microbiota is growing. Experiments that artificially diminish the native microbial communities of bivalvesin vivowill be increasingly necessary to evaluate the functional role of microbes within their hosts. Previous methods to manipulate the microbiome of bivalves lack standardization and, often, verification of successful disturbance. The goal of this study was to evaluate antibiotic administration as a method for perturbing the gut microbiome of bivalves in two separate, but related, experiments. In the first, a mixture of antibiotics was delivered to eastern oysters for 4 days to probe effects on gut microbial carbon usage, diversity, and taxonomic composition. In the second, the same antibiotic mixture was administered to blue mussels for 21 days to probe effects on microbial abundance, diversity, and taxonomic composition. In both experiments, animals were administered antibiotics in isolation, and stringent sterilization methods were employed, which included sterilized seawater and microalgal food. The results of the oyster experiment revealed that antibiotics substantially reduced microbial carbon usage and perturbed community composition. In the mussel experiment, antibiotics lowered microbial abundance and species richness and significantly altered community composition. Taken together, results from the two experiments demonstratemore »that antibiotics can be used to effectively alter the function and composition of the gut microbial community of bivalves. Future research that aims to perturb the microbiomes of suspension‐feeding animals should incorporate aspects similar to the protocols described herein. Additionally, future studies must include verification, ideally high‐throughput DNA sequencing coupled with microbial quantification, that the antibiotic perturbation was successful.

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4. Household composition and the infant fecal microbiome: The INSPIRE study

   https://doi.org/10.1002/ajpa.23843  

   Lane, Avery A. ; McGuire, Michelle K. ; McGuire, Mark A. ; Williams, Janet E. ; Lackey, Kimberly A. ; Hagen, Edward H. ; Kaul, Abhishek ; Gindola, Debela ; Gebeyehu, Dubale ; Flores, Katherine E. ; et al ( April 2019 , American Journal of Physical Anthropology)

   Establishment and development of the infant gastrointestinal microbiome (GIM) varies cross‐culturally and is thought to be influenced by factors such as gestational age, birth mode, diet, and antibiotic exposure. However, there is little data as to how the composition of infants' households may play a role, particularly from a cross‐cultural perspective. Here, we examined relationships between infant fecal microbiome (IFM) diversity/composition and infants' household size, number of siblings, and number of other household members.

   We analyzed 377 fecal samples from healthy, breastfeeding infants across 11 sites in eight different countries (Ethiopia, The Gambia, Ghana, Kenya, Peru, Spain, Sweden, and the United States). Fecal microbial community structure was determined by amplifying, sequencing, and classifying (to the genus level) the V1–V3 region of the bacterial 16S rRNA gene. Surveys administered to infants' mothers identified household members and composition.

   Our results indicated that household composition (represented by the number of cohabitating siblings and other household members) did not have a measurable impact on the bacterial diversity, evenness, or richness of the IFM. However, we observed that variation in household composition categories did correspond to differential relative abundances of specific taxa, namely:Lactobacillus,Clostridium,Enterobacter, andKlebsiella.

   This study, to our knowledge, is the largestmore »cross‐cultural study to date examining the association between household composition and the IFM. Our results indicate that the social environment of infants (represented here by the proxy of household composition) may influence the bacterial composition of the infant GIM, although the mechanism is unknown. A higher number and diversity of cohabitants and potential caregivers may facilitate social transmission of beneficial bacteria to the infant gastrointestinal tract, by way of shared environment or through direct physical and social contact between the maternal–infant dyad and other household members. These findings contribute to the discussion concerning ways by which infants are influenced by their social environments and add further dimensionality to the ongoing exploration of social transmission of gut microbiota and the “old friends” hypothesis.

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5. Extensive variability in the gut microbiome of a highly‐specialized and critically endangered lemur species across sites

   https://doi.org/10.1002/ajp.23046  

   Donohue, Mariah E. ; Asangba, Abigail E. ; Ralainirina, Jocelyn ; Weisrock, David W. ; Stumpf, Rebecca M. ; Wright, Patricia C. ( September 2019 , American Journal of Primatology)

   Deforestation continues to jeopardize Malagasy primates as viable habitats become smaller, more fragmented, and more disturbed. This deforestation can lead to changes in diet, microhabitat, and gene flow between populations of endangered species, and it remains unclear how these changes may affect gut microbiome (GM) characteristics. The black‐and‐white ruffed lemur (Varecia variegata), which is among Madagascar's most threatened lemur species, provides a critical model for understanding the relationships between historical and on‐going deforestation (habitat disturbance), feeding ecology, and GM composition and diversity. We studied four populations inhabiting two rainforests (relatively pristine vs. highly disturbed) in southeastern Madagascar. We conducted full‐day focal animal behavioral follows and collected fecal samples opportunistically across a three‐month period. Our results indicate that lemurs inhabiting sites characterized by habitat disturbance and low dietary diversity exhibited reduced gut microbial alpha diversity. We also show that these same factors were associated with high community dissimilarity using weighted and unweighted UniFrac metrics. Finally, an indicator species analysis showed that the most pristine site was characterized by an abundance of methanogenic archaea. While it is impossible to disentangle the relative contributions of each confounding variable presented by our sampling design, these results provide crucial information about GM variability, therebymore »underscoring the importance of monitoring endangered species at the population‐level.

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