Domestication shapes the pig gut microbiome and immune traits from the scale of lineage to population.

Animal ecology and evolution have long been known to shape host physiology, but more recently, the gut microbiome has been identified as a mediator between animal ecology and evolution and health. The gut microbiome has been shown to differ between wild and domestic animals, but the role of these differences for domestic animal evolution remains unknown. Gut microbiome responses to new animal genotypes and local environmental change during domestication may promote specific host phenotypes that are adaptive (or not) to the domestic environment. Because the gut microbiome supports host immune function, understanding the effects of animal ecology and evolution on the gut microbiome and immune phenotypes is critical. We investigated how domestication affects the gut microbiome and host immune state in multiple pig populations across five domestication contexts representing domestication status and current living conditions: free-ranging wild, captive wild, free-ranging domestic, captive domestic in research or industrial settings. We observed that domestication context explained much of the variation in gut microbiome composition, pathogen abundances and immune markers, yet the main differences in the repertoire of metabolic genes found in the gut microbiome were between the wild and domestic genetic lineages. We also documented population-level effects within domestication contexts, demonstrating that fine scale environmental variation also shaped host and microbe features. Our findings highlight that understanding which gut microbiome and immune traits respond to host genetic lineage and/or scales of local ecology could inform targeted interventions that manipulate the gut microbiome to achieve beneficial health outcomes.

Prenatal household size and composition are associated with infant fecal bacterial diversity in Cebu, Philippines.

OBJECTIVES: The gut microbiome (GM) connects physical and social environments to infant health. Since the infant GM affects immune system development, there is interest in understanding how infants acquire microbes from mothers and other household members. MATERIALS AND METHODS: As a part of the Cebu Longitudinal Health and Nutrition Survey (CLHNS), we paired fecal samples (proxy for the GM) collected from infants living in Metro Cebu, Philippines at 2 weeks (N = 39) and 6 months (N = 36) with maternal interviews about prenatal household composition. We hypothesized that relationships between prenatal household size and composition and infant GM bacterial diversity (as measured in fecal samples) would vary by infant age, as well as by household member age and sex. We also hypothesized that infant GM bacterial abundances would differ by prenatal household size and composition. RESULTS: Data from 16 S rRNA bacterial gene sequencing show that prenatal household size was the most precise estimator of infant GM bacterial diversity, and that the direction of the association between this variable and infant GM bacterial diversity changed between the two time points. The abundances of bacterial families in the infant GM varied by prenatal household variables. CONCLUSIONS: Results highlight the contributions of various household sources to the bacterial diversity of the infant GM, and suggest that prenatal household size is a useful measure for estimating infant GM bacterial diversity in this cohort. Future research should measure the effect of specific sources of household bacterial exposures, including social interactions with caregivers, on the infant GM.

Limited microbiome differences in captive and semi-wild primate populations consuming similar diets.

Gut microbial communities are shaped by a myriad of extrinsic factors, including diet and the environment. Although distinct human populations consistently exhibit different gut microbiome compositions, variation in diet and environmental factors are almost always coupled, making it difficult to disentangle their relative contributions to shaping the gut microbiota. Data from discrete animal populations with similar diets can help reduce confounds. Here, we assessed the gut microbiota of free-ranging and captive rhesus macaques with at least 80% diet similarity to test the hypothesis that hosts in difference environments will have different gut microbiomes despite a shared diet. Although we found that location was a significant predictor of gut microbial composition, the magnitude of observed differences was relatively small. These patterns suggest that a shared diet may limit the typical influence of environmental microbial exposure on the gut microbiota.

Molecular characterization of Giardia duodenalis and evidence for cross-species transmission in Northern Argentina.

Anthropogenic activities, such as human population expansion and land-use change, create ecological overlap between humans, domesticated animals, and wildlife and can exacerbate the zoonotic transmission of parasites. To improve our understanding of this dynamic, we employed multi-locus genotyping to conduct a cross-sectional study of the potential for zoonotic transmission of the protozoan parasite Giardia duodenalis among humans, household associated livestock and dogs, and black and gold howler monkeys (Alouatta caraya) in the Corrientes Province of Argentina. We found Giardia prevalence to be highest in howler monkeys (90.3% (47/52)), followed by humans (61.1% (22/36)), dogs (44.4% (16/36)), and cattle (41.9% (18/43)). We further established that howler monkeys exclusively harbored strains of assemblage B (100%) while humans were infected with either assemblage A (13.3%) or B (80%) or A and B (6.7%), and cattle and dogs were infected with either assemblage A (cattle, 94.1%; dogs, 80%)), A and C (10%), or their host-adapted assemblage (cattle, 5.9%; dogs, 10%). Our finding of G. duodenalis in both humans and domesticated animals (assemblage A) and humans and wild primates (assemblage B) suggests that cross-species transmission of multiple assemblages of G. duodenalis may occur in rural complexes such as northern Argentina where people, domesticated animals, and wildlife overlap. We further highlight the need to investigate the implications of these results for human health, the economics of livestock production, and wildlife conservation in this and similar systems.

Comparing different sample collection and storage methods for field-based skin microbiome research.

OBJECTIVES: The skin, as well as its microbial communities, serves as the primary interface between the human body and the surrounding environment. In order to implement the skin microbiome into human biology research, there is a need to explore the effects of different sample collection and storage methodologies, including the feasibility of conducting skin microbiome studies in field settings. METHODS: We collected 99 skin microbiome samples from nine infants living in Veracruz, Mexico using a dual-tipped "dry" swab on the right armpit, palm, and forehead and a "wet" swab (0.15 M NaCl and 0.1% Tween 20) on the same body parts on the left side of the body. One swab from each collection method was stored in 95% ethanol while the other was frozen at -20°C. 16S rRNA amplicon sequencing generated data on bacterial diversity and community composition, which were analyzed using PERMANOVA, linear mixed effects models, and an algorithm-based classifier. RESULTS: Treatment (wet_ethanol, wet_freezer, dry_ethanol, and dry_freezer) had an effect (~10% explanatory power) on the bacterial community diversity and composition of skin samples, although body site exhibited a stronger effect (~20% explanatory power). Within treatments, the collection method (wet vs. dry) affected measures of bacterial diversity to a greater degree than did the storage method (ethanol vs. freezer). CONCLUSIONS: Our study provides novel information on skin microbiome sample collection and storage methods, suggesting that ethanol storage is suitable for research in resource-limited settings. Our results highlight the need for future study design to account for interbody site microbial variation.

Variation in Microbial Exposure at the Human-Animal Interface and the Implications for Microbiome-Mediated Health Outcome.

The human gut microbiome varies between populations, largely reflecting ecological differences. One ecological variable that is rarely considered but may contribute substantially to microbiome variation is the multifaceted nature of human-animal interfaces. We present the hypothesis that different interactions with animals contribute to shaping the human microbiome globally. We utilize a One Health framework to explore how changes in microbial exposure from human-animal interfaces shape the microbiome and, in turn, contribute to differential human health across populations, focusing on commensal and pathogen exposure, changes in colonization resistance and immune system training, and the potential for other functional shifts. Although human-animal interfaces are known to underlie human health and particularly infectious disease disparities, since their impact on the human microbiome remains woefully understudied, we propose foci for future research. We believe it will be crucial to understand this critical aspect of biology and its impacts on human health around the globe.

Introducing the Microbes and Social Equity Working Group: Considering the Microbial Components of Social, Environmental, and Health Justice.

Humans are inextricably linked to each other and our natural world, and microorganisms lie at the nexus of those interactions. Microorganisms form genetically flexible, taxonomically diverse, and biochemically rich communities, i.e., microbiomes that are integral to the health and development of macroorganisms, societies, and ecosystems. Yet engagement with beneficial microbiomes is dictated by access to public resources, such as nutritious food, clean water and air, safe shelter, social interactions, and effective medicine. In this way, microbiomes have sociopolitical contexts that must be considered. The Microbes and Social Equity (MSE) Working Group connects microbiology with social equity research, education, policy, and practice to understand the interplay of microorganisms, individuals, societies, and ecosystems. Here, we outline opportunities for integrating microbiology and social equity work through broadening education and training; diversifying research topics, methods, and perspectives; and advocating for evidence-based public policy that supports sustainable, equitable, and microbial wealth for all.

Effects of anthropogenic habitat disturbance and Giardia duodenalis infection on a sentinel species' gut bacteria.

Habitat disturbance, a common consequence of anthropogenic land use practices, creates human-animal interfaces where humans, wildlife, and domestic species can interact. These altered habitats can influence host-microbe dynamics, leading to potential downstream effects on host physiology and health. Here, we explored the effect of ecological overlap with humans and domestic species and infection with the protozoan parasite Giardia duodenalis on the bacteria of black and gold howler monkeys (Alouatta caraya), a key sentinel species, in northeastern Argentina. Fecal samples were screened for Giardia duodenalis infection using a nested PCR reaction, and the gut bacterial community was characterized using 16S rRNA gene amplicon sequencing. Habitat type was correlated with variation in A. caraya gut bacterial community composition but did not affect gut bacterial diversity. Giardia presence did not have a universal effect on A. caraya gut bacteria across habitats, perhaps due to the high infection prevalence across all habitats. However, some bacterial taxa were found to vary with Giardia infection. While A. caraya's behavioral plasticity and dietary flexibility allow them to exploit a range of habitat conditions, habitats are generally becoming more anthropogenically disturbed and, thus, less hospitable. Alterations in gut bacterial community dynamics are one possible indicator of negative health outcomes for A. caraya in these environments, since changes in host-microbe relationships due to stressors from habitat disturbance may lead to negative repercussions for host health. These dynamics are likely relevant for understanding organism responses to environmental change in other mammals.

Infant Skin Bacterial Communities Vary by Skin Site and Infant Age across Populations in Mexico and the United States.

Daily practices put humans in close contact with the surrounding environment, and differences in these practices have an impact on human physiology, development, and health. There is mounting evidence that the microbiome represents an interface that mediates interactions between the human body and the environment. In particular, the skin microbiome serves as the primary interface with the external environment and aids in host immune function by contributing as the first line of defense against pathogens. Despite these important connections, we have only a basic understanding of how the skin microbiome is first established, or which environmental factors contribute to its development. To this end, this study compared the skin bacterial communities of infants (n = 47) living in four populations in Mexico and the United States that span the socioeconomic gradient, where we predicted that variation in physical and social environments would shape the infant skin microbiome. Results of 16S rRNA bacterial gene sequencing on 119 samples (armpit, hand, and forehead) showed that infant skin bacterial diversity and composition are shaped by population-level factors, including those related to socioeconomic status and household composition, and vary by skin site and infant age. Differences in infant-environment interactions, including with other people, appear to vary across the populations, likely influencing infant microbial exposures and, in turn, the composition of infant skin bacterial communities. These findings suggest that variation in microbial exposures stemming from the local environment in infancy can impact the establishment of the skin microbiome across body sites, with implications for developmental and health outcomes.IMPORTANCE This study contributes to the sparse literature on the infant skin microbiome in general, and the virtually nonexistent literature on the infant skin microbiome in a field setting. While microbiome research often addresses patterns at a national scale, this study addresses the influence of population-level factors, such as maternal socioeconomic status and contact with caregivers, on infant skin bacterial communities. This approach strengthens our understanding of how local variables influence the infant skin microbiome, and paves the way for additional studies to combine biological sample collection with questionnaires to adequately capture how specific behaviors dictate infant microbial exposures. Work in this realm has implications for infant care and health, as well as for investigating how the microbial communities of different body sites develop over time, with applications to specific health outcomes associated with the skin microbiome (e.g., immune system development or atopic dermatitis).

Leveraging non-human primates for exploring the social transmission of microbes.

Host social interactions can provide multiple complex pathways for microbial transmission. Here, we suggest non-human primates as models to study the social transmission of commensal or mutualistic microbes due to their high sociality, wide range of group compositions and dominance structures, and diverse group interactions. Microbial sharing from social interactions can positively impact host health by promoting microbial diversity and influencing immunity. Microbes may also drive their own transmission by shaping host behavior, which could lead to fitness benefits for both microbes and hosts. Variation in patterns of social interactions at both the individual and group scale make non-human primates an ideal system to explore the relationship between social behavior, microbial sharing, and their impact on host health and evolution.