An official website of the United States government
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.
more »
« less
Data from: The meta-gut: community coalescence of animal gut and environmental microbiomes
{"Abstract":["This is the data and R code necessary to reproduce the findings in the manuscript, "The meta-gut: community coalescence of animal gut and environmental microbiomes."\n\nHippo pool biogeochemistry and fecal and pool water microbial communities were examined through field sampling and an experiment. Sequencing using 16S RNA methods revealed that the active microbial communities in hippo pools that received high inputs of hippo feces are more similar to the hippo gut microbiome than other nearby aquatic environments. The overlap between the microbiomes of the hippo gut and the waters into which they excrete therefore constitutes a meta-gut system with potentially strong influence on the biogeochemistry of pools and downstream waters. We propose that the meta-gut may be present where other species congregate in high densities, particularly in aquatic environments, and share gut microbiota between individuals."]}
more »
« less
- Award ID(s):
- 2103884
- PAR ID:
- 10352417
- Publisher / Repository:
- Mendeley
- Date Published:
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Given the rapidly changing landscapes of habitats across the globe, a sound understanding of host-associated microbial communities and the ecoevolutionary forces that shape them is needed to assess general organismal adaptability. Knowledge of the symbiotic endogenous microbiomes of most reptilian species worldwide remains limited. We sampled gut microbiomes of geckos spanning nine species and four genera in the Philippines to (i) provide baseline data on gut microbiota in these host species, (ii) test for significant associations between host phylogenetic relationships and observed microbial assemblages, potentially indicative of phylosymbiosis, and (iii) identify correlations between multiple ecoevolutionary factors (e.g. species identity, habitat tendencies, range extents, and maximum body sizes) and gut microbiomes in Philippine gekkonids. We recovered no significant association between interspecific host genetic distances and observed gut microbiomes, providing limited evidence for phylosymbiosis in this group. Philippine gekkonid microbiomes were associated most heavily with host species identity, though marked variation among conspecifics at distinct sampling sites indicates that host locality influences gut microbiomes as well. Interestingly, individuals grouped as widespread and microendemic regardless of host species identity displayed significant differences in alpha and beta diversity metrics examined, likely driven by differences in rare OTU presence between groups. These results provide much needed insight in host-associated microbiomes in wild reptiles and the ecoevolutionary forces that structure such communities.more » « less
-
Microbial rewilding in the gut microbiomes of captive ring-tailed lemurs (Lemur catta) in MadagascarAbstract 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.more » « less
-
Abstract Animals often shape environmental microbial communities, which can in turn influence animal gut microbiomes. Invasive species in critical habitats may reduce grazing pressure from native species and shift microbial communities. The landlocked coastal ponds, pools, and caves that make up the Hawaiian anchialine ecosystem support an endemic shrimp (Halocaridina rubra) that grazes on diverse benthic microbial communities, including orange cyanobacterial‐bacterial crusts and green algal mats. Here, we asked how shrimp: (1) shape the abundance and composition of microbial communities, (2) respond to invasive fishes, and (3) whether their gut microbiomes are affected by environmental microbial communities. We demonstrate that ecologically relevant levels of shrimp grazing significantly reduce epilithon biomass. Shrimp grazed readily and grew well on both orange crusts and green mat communities. However, individuals from orange crusts were larger, despite crusts having reduced concentrations of key fatty acids. DNA profiling revealed shrimp harbor a resident gut microbiome distinct from the environment, which is relatively simple and stable across space (including habitats with different microbial communities) and time (between wild‐caught individuals and those maintained in the laboratory for >2 yr). DNA profiling also suggests shrimp grazing alters environmental microbial community composition, possibly through selective consumption and/or physical interactions. While this work suggests grazing by endemic shrimp plays a key role in shaping microbial communities in the Hawaiian anchialine ecosystem, the hypothesized drastic ecological shifts resulting from invasive fishes may be an oversimplification as shrimp may largely avoid predation. Moreover, environmental microbial communities may have little influence on shrimp gut microbiomes.more » « less
-
Schloss, P. D. (Ed.)ABSTRACT The European honey bee ( Apis mellifera ) is used extensively to produce hive products and for crop pollination, but pervasive concerns about colony health and population decline have sparked an interest in the microbial communities that are associated with these important insects. Currently, only the microbiome of workers has been characterized, while little to nothing is known about the bacterial communities that are associated with queens, even though their health and proper function are central to colony productivity. Here, we provide a large-scale analysis of the gut microbiome of honey bee queens during their developmental trajectory and through the multiple colonies that host them as part of modern queen-rearing practices. We found that queen microbiomes underwent a dramatic shift in size and composition as they aged and encountered different worker populations and colony environments. Queen microbiomes were dominated by enteric bacteria in early life but were comprised primarily of alphaproteobacteria at maturity. Furthermore, queen gut microbiomes did not reflect those of the workers who tended them and, indeed, they lacked many of the bacteria that are considered vital to workers. While worker gut microbiotas were consistent across the unrelated colony populations sampled, the microbiotas of the related queens were highly variable. Bacterial communities in mature queen guts were similar in size to those of mature workers and were characterized by dominant and specific alphaproteobacterial strains known to be associated with worker hypopharyngeal glands. Our results suggest a model in which queen guts are colonized by bacteria from workers' glands, in contrast to routes of maternal inoculation for other animal microbiomes.more » « less
