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The microbiome of African penguins (Spheniscus demersus) under managed care resembles that of wild marine mammals and birds.

ABSTRACT: Animals under managed care in zoos and aquariums are ideal surrogate study subjects for endangered species that are difficult to obtain in the wild. We compared the fecal and oral microbiomes of healthy, managed African penguins (Spheniscus demersus) to those of other domestic and wild vertebrate hosts to determine how host identity, diet, and environment shape the penguin microbiome. The African penguin oral microbiome was more similar to that of piscivorous marine mammals, suggesting that diet and a marine environment together play a strong role in shaping the oral microbiome. Conversely, the penguin cloaca/fecal microbiome was more similar to that of other birds, suggesting that host phylogeny plays a significant role in shaping the gut microbiome. Although the penguins were born under managed care, they had a gut microbiome more similar to that of wild bird species compared to domesticated (factory-farmed) birds, suggesting that the managed care environment and diet resemble those experienced by wild birds. Finally, the microbiome composition at external body sites was broadly similar to that of the habitat, suggesting sharing of microbes between animals and their environment. Future studies should link these results to microbial functional capacity and host health, which will help inform conservation efforts.

SUBMITTER: Graciette AGC

PROVIDER: S-EPMC10551019 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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The microbiome of African penguins (Spheniscus demersus) under managed care resembles that of wild marine mammals and birds.

Graciette Ana G Clavere AGC Hoopes Lisa A LA Clauss Tonya T Stewart Frank J FJ Pratte Zoe A ZA

Scientific reports 20231004 1

Animals under managed care in zoos and aquariums are ideal surrogate study subjects for endangered species that are difficult to obtain in the wild. We compared the fecal and oral microbiomes of healthy, managed African penguins (Spheniscus demersus) to those of other domestic and wild vertebrate hosts to determine how host identity, diet, and environment shape the penguin microbiome. The African penguin oral microbiome was more similar to that of piscivorous marine mammals, suggesting that diet ...[more]

PMID: 37794122

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Project description:Enterococci are commensals that proliferated as animals crawled ashore hundreds of millions of years ago. They are also leading causes of multidrug-resistant hospital-acquired infections. While most studies are driven by clinical interest, comparatively little is known about enterococci in the wild or the effect of human activity on them. Pharmaceutical pollution and runoff from other human activities are encroaching widely into natural habitats. To assess their reach into remote habitats, we investigated the identity, genetic relatedness, and presence of specific traits among 172 enterococcal isolates from wild Magellanic penguins. Four enterococcal species, 18 lineage groups, and different colonization patterns were identified. One Enterococcus faecalis lineage, sequence type 475 (ST475), was isolated from three different penguins, making it of special interest. Its genome was compared to those of other E. faecalis sequence types (ST116 and ST242) recovered from Magellanic penguins, as well as to an existing phylogeny of E. faecalis isolated from diverse origins over the past 100 years. No penguin-derived E. faecalis strains were closely related to dominant clinical lineages. Most possessed intact CRISPR defenses, few mobile elements, and antibiotic resistances limited to those intrinsic to the species and lacked pathogenic features conveyed by mobile elements. Interestingly, plasmids were identified in penguin isolates that also had been reported for other marine mammals. Enterococci isolated from penguins showed limited anthropogenic impact, indicating that they are likely representative of those naturally circulating in the ecosystem inhabited by the penguins. These findings establish an important baseline for detecting the encroachment of human activity into remote planetary environments.IMPORTANCE Enterococci are host-associated microbes that have an unusually broad range, from the built hospital environment to the guts of insects and other animals in remote locations. Despite their occurrence in the guts of animals for hundreds of millions of years, we know little about the properties that confer this range or how anthropogenic activities may be introducing new selective forces. Magellanic penguins live at the periphery of human habitation. It was of interest to examine enterococci from these animals for the presence of antibiotic resistance and other markers reflective of anthropogenic selection. Diverse enterococcal lineages found discount the existence of a single well-adapted intrinsic penguin-specific species. Instead, they appear to be influenced by a carnivorous lifestyle and enterococci present in the coastal sea life consumed. These results indicate that currently, the penguin habitat remains relatively free of pollutants that select for adaptation to human-derived stressors.

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Dataset Information

The microbiome of African penguins (Spheniscus demersus) under managed care resembles that of wild marine mammals and birds.

Publications

The microbiome of African penguins (Spheniscus demersus) under managed care resembles that of wild marine mammals and birds.

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