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Environmental Microbiology | Spotlight

Enterococci from Wild Magellanic Penguins (Spheniscus magellanicus) as an Indicator of Marine Ecosystem Health and Human Impact

Janira Prichula, Daria Van Tyne, Julia Schwartzman, Fernando Hayashi Sant’Anna, Rebeca Inhoque Pereira, Gabriela Rosa da Cunha, Maurício Tavares, François Lebreton, Jeverson Frazzon, Pedro Alves d’Azevedo, Adriana Seixas, Ana Paula Guedes Frazzon, Michael S. Gilmore
Edward G. Dudley, Editor
Janira Prichula
aGram-positive Cocci Laboratory, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Rio Grande do Sul, Brazil
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  • ORCID record for Janira Prichula
Daria Van Tyne
bDepartment of Ophthalmology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA
cDepartment of Microbiology, Harvard Medical School, Boston, Massachusetts, USA
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Julia Schwartzman
bDepartment of Ophthalmology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA
cDepartment of Microbiology, Harvard Medical School, Boston, Massachusetts, USA
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Fernando Hayashi Sant’Anna
dDepartment of Genetics, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Rio Grande do Sul, Brazil
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Rebeca Inhoque Pereira
aGram-positive Cocci Laboratory, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Rio Grande do Sul, Brazil
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Gabriela Rosa da Cunha
aGram-positive Cocci Laboratory, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Rio Grande do Sul, Brazil
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Maurício Tavares
eCentro de Estudos Costeiros, Limnológicos e Marinhos (CECLIMAR), Campus Litoral Norte, UFRGS, UFRGS, Imbé, Rio Grande do Sul, Brazil
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François Lebreton
bDepartment of Ophthalmology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA
cDepartment of Microbiology, Harvard Medical School, Boston, Massachusetts, USA
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Jeverson Frazzon
fFood Science Institute, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
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Pedro Alves d’Azevedo
aGram-positive Cocci Laboratory, Federal University of Health Sciences of Porto Alegre (UFCSPA), Porto Alegre, Rio Grande do Sul, Brazil
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Adriana Seixas
gDepartment of Pharmacosciences, UFCSPA, Porto Alegre, Rio Grande do Sul, Brazil
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Ana Paula Guedes Frazzon
hDepartment of Microbiology, Immunology and Parasitology, UFRGS, Porto Alegre, Rio Grande do Sul, Brazil
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Michael S. Gilmore
bDepartment of Ophthalmology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA
cDepartment of Microbiology, Harvard Medical School, Boston, Massachusetts, USA
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Edward G. Dudley
The Pennsylvania State University
Roles: Editor
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DOI: 10.1128/AEM.01662-20
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ABSTRACT

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.

FOOTNOTES

    • Received 21 July 2020.
    • Accepted 23 July 2020.
    • Accepted manuscript posted online 31 July 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Enterococci from Wild Magellanic Penguins (Spheniscus magellanicus) as an Indicator of Marine Ecosystem Health and Human Impact
Janira Prichula, Daria Van Tyne, Julia Schwartzman, Fernando Hayashi Sant’Anna, Rebeca Inhoque Pereira, Gabriela Rosa da Cunha, Maurício Tavares, François Lebreton, Jeverson Frazzon, Pedro Alves d’Azevedo, Adriana Seixas, Ana Paula Guedes Frazzon, Michael S. Gilmore
Applied and Environmental Microbiology Sep 2020, 86 (19) e01662-20; DOI: 10.1128/AEM.01662-20

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Enterococci from Wild Magellanic Penguins (Spheniscus magellanicus) as an Indicator of Marine Ecosystem Health and Human Impact
Janira Prichula, Daria Van Tyne, Julia Schwartzman, Fernando Hayashi Sant’Anna, Rebeca Inhoque Pereira, Gabriela Rosa da Cunha, Maurício Tavares, François Lebreton, Jeverson Frazzon, Pedro Alves d’Azevedo, Adriana Seixas, Ana Paula Guedes Frazzon, Michael S. Gilmore
Applied and Environmental Microbiology Sep 2020, 86 (19) e01662-20; DOI: 10.1128/AEM.01662-20
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KEYWORDS

enterococci
genetic diversity
plasmids
wild Magellanic penguin
marine ecosystem health

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