Applications of VirScan to broad serological profiling of bat reservoirs for emerging zoonoses

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Abstract

Introduction

Bats are important providers of ecosystem services such as pollination, seed dispersal, and insect control but also act as natural reservoirs for virulent zoonotic viruses. Bats host multiple viruses that cause life-threatening pathology in other animals and humans but, themselves, experience limited pathological disease from infection. Despite bats’ importance as reservoirs for several zoonotic viruses, we know little about the broader viral diversity that they host. Bat virus surveillance efforts are challenged by difficulties of field capture and the limited scope of targeted PCR- or ELISA-based molecular and serological detection. Additionally, virus shedding is often transient, thus also limiting insights gained from nucleic acid testing of field specimens. Phage ImmunoPrecipitation Sequencing (PhIP-Seq), a broad serological tool used previously to comprehensively profile viral exposure history in humans, offers an exciting prospect for viral surveillance efforts in wildlife, including bats.

Methods

Here, for the first time, we apply PhIP-Seq technology to bat serum, using a viral peptide library originally designed to simultaneously assay exposures to the entire human virome.

Results

Using VirScan, we identified past exposures to 57 viral genera—including betacoronaviruses, henipaviruses, lyssaviruses, and filoviruses—in semi-captive Pteropus alecto and to nine viral genera in captive Eonycteris spelaea. Consistent with results from humans, we find that both total peptide hits (the number of enriched viral peptides in our library) and the corresponding number of inferred past virus exposures in bat hosts were correlated with poor bat body condition scores and increased with age. High and low body condition scores were associated with either seropositive or seronegative status for different viruses, though in general, virus-specific age-seroprevalence curves defied assumptions of lifelong immunizing infection, suggesting that many bat viruses may circulate via complex transmission dynamics.

Discussion

Overall, our work emphasizes the utility of applying biomedical tools, like PhIP-Seq, first developed for humans to viral surveillance efforts in wildlife, while highlighting opportunities for taxon-specific improvements.

Related collections

Most cited references 74

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Bats are natural reservoirs of SARS-like coronaviruses.

Wendong Li, Zhengli Shi, Meng Yu … (2005)

Severe acute respiratory syndrome (SARS) emerged in 2002 to 2003 in southern China. The origin of its etiological agent, the SARS coronavirus (SARS-CoV), remains elusive. Here we report that species of bats are a natural host of coronaviruses closely related to those responsible for the SARS outbreak. These viruses, termed SARS-like coronaviruses (SL-CoVs), display greater genetic variation than SARS-CoV isolated from humans or from civets. The human and civet isolates of SARS-CoV nestle phylogenetically within the spectrum of SL-CoVs, indicating that the virus responsible for the SARS outbreak was a member of this coronavirus group.

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Viral epitope profiling of COVID-19 patients reveals cross-reactivity and correlates of severity

Ellen Shrock, Eric Fujimura, Tomasz Kula … (2020)

Profiling coronaviruses Among the coronaviruses that infect humans, four cause mild common colds, whereas three others, including the currently circulating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), result in severe infections. Shrock et al. used a technology known as VirScan to probe the antibody repertoires of hundreds of coronavirus disease 2019 (COVID-19) patients and pre–COVID-19 era controls. They identified hundreds of antibody targets, including several antibody epitopes shared by the mild and severe coronaviruses and many specific to SARS-CoV-2. A machine-learning model accurately classified patients infected with SARS-CoV-2 and guided the design of an assay for rapid SARS-CoV-2 antibody detection. The study also looked at how the antibody response and viral exposure history differ in patients with diverging outcomes, which could inform the production of improved vaccine and antibody therapies. Science, this issue p. eabd4250

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Pathways to zoonotic spillover

Raina K. Plowright, Colin Parrish, Hamish McCallum … (2017)

Zoonotic diseases present a substantial global health burden. In this Opinion article, Plowrightet al. present an integrative conceptual and quantitative model that reveals that all zoonotic pathogens must overcome a hierarchical series of barriers to cause spillover infections in humans. Supplementary information The online version of this article (doi:10.1038/nrmicro.2017.45) contains supplementary material, which is available to authorized users.

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Author and article information

Contributors

Emily Cornelius Ruhs: URI : https://loop.frontiersin.org/people/1950774/overview

Wan Ni Chia: URI : https://loop.frontiersin.org/people/181003/overview

Alison J. Peel: URI : https://loop.frontiersin.org/people/760008/overview

H. Benjamin Larman: URI : https://loop.frontiersin.org/people/1185217/overview

Aaron T. Irving: URI : https://loop.frontiersin.org/people/18312/overview

Linfa Wang: URI : https://loop.frontiersin.org/people/18556/overview

Cara E. Brook: URI : https://loop.frontiersin.org/people/1232308/overview

Journal

Journal ID (nlm-ta): Front Public Health

Journal ID (iso-abbrev): Front Public Health

Journal ID (publisher-id): Front. Public Health

Title: Frontiers in Public Health

Publisher: Frontiers Media S.A.

ISSN (Electronic): 2296-2565

Publication date (Electronic): 22 September 2023

Publication date Collection: 2023

Volume: 11

Electronic Location Identifier: 1212018

Affiliations

[1] ¹Department of Ecology and Evolution, University of Chicago , Chicago, IL, United States

[2] ²Grainger Bioinformatics Center, Field Museum of Natural History , Chicago, IL, United States

[3] ³Program in Emerging Infectious Diseases, Duke-NUS Medical School , Singapore, Singapore

[4] ⁴CoV Biotechnology Pte Ltd. , Singapore, Singapore

[5] ⁵Centre for Planetary Health and Food Security, School of Environment and Science, Griffith University , Brisband, QLD, Australia

[6] ⁶Quantitative and Computational Biology, Princeton University , Princeton, NJ, United States

[7] ⁷HBL – Institute for Cell Engineering, Division of Immunology, Department of Pathology, Johns Hopkins University , Baltimore, MD, United States

[8] ⁸Second Affiliated Hospital of Zhejiang University, Zhejiang University School of Medicine , Hangzhou, Zhejiang, China

[9] ⁹Zhejiang University-University of Edinburgh Institute , Haining, Zhejiang, China

[10] ¹⁰BIMET - Biomedical and Translational Research Centre of Zhejiang Province , Zhejiang Province, China

[11] ¹¹SingHealth Duke-NUS Global Health Institute , Singapore, Singapore

Author notes

Edited by: Haibo Wu, Zhejiang University, China

Reviewed by: Sreelekshmy Mohandas, Indian Council of Medical Research (ICMR), India; Anita Shete, Indian Council of Medical Research (ICMR), India

*Correspondence: Emily Cornelius Ruhs, ecruhs@ 123456uchicago.edu

^†These authors share senior authorship

Article

DOI: 10.3389/fpubh.2023.1212018

PMC ID: 10559906

PubMed ID: 37808979

SO-VID: 9a2ec736-8b27-436e-a326-f030ddc88234

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 25 April 2023

Date accepted : 04 September 2023

Page count

Figures: 6, Tables: 0, Equations: 0, References: 76, Pages: 12, Words: 9696

Funding

Funded by: Griffith University, doi 10.13039/501100001791;

Award ID: DE190100710

Funded by: University of Chicago, doi 10.13039/100007234;

Funded by: National Research Foundation, doi 10.13039/501100001321;

Funded by: National Medical Research Council, doi 10.13039/501100001349;

Custom metadata

section-at-acceptance Infectious Diseases: Epidemiology and Prevention

Keywords: chiroptera,phip-seq,surveillance,virscan,virus

Data availability:

Keywords: chiroptera, phip-seq, surveillance, virscan, virus

Applications of VirScan to broad serological profiling of bat reservoirs for emerging zoonoses

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Abstract

Introduction

Methods

Results

Discussion

Related collections

Zoonoses

Most cited references 74

Bats are natural reservoirs of SARS-like coronaviruses.

Viral epitope profiling of COVID-19 patients reveals cross-reactivity and correlates of severity

Pathways to zoonotic spillover

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