Influenza A viruses in gulls in landfills and freshwater habitats in Minnesota, United States

Elizabeth A Rasmussen; Agata Czaja; Francesca J Cuthbert; Gene S Tan; Philippe Lemey; Martha I Nelson; Marie R Culhane

doi:10.3389/fgene.2023.1172048

Influenza A viruses in gulls in landfills and freshwater habitats in Minnesota, United States

Front Genet. 2023 May 9:14:1172048. doi: 10.3389/fgene.2023.1172048. eCollection 2023.

Authors

Elizabeth A Rasmussen¹, Agata Czaja², Francesca J Cuthbert³, Gene S Tan⁴, Philippe Lemey⁵, Martha I Nelson², Marie R Culhane¹

Affiliations

¹ Department of Veterinary Population Medicine, College of Veterinary Medicine, University of Minnesota, Saint Paul, MN, United States.
² Computational Biology Branch, National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, United States.
³ Department of Fisheries, Wildlife and Conservation Biology, College of Food, Agricultural and Natural Resource Sciences, University of Minnesota, Minneapolis, MN, United States.
⁴ J. Craig Venter Institute, La Jolla, Division of Infectious Diseases, Department of Medicine, University of California San Diego, La Jolla, CA, United States.
⁵ Department of Microbiology, Immunology and Transplantation, Rega Institute, KU Leuven, Leuven, Belgium.

Abstract

Introduction: The unpredictable evolution of avian influenza viruses (AIVs) presents an ongoing threat to agricultural production and public and wildlife health. Severe outbreaks of highly pathogenic H5N1 viruses in US poultry and wild birds since 2022 highlight the urgent need to understand the changing ecology of AIV. Surveillance of gulls in marine coastal environments has intensified in recent years to learn how their long-range pelagic movements potentially facilitate inter-hemispheric AIV movements. In contrast, little is known about inland gulls and their role in AIV spillover, maintenance, and long-range dissemination. Methods: To address this gap, we conducted active AIV surveillance in ring-billed gulls (Larus delawarensis) and Franklin's gulls (Leucophaeus pipixcan) in Minnesota's natural freshwater lakes during the summer breeding season and in landfills during fall migration (1,686 samples). Results: Whole-genome AIV sequences obtained from 40 individuals revealed three-lineage reassortants with a mix of genome segments from the avian Americas lineage, avian Eurasian lineage, and a global "Gull" lineage that diverged more than 50 years ago from the rest of the AIV global gene pool. No poultry viruses contained gull-adapted H13, NP, or NS genes, pointing to limited spillover. Geolocators traced gull migration routes across multiple North American flyways, explaining how inland gulls imported diverse AIV lineages from distant locations. Migration patterns were highly varied and deviated far from assumed "textbook" routes. Discussion: Viruses circulating in Minnesota gulls during the summer breeding season in freshwater environments reappeared in autumn landfills, evidence of AIV persistence in gulls between seasons and transmission between habitats. Going forward, wider adoption of technological advances in animal tracking devices and genetic sequencing is needed to expand AIV surveillance in understudied hosts and habitats.

Keywords: franklin's gull; freshwater; influenza; migration; minnesota; ring-billed gull.

Grants and funding

Whole genome sequencing for this project and GT have been funded in whole or part with federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services under Award Number U19AI110819 and as part of the Influenza Genome Sequencing Project, Grant ID HHSN272200900007C, National Institutes of Allergy and Infectious Diseases. MN is supported by the Intramural Research Program of the US National Library of Medicine at the NIH. This work was supported by the Centers of Excellence for Influenza Research and Response, National Institute of Allergy and Infectious Diseases, National Institutes of Health (NIH), Department of Health and Human Services, under contract 75N93021C00014. This work conducted by ER, MC, and FC at the University of Minnesota were supported in whole or in part by the following organizations and research grants: the Minnesota Agricultural Experimental Station 2020 Avian Influenza Program grant (CON 81431, Project 85606), “Capturing movements of avian influenza virus from wild birds to domestic poultry in Minnesota,” Minnesota Agricultural Experimental Station 2015 Avian Influenza Program grant (CON 58786, Project 72634) “Defining the role gull species play in the disease ecology of avian influenza in Minnesota,” and the Environment and Natural Resources Trust Fund from the Legislative–Citizen Commission on Minnesota Resources program grant M.L. 2016, “Avian Influenza distribution, evolution, and impacts on ring-billed and herring gulls in Minnesota.”