Identification and characterization of novel lineage 1 Powassan virus strains in New York State

ABSTRACT

Powassan virus (POWV, family Flaviviridae) is a reemerging tick-borne virus endemic in North America and Russia. In 1997, a POWV-like agent was isolated from Ixodes scapularis in New England and determined to be genetically distinct from the original POWV isolate. This revealed the existence of two lineages: lineage 1, prototype Powassan virus (POWV-1) and lineage 2, deer tick virus (DTV). POWV-1 is thought to be primarily maintained in a cycle between I. cookei and woodchucks and I. marxi and squirrels, while DTV is primarily maintained in a cycle between I. scapularis and small mammal hosts. Recent tick, mammalian, and human isolates from New York State (NYS) have been identified as DTV, but for the first time in 45 years, we detected four POWV-1 isolates, including the first reported isolation of POWV-1 from I. scapularis. We aimed to investigate genotypic and phenotypic characteristics of recent NYS isolates through sequence analysis and evaluation of replication kinetics in vitro and in vivo. Our sequencing revealed genetic divergence between NYS POWV-1 isolates, with two distinct foci. We found that POWV-1 isolates displayed variable replication kinetics in nymphal ticks but not in cell culture. POWV-1 isolated from I. scapularis displayed increased fitness in experimentally infected I. scapularis as compared to historic and recent POWV-1 isolates from I. cookei. These data suggest the emergence of divergent POWV-1 strains in alternate tick hosts and maintenance of genetically and phenotypically discrete POWV-1 foci.

KEYWORDS:

• Powassan virus
• deer tick virus
• New York State
• lineage 1
• Ixodes scapularis

Acknowledgements

The authors would like to thank the New York State Bureau of Communicable Disease Control, NYS county health departments, Lee Ann Sporn and the students at Paul Smith’s College, Jake Sporn and the boat launch stewards of the Adirondack Watershed Institute, Melissa Fierke and associates with the State University of New York (SUNY) College of Environmental Science and Forestry, and Claire Hartl and others from SUNY Brockport and James A Sherwood with the New York State Department of Health for tick collections. We thank the Wadsworth Centre Media and Tissue Culture Core for providing media and cells and the Wadsworth Centre Advanced Genomic Technologies Core for sequencing. We also thank the Centre for Disease Control and Prevention BEI Resources for providing live ticks.

Author contributions

REL, APD, and ATC conceptualized the study. MAP, BB, and JO were involved in sample collection. JGM and CAK were involved in sample processing. KN, CBFV, and NDG developed sequencing methodology and preliminary sequencing results. REL developed in vivo methodology and conducted all experiments. REL and ATC analyzed the data. Funding for the project was acquired by ATC and LDK. REL wrote the original draft. REL, APD, JO, and ATC reviewed and edited the manuscript.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Funding

NYS tick surveillance is supported by the NYSDOH and the National Institutes of Health (grants AI097137 and AI142572). This project was supported by the Cooperative Agreement Number U01CK000509 funded by the Centers for Disease Control and Northeast Center of Excellence. This work was also supported by the National Institutes of Health RNA Science and Technology in Health and Disease Training Grant provided by the Office of Graduate Studies and RNA Institute of the University of Albany. The contents of this publication are solely the responsibility of the authors and do not represent the official views of the Centers for Disease Control and Prevention, National Institutes of Health, or the Department of Health and Human Services.

Correction Statement

This article has been corrected with minor changes. These changes do not impact the academic content of the article.