Recent Emergence of Bovine Coronavirus Variants with Mutations in the Hemagglutinin-Esterase Receptor Binding Domain in U.S. Cattle

Bovine coronavirus (BCoV) has spilled over to many species, including humans, where the host range variant coronavirus OC43 is endemic. The balance of the opposing activities of the surface spike (S) and hemagglutinin-esterase (HE) glycoproteins controls BCoV avidity, which is critical for interspec...

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Main Authors: Aspen M. Workman, Tara G. McDaneld, Gregory P. Harhay, Subha Das, John Dustin Loy, Benjamin M. Hause
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/14/10/2125
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author Aspen M. Workman
Tara G. McDaneld
Gregory P. Harhay
Subha Das
John Dustin Loy
Benjamin M. Hause
author_facet Aspen M. Workman
Tara G. McDaneld
Gregory P. Harhay
Subha Das
John Dustin Loy
Benjamin M. Hause
author_sort Aspen M. Workman
collection DOAJ
description Bovine coronavirus (BCoV) has spilled over to many species, including humans, where the host range variant coronavirus OC43 is endemic. The balance of the opposing activities of the surface spike (S) and hemagglutinin-esterase (HE) glycoproteins controls BCoV avidity, which is critical for interspecies transmission and host adaptation. Here, 78 genomes were sequenced directly from clinical samples collected between 2013 and 2022 from cattle in 12 states, primarily in the Midwestern U.S. Relatively little genetic diversity was observed, with genomes having >98% nucleotide identity. Eleven isolates collected between 2020 and 2022 from four states (Nebraska, Colorado, California, and Wisconsin) contained a 12 nucleotide insertion in the receptor-binding domain (RBD) of the HE gene similar to one recently reported in China, and a single genome from Nebraska collected in 2020 contained a novel 12 nucleotide deletion in the HE gene RBD. Isogenic HE proteins containing either the insertion or deletion in the HE RBD maintained esterase activity and could bind bovine submaxillary mucin, a substrate enriched in the receptor 9-<i>O</i>-acetylated-sialic acid, despite modeling that predicted structural changes in the HE R3 loop critical for receptor binding. The emergence of BCoV with structural variants in the RBD raises the possibility of further interspecies transmission.
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spelling doaj.art-2eb5864e84ee49bb9dea288d7544b73a2023-11-24T03:07:52ZengMDPI AGViruses1999-49152022-09-011410212510.3390/v14102125Recent Emergence of Bovine Coronavirus Variants with Mutations in the Hemagglutinin-Esterase Receptor Binding Domain in U.S. CattleAspen M. Workman0Tara G. McDaneld1Gregory P. Harhay2Subha Das3John Dustin Loy4Benjamin M. Hause5United States Department of Agriculture (USDA) Agricultural Research Service (ARS), US Meat Animal Research Center (USMARC), State Spur 18D, Clay Center, NE 68933, USAUnited States Department of Agriculture (USDA) Agricultural Research Service (ARS), US Meat Animal Research Center (USMARC), State Spur 18D, Clay Center, NE 68933, USAUnited States Department of Agriculture (USDA) Agricultural Research Service (ARS), US Meat Animal Research Center (USMARC), State Spur 18D, Clay Center, NE 68933, USAVeterinary & Biomedical Sciences, South Dakota State University, Brookings, SD 57007, USANebraska Veterinary Diagnostic Center, School of Veterinary Medicine and Biomedical Sciences, University of Nebraska-Lincoln, 4040 East Campus Loop N, Lincoln, NE 68503, USAVeterinary & Biomedical Sciences, South Dakota State University, Brookings, SD 57007, USABovine coronavirus (BCoV) has spilled over to many species, including humans, where the host range variant coronavirus OC43 is endemic. The balance of the opposing activities of the surface spike (S) and hemagglutinin-esterase (HE) glycoproteins controls BCoV avidity, which is critical for interspecies transmission and host adaptation. Here, 78 genomes were sequenced directly from clinical samples collected between 2013 and 2022 from cattle in 12 states, primarily in the Midwestern U.S. Relatively little genetic diversity was observed, with genomes having >98% nucleotide identity. Eleven isolates collected between 2020 and 2022 from four states (Nebraska, Colorado, California, and Wisconsin) contained a 12 nucleotide insertion in the receptor-binding domain (RBD) of the HE gene similar to one recently reported in China, and a single genome from Nebraska collected in 2020 contained a novel 12 nucleotide deletion in the HE gene RBD. Isogenic HE proteins containing either the insertion or deletion in the HE RBD maintained esterase activity and could bind bovine submaxillary mucin, a substrate enriched in the receptor 9-<i>O</i>-acetylated-sialic acid, despite modeling that predicted structural changes in the HE R3 loop critical for receptor binding. The emergence of BCoV with structural variants in the RBD raises the possibility of further interspecies transmission.https://www.mdpi.com/1999-4915/14/10/2125bovine coronavirushemagglutinin-esterasevariantbovine respiratory diseasecalf diarrhea
spellingShingle Aspen M. Workman
Tara G. McDaneld
Gregory P. Harhay
Subha Das
John Dustin Loy
Benjamin M. Hause
Recent Emergence of Bovine Coronavirus Variants with Mutations in the Hemagglutinin-Esterase Receptor Binding Domain in U.S. Cattle
Viruses
bovine coronavirus
hemagglutinin-esterase
variant
bovine respiratory disease
calf diarrhea
title Recent Emergence of Bovine Coronavirus Variants with Mutations in the Hemagglutinin-Esterase Receptor Binding Domain in U.S. Cattle
title_full Recent Emergence of Bovine Coronavirus Variants with Mutations in the Hemagglutinin-Esterase Receptor Binding Domain in U.S. Cattle
title_fullStr Recent Emergence of Bovine Coronavirus Variants with Mutations in the Hemagglutinin-Esterase Receptor Binding Domain in U.S. Cattle
title_full_unstemmed Recent Emergence of Bovine Coronavirus Variants with Mutations in the Hemagglutinin-Esterase Receptor Binding Domain in U.S. Cattle
title_short Recent Emergence of Bovine Coronavirus Variants with Mutations in the Hemagglutinin-Esterase Receptor Binding Domain in U.S. Cattle
title_sort recent emergence of bovine coronavirus variants with mutations in the hemagglutinin esterase receptor binding domain in u s cattle
topic bovine coronavirus
hemagglutinin-esterase
variant
bovine respiratory disease
calf diarrhea
url https://www.mdpi.com/1999-4915/14/10/2125
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