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...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
MDPI AG
2022-09-01
|
Series: | Viruses |
Subjects: | |
Online Access: | https://www.mdpi.com/1999-4915/14/10/2125 |
_version_ | 1797469608487157760 |
---|---|
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. |
first_indexed | 2024-03-09T19:23:45Z |
format | Article |
id | doaj.art-2eb5864e84ee49bb9dea288d7544b73a |
institution | Directory Open Access Journal |
issn | 1999-4915 |
language | English |
last_indexed | 2024-03-09T19:23:45Z |
publishDate | 2022-09-01 |
publisher | MDPI AG |
record_format | Article |
series | Viruses |
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 |
work_keys_str_mv | AT aspenmworkman recentemergenceofbovinecoronavirusvariantswithmutationsinthehemagglutininesterasereceptorbindingdomaininuscattle AT taragmcdaneld recentemergenceofbovinecoronavirusvariantswithmutationsinthehemagglutininesterasereceptorbindingdomaininuscattle AT gregorypharhay recentemergenceofbovinecoronavirusvariantswithmutationsinthehemagglutininesterasereceptorbindingdomaininuscattle AT subhadas recentemergenceofbovinecoronavirusvariantswithmutationsinthehemagglutininesterasereceptorbindingdomaininuscattle AT johndustinloy recentemergenceofbovinecoronavirusvariantswithmutationsinthehemagglutininesterasereceptorbindingdomaininuscattle AT benjaminmhause recentemergenceofbovinecoronavirusvariantswithmutationsinthehemagglutininesterasereceptorbindingdomaininuscattle |