Spatial epidemiology and genetic diversity of SARS-CoV-2 and related coronaviruses in domestic and wild animals

The Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) showed susceptibility to diverse animal species. We conducted this study to understand the spatial epidemiology, genetic diversity, and statistically significant genetic similarity along with per-gene recombination events of SARS-CoV-2...

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Veröffentlicht in:PloS one 2021-12, Vol.16 (12), p.e0260635
Hauptverfasser: Islam, Ariful, Ferdous, Jinnat, Sayeed, Md Abu, Islam, Shariful, Kaisar Rahman, Md, Abedin, Josefina, Saha, Otun, Hassan, Mohammad Mahmudul, Shirin, Tahmina
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container_title PloS one
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creator Islam, Ariful
Ferdous, Jinnat
Sayeed, Md Abu
Islam, Shariful
Kaisar Rahman, Md
Abedin, Josefina
Saha, Otun
Hassan, Mohammad Mahmudul
Shirin, Tahmina
description The Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) showed susceptibility to diverse animal species. We conducted this study to understand the spatial epidemiology, genetic diversity, and statistically significant genetic similarity along with per-gene recombination events of SARS-CoV-2 and related viruses (SC2r-CoVs) in animals globally. We collected a number of different animal species infected with SARS-CoV-2 and its related viruses. Then, we retrieved genome sequences of SARS-CoV-2 and SC2r-CoVs from GISAID and NCBI GenBank for genomic and mutational analysis. Although the evolutionary origin of SARS-CoV-2 remains elusive, the diverse SC2r-CoV have been detected in multiple Rhinolophus bat species and in Malayan pangolin. To date, human-to-animal spillover events have been reported in cat, dog, tiger, lion, gorilla, leopard, ferret, puma, cougar, otter, and mink in 25 countries. Phylogeny and genetic recombination events of SC2r-CoVs showed higher similarity to the bat coronavirus RaTG13 and BANAL-103 for most of the genes and to some Malayan pangolin coronavirus (CoV) strains for the N protein from bats and pangolin showed close resemblance to SARS-CoV-2. The clustering of animal and human strains from the same geographical area has proved human-to-animal transmission of the virus. The Alpha, Delta and Mu-variant of SARS-CoV-2 was detected in dog, gorilla, lion, tiger, otter, and cat in the USA, India, Czech Republic, Belgium, and France with momentous genetic similarity with human SARS-CoV-2 sequences. The mink variant mutation (spike_Y453F) was detected in both humans and domestic cats. Moreover, the dog was affected mostly by clade O (66.7%), whereas cat and American mink were affected by clade GR (31.6 and 49.7%, respectively). The α-variant was detected as 2.6% in cat, 4.8% in dog, 14.3% in tiger, 66.7% in gorilla, and 77.3% in lion. The highest mutations observed in mink where the substitution of D614G in spike (95.2%) and P323L in NSP12 (95.2%) protein. In dog, cat, gorilla, lion, and tiger, Y505H and Y453F were the common mutations followed by Y145del, Y144del, and V70I in S protein. We recommend vaccine provision for pet and zoo animals to reduce the chance of transmission in animals. Besides, continuous epidemiological and genomic surveillance of coronaviruses in animal host is crucial to find out the immediate ancestor of SARS-CoV-2 and to prevent future CoVs threats to humans.
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We conducted this study to understand the spatial epidemiology, genetic diversity, and statistically significant genetic similarity along with per-gene recombination events of SARS-CoV-2 and related viruses (SC2r-CoVs) in animals globally. We collected a number of different animal species infected with SARS-CoV-2 and its related viruses. Then, we retrieved genome sequences of SARS-CoV-2 and SC2r-CoVs from GISAID and NCBI GenBank for genomic and mutational analysis. Although the evolutionary origin of SARS-CoV-2 remains elusive, the diverse SC2r-CoV have been detected in multiple Rhinolophus bat species and in Malayan pangolin. To date, human-to-animal spillover events have been reported in cat, dog, tiger, lion, gorilla, leopard, ferret, puma, cougar, otter, and mink in 25 countries. Phylogeny and genetic recombination events of SC2r-CoVs showed higher similarity to the bat coronavirus RaTG13 and BANAL-103 for most of the genes and to some Malayan pangolin coronavirus (CoV) strains for the N protein from bats and pangolin showed close resemblance to SARS-CoV-2. The clustering of animal and human strains from the same geographical area has proved human-to-animal transmission of the virus. The Alpha, Delta and Mu-variant of SARS-CoV-2 was detected in dog, gorilla, lion, tiger, otter, and cat in the USA, India, Czech Republic, Belgium, and France with momentous genetic similarity with human SARS-CoV-2 sequences. The mink variant mutation (spike_Y453F) was detected in both humans and domestic cats. Moreover, the dog was affected mostly by clade O (66.7%), whereas cat and American mink were affected by clade GR (31.6 and 49.7%, respectively). The α-variant was detected as 2.6% in cat, 4.8% in dog, 14.3% in tiger, 66.7% in gorilla, and 77.3% in lion. The highest mutations observed in mink where the substitution of D614G in spike (95.2%) and P323L in NSP12 (95.2%) protein. In dog, cat, gorilla, lion, and tiger, Y505H and Y453F were the common mutations followed by Y145del, Y144del, and V70I in S protein. We recommend vaccine provision for pet and zoo animals to reduce the chance of transmission in animals. Besides, continuous epidemiological and genomic surveillance of coronaviruses in animal host is crucial to find out the immediate ancestor of SARS-CoV-2 and to prevent future CoVs threats to humans.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0260635</identifier><identifier>PMID: 34910734</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal species ; Animals ; Animals, Domestic - virology ; Animals, Wild - virology ; Bats ; Biology and life sciences ; Clustering ; Coronaviridae ; Coronaviruses ; COVID-19 ; COVID-19 - epidemiology ; COVID-19 - transmission ; COVID-19 - virology ; Disease control ; Disease transmission ; Dogs ; Domestic animals ; Epidemics ; Epidemiology ; Evaluation ; Evolution ; Gene sequencing ; Genes ; Genetic diversity ; Genetic Variation ; Genome, Viral ; Genomes ; Genomics ; Humans ; Infections ; Mammals ; Medicine and health sciences ; Metadata ; Mutation ; N protein ; Pandemics ; Pangolins - virology ; Phylogenetics ; Phylogeny ; Proteins ; Recombination ; Recombination, Genetic ; Respiratory diseases ; SARS-CoV-2 - classification ; SARS-CoV-2 - genetics ; SARS-CoV-2 - isolation &amp; purification ; Severe acute respiratory syndrome ; Severe acute respiratory syndrome coronavirus 2 ; Similarity ; Species ; Statistical analysis ; Strains (organisms) ; Vaccines ; Veterinary medicine ; Viral diseases ; Viruses ; Wild animals ; Zoo animals</subject><ispartof>PloS one, 2021-12, Vol.16 (12), p.e0260635</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Islam et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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We conducted this study to understand the spatial epidemiology, genetic diversity, and statistically significant genetic similarity along with per-gene recombination events of SARS-CoV-2 and related viruses (SC2r-CoVs) in animals globally. We collected a number of different animal species infected with SARS-CoV-2 and its related viruses. Then, we retrieved genome sequences of SARS-CoV-2 and SC2r-CoVs from GISAID and NCBI GenBank for genomic and mutational analysis. Although the evolutionary origin of SARS-CoV-2 remains elusive, the diverse SC2r-CoV have been detected in multiple Rhinolophus bat species and in Malayan pangolin. To date, human-to-animal spillover events have been reported in cat, dog, tiger, lion, gorilla, leopard, ferret, puma, cougar, otter, and mink in 25 countries. Phylogeny and genetic recombination events of SC2r-CoVs showed higher similarity to the bat coronavirus RaTG13 and BANAL-103 for most of the genes and to some Malayan pangolin coronavirus (CoV) strains for the N protein from bats and pangolin showed close resemblance to SARS-CoV-2. The clustering of animal and human strains from the same geographical area has proved human-to-animal transmission of the virus. The Alpha, Delta and Mu-variant of SARS-CoV-2 was detected in dog, gorilla, lion, tiger, otter, and cat in the USA, India, Czech Republic, Belgium, and France with momentous genetic similarity with human SARS-CoV-2 sequences. The mink variant mutation (spike_Y453F) was detected in both humans and domestic cats. Moreover, the dog was affected mostly by clade O (66.7%), whereas cat and American mink were affected by clade GR (31.6 and 49.7%, respectively). The α-variant was detected as 2.6% in cat, 4.8% in dog, 14.3% in tiger, 66.7% in gorilla, and 77.3% in lion. The highest mutations observed in mink where the substitution of D614G in spike (95.2%) and P323L in NSP12 (95.2%) protein. In dog, cat, gorilla, lion, and tiger, Y505H and Y453F were the common mutations followed by Y145del, Y144del, and V70I in S protein. We recommend vaccine provision for pet and zoo animals to reduce the chance of transmission in animals. Besides, continuous epidemiological and genomic surveillance of coronaviruses in animal host is crucial to find out the immediate ancestor of SARS-CoV-2 and to prevent future CoVs threats to humans.</description><subject>Animal species</subject><subject>Animals</subject><subject>Animals, Domestic - virology</subject><subject>Animals, Wild - virology</subject><subject>Bats</subject><subject>Biology and life sciences</subject><subject>Clustering</subject><subject>Coronaviridae</subject><subject>Coronaviruses</subject><subject>COVID-19</subject><subject>COVID-19 - epidemiology</subject><subject>COVID-19 - transmission</subject><subject>COVID-19 - virology</subject><subject>Disease control</subject><subject>Disease transmission</subject><subject>Dogs</subject><subject>Domestic animals</subject><subject>Epidemics</subject><subject>Epidemiology</subject><subject>Evaluation</subject><subject>Evolution</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic diversity</subject><subject>Genetic Variation</subject><subject>Genome, Viral</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Humans</subject><subject>Infections</subject><subject>Mammals</subject><subject>Medicine and health sciences</subject><subject>Metadata</subject><subject>Mutation</subject><subject>N protein</subject><subject>Pandemics</subject><subject>Pangolins - virology</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Proteins</subject><subject>Recombination</subject><subject>Recombination, Genetic</subject><subject>Respiratory diseases</subject><subject>SARS-CoV-2 - classification</subject><subject>SARS-CoV-2 - genetics</subject><subject>SARS-CoV-2 - isolation &amp; purification</subject><subject>Severe acute respiratory syndrome</subject><subject>Severe acute respiratory syndrome coronavirus 2</subject><subject>Similarity</subject><subject>Species</subject><subject>Statistical analysis</subject><subject>Strains (organisms)</subject><subject>Vaccines</subject><subject>Veterinary medicine</subject><subject>Viral diseases</subject><subject>Viruses</subject><subject>Wild animals</subject><subject>Zoo animals</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11r2zAUhs3YWLtu_2BshsHYLpzpw5alm0EI-wgUCs3WWyHrw1FRrEyys-XfT27SEo9eDF1ISM95j84rnSx7DcEM4hp-uvVD6ISbbX2nZwARQHD1JDuHDKOCIICfnqzPshcx3gJQYUrI8-wMlwyCGpfnmV9tRW-Fy_XWKr2x3vl2n4tO5a3udG9lruxOh2j7fe5Nvppfr4qFvynQHRO0E71WufTBd2JnwxB1zG2XK7_RcYweqd_WqbSwG-Hiy-yZSZN-dZwvsp9fv_xYfC8ur74tF_PLQhKG-sIgUhFU4qY0wAjJyoqqRjZGN4QCXRpYUwaw1JCIhlLBhKorRhsjMWNlKSt8kb096G6dj_zoVeSIQIApY2gklgdCeXHLtyFdL-y5F5bfbfjQchFSCU5zyIBWDSVCMVjSElGmAKCAQVEZWkuQtD4fsw3NRiupuz4INxGdnnR2zVu_45TUmJR1EvhwFAj-15Cs4xsbpXZOdNoPh3szkBxBCX33D_p4dUeqFakA2xmf8spRlM8JTR6jGo9pZ49QaYxfQaaPZWzanwR8nAQkptd_-lYMMfLl6vr_2aubKfv-hF1r4fp19G7ore_iFCwPoAw-xqDNg8kQ8LEv7t3gY1_wY1-ksDenD_QQdN8I-C9B9wgN</recordid><startdate>20211215</startdate><enddate>20211215</enddate><creator>Islam, Ariful</creator><creator>Ferdous, Jinnat</creator><creator>Sayeed, Md Abu</creator><creator>Islam, Shariful</creator><creator>Kaisar Rahman, Md</creator><creator>Abedin, Josefina</creator><creator>Saha, Otun</creator><creator>Hassan, Mohammad Mahmudul</creator><creator>Shirin, Tahmina</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>COVID</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-9210-3351</orcidid><orcidid>https://orcid.org/0000-0002-6626-4178</orcidid><orcidid>https://orcid.org/0000-0001-9159-0437</orcidid><orcidid>https://orcid.org/0000-0001-6495-4637</orcidid></search><sort><creationdate>20211215</creationdate><title>Spatial epidemiology and genetic diversity of SARS-CoV-2 and related coronaviruses in domestic and wild animals</title><author>Islam, Ariful ; Ferdous, Jinnat ; Sayeed, Md Abu ; Islam, Shariful ; Kaisar Rahman, Md ; Abedin, Josefina ; Saha, Otun ; Hassan, Mohammad Mahmudul ; Shirin, Tahmina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-f2656243b4f0fac9458dbcbfeb680e4f178903ce16ab88a9ad7598bfc39944c53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animal species</topic><topic>Animals</topic><topic>Animals, Domestic - virology</topic><topic>Animals, Wild - virology</topic><topic>Bats</topic><topic>Biology and life sciences</topic><topic>Clustering</topic><topic>Coronaviridae</topic><topic>Coronaviruses</topic><topic>COVID-19</topic><topic>COVID-19 - epidemiology</topic><topic>COVID-19 - transmission</topic><topic>COVID-19 - virology</topic><topic>Disease control</topic><topic>Disease transmission</topic><topic>Dogs</topic><topic>Domestic animals</topic><topic>Epidemics</topic><topic>Epidemiology</topic><topic>Evaluation</topic><topic>Evolution</topic><topic>Gene sequencing</topic><topic>Genes</topic><topic>Genetic diversity</topic><topic>Genetic Variation</topic><topic>Genome, Viral</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Humans</topic><topic>Infections</topic><topic>Mammals</topic><topic>Medicine and health sciences</topic><topic>Metadata</topic><topic>Mutation</topic><topic>N protein</topic><topic>Pandemics</topic><topic>Pangolins - virology</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Proteins</topic><topic>Recombination</topic><topic>Recombination, Genetic</topic><topic>Respiratory diseases</topic><topic>SARS-CoV-2 - classification</topic><topic>SARS-CoV-2 - genetics</topic><topic>SARS-CoV-2 - isolation &amp; 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Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Islam, Ariful</au><au>Ferdous, Jinnat</au><au>Sayeed, Md Abu</au><au>Islam, Shariful</au><au>Kaisar Rahman, Md</au><au>Abedin, Josefina</au><au>Saha, Otun</au><au>Hassan, Mohammad Mahmudul</au><au>Shirin, Tahmina</au><au>Makarenkov, Vladimir</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Spatial epidemiology and genetic diversity of SARS-CoV-2 and related coronaviruses in domestic and wild animals</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2021-12-15</date><risdate>2021</risdate><volume>16</volume><issue>12</issue><spage>e0260635</spage><pages>e0260635-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) showed susceptibility to diverse animal species. We conducted this study to understand the spatial epidemiology, genetic diversity, and statistically significant genetic similarity along with per-gene recombination events of SARS-CoV-2 and related viruses (SC2r-CoVs) in animals globally. We collected a number of different animal species infected with SARS-CoV-2 and its related viruses. Then, we retrieved genome sequences of SARS-CoV-2 and SC2r-CoVs from GISAID and NCBI GenBank for genomic and mutational analysis. Although the evolutionary origin of SARS-CoV-2 remains elusive, the diverse SC2r-CoV have been detected in multiple Rhinolophus bat species and in Malayan pangolin. To date, human-to-animal spillover events have been reported in cat, dog, tiger, lion, gorilla, leopard, ferret, puma, cougar, otter, and mink in 25 countries. Phylogeny and genetic recombination events of SC2r-CoVs showed higher similarity to the bat coronavirus RaTG13 and BANAL-103 for most of the genes and to some Malayan pangolin coronavirus (CoV) strains for the N protein from bats and pangolin showed close resemblance to SARS-CoV-2. The clustering of animal and human strains from the same geographical area has proved human-to-animal transmission of the virus. The Alpha, Delta and Mu-variant of SARS-CoV-2 was detected in dog, gorilla, lion, tiger, otter, and cat in the USA, India, Czech Republic, Belgium, and France with momentous genetic similarity with human SARS-CoV-2 sequences. The mink variant mutation (spike_Y453F) was detected in both humans and domestic cats. Moreover, the dog was affected mostly by clade O (66.7%), whereas cat and American mink were affected by clade GR (31.6 and 49.7%, respectively). The α-variant was detected as 2.6% in cat, 4.8% in dog, 14.3% in tiger, 66.7% in gorilla, and 77.3% in lion. The highest mutations observed in mink where the substitution of D614G in spike (95.2%) and P323L in NSP12 (95.2%) protein. In dog, cat, gorilla, lion, and tiger, Y505H and Y453F were the common mutations followed by Y145del, Y144del, and V70I in S protein. We recommend vaccine provision for pet and zoo animals to reduce the chance of transmission in animals. Besides, continuous epidemiological and genomic surveillance of coronaviruses in animal host is crucial to find out the immediate ancestor of SARS-CoV-2 and to prevent future CoVs threats to humans.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34910734</pmid><doi>10.1371/journal.pone.0260635</doi><tpages>e0260635</tpages><orcidid>https://orcid.org/0000-0002-9210-3351</orcidid><orcidid>https://orcid.org/0000-0002-6626-4178</orcidid><orcidid>https://orcid.org/0000-0001-9159-0437</orcidid><orcidid>https://orcid.org/0000-0001-6495-4637</orcidid><oa>free_for_read</oa></addata></record>
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issn 1932-6203
1932-6203
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source MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS) Journals Open Access; PubMed Central; Free Full-Text Journals in Chemistry
subjects Animal species
Animals
Animals, Domestic - virology
Animals, Wild - virology
Bats
Biology and life sciences
Clustering
Coronaviridae
Coronaviruses
COVID-19
COVID-19 - epidemiology
COVID-19 - transmission
COVID-19 - virology
Disease control
Disease transmission
Dogs
Domestic animals
Epidemics
Epidemiology
Evaluation
Evolution
Gene sequencing
Genes
Genetic diversity
Genetic Variation
Genome, Viral
Genomes
Genomics
Humans
Infections
Mammals
Medicine and health sciences
Metadata
Mutation
N protein
Pandemics
Pangolins - virology
Phylogenetics
Phylogeny
Proteins
Recombination
Recombination, Genetic
Respiratory diseases
SARS-CoV-2 - classification
SARS-CoV-2 - genetics
SARS-CoV-2 - isolation & purification
Severe acute respiratory syndrome
Severe acute respiratory syndrome coronavirus 2
Similarity
Species
Statistical analysis
Strains (organisms)
Vaccines
Veterinary medicine
Viral diseases
Viruses
Wild animals
Zoo animals
title Spatial epidemiology and genetic diversity of SARS-CoV-2 and related coronaviruses in domestic and wild animals
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