Metagenomic profiling of viral and microbial communities from the pox lesions of lumpy skin disease virus and sheeppox virus-infected hosts

IntroductionIt has been recognized that capripoxvirus infections have a strong cutaneous tropism with the manifestation of skin lesions in the form of nodules and scabs in the respective hosts, followed by necrosis and sloughing off. Considering that the skin microbiota is a complex community of com...

Full description

Bibliographic Details
Main Authors: Fedor S. Sharko, Ali Mazloum, Alena O. Krotova, Olga P. Byadovskaya, Larisa B. Prokhvatilova, Ilya A. Chvala, Ustin E. Zolotikov, Alexandra D. Kozlova, Anastasia S. Krylova, Erika V. Grosfeld, Anastasia V. Prokopenko, Aleksei A. Korzhenkov, Maxim V. Patrushev, Zorigto B. Namsaraev, Alexander V. Sprygin, Stepan V. Toshchakov
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-02-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2024.1321202/full
_version_ 1797311561297035264
author Fedor S. Sharko
Ali Mazloum
Alena O. Krotova
Olga P. Byadovskaya
Larisa B. Prokhvatilova
Ilya A. Chvala
Ustin E. Zolotikov
Alexandra D. Kozlova
Anastasia S. Krylova
Erika V. Grosfeld
Erika V. Grosfeld
Anastasia V. Prokopenko
Aleksei A. Korzhenkov
Maxim V. Patrushev
Zorigto B. Namsaraev
Alexander V. Sprygin
Stepan V. Toshchakov
author_facet Fedor S. Sharko
Ali Mazloum
Alena O. Krotova
Olga P. Byadovskaya
Larisa B. Prokhvatilova
Ilya A. Chvala
Ustin E. Zolotikov
Alexandra D. Kozlova
Anastasia S. Krylova
Erika V. Grosfeld
Erika V. Grosfeld
Anastasia V. Prokopenko
Aleksei A. Korzhenkov
Maxim V. Patrushev
Zorigto B. Namsaraev
Alexander V. Sprygin
Stepan V. Toshchakov
author_sort Fedor S. Sharko
collection DOAJ
description IntroductionIt has been recognized that capripoxvirus infections have a strong cutaneous tropism with the manifestation of skin lesions in the form of nodules and scabs in the respective hosts, followed by necrosis and sloughing off. Considering that the skin microbiota is a complex community of commensal bacteria, fungi and viruses that are influenced by infections leading to pathological states, there is no evidence on how the skin microbiome is affected during capripoxvirus pathogenesis.MethodsIn this study, shotgun metagenomic sequencing was used to investigate the microbiome in pox lesions from hosts infected with lumpy skin disease virus and sheep pox virus.ResultsThe analysis revealed a high degree of variability in bacterial community structures across affected skin samples, indicating the importance of specific commensal microorganisms colonizing individual hosts. The most common and abundant bacteria found in scab samples were Fusobacterium necrophorum, Streptococcus dysgalactiae, Helcococcus ovis and Trueperella pyogenes, irrespective of host. Bacterial reads belonging to the genera Moraxella, Mannheimia, Corynebacterium, Staphylococcus and Micrococcus were identified.DiscussionThis study is the first to investigate capripox virus-associated changes in the skin microbiome using whole-genome metagenomic profiling. The findings will provide a basis for further investigation into capripoxvirus pathogenesis. In addition, this study highlights the challenge of selecting an optimal bioinformatics approach for the analysis of metagenomic data in clinical and veterinary practice. For example, direct classification of reads using a kmer-based algorithm resulted in a significant number of systematic false positives, which may be attributed to the peculiarities of the algorithm and database selection. On the contrary, the process of de novo assembly requires a large number of target reads from the symbiotic microbial community. In this work, the obtained sequencing data were processed by three different approaches, including direct classification of reads based on k-mers, mapping of reads to a marker gene database, and de novo assembly and binning of metagenomic contigs. The advantages and disadvantages of these techniques and their practicality in veterinary settings are discussed in relation to the results obtained.
first_indexed 2024-03-08T02:02:28Z
format Article
id doaj.art-1f891829bde0427e862f59abd567af92
institution Directory Open Access Journal
issn 2297-1769
language English
last_indexed 2024-03-08T02:02:28Z
publishDate 2024-02-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Veterinary Science
spelling doaj.art-1f891829bde0427e862f59abd567af922024-02-14T05:01:38ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692024-02-011110.3389/fvets.2024.13212021321202Metagenomic profiling of viral and microbial communities from the pox lesions of lumpy skin disease virus and sheeppox virus-infected hostsFedor S. Sharko0Ali Mazloum1Alena O. Krotova2Olga P. Byadovskaya3Larisa B. Prokhvatilova4Ilya A. Chvala5Ustin E. Zolotikov6Alexandra D. Kozlova7Anastasia S. Krylova8Erika V. Grosfeld9Erika V. Grosfeld10Anastasia V. Prokopenko11Aleksei A. Korzhenkov12Maxim V. Patrushev13Zorigto B. Namsaraev14Alexander V. Sprygin15Stepan V. Toshchakov16National Research Center “Kurchatov Institute”, Moscow, RussiaFederal Center for Animal Health FGBI ARRIAH, Vladimir, RussiaFederal Center for Animal Health FGBI ARRIAH, Vladimir, RussiaFederal Center for Animal Health FGBI ARRIAH, Vladimir, RussiaFederal Center for Animal Health FGBI ARRIAH, Vladimir, RussiaFederal Center for Animal Health FGBI ARRIAH, Vladimir, RussiaNational Research Center “Kurchatov Institute”, Moscow, RussiaNational Research Center “Kurchatov Institute”, Moscow, RussiaNational Research Center “Kurchatov Institute”, Moscow, RussiaNational Research Center “Kurchatov Institute”, Moscow, RussiaMoscow Institute of Physics and Technology, National Research University, Dolgoprudny, RussiaNational Research Center “Kurchatov Institute”, Moscow, RussiaNational Research Center “Kurchatov Institute”, Moscow, RussiaNational Research Center “Kurchatov Institute”, Moscow, RussiaNational Research Center “Kurchatov Institute”, Moscow, RussiaFederal Center for Animal Health FGBI ARRIAH, Vladimir, RussiaNational Research Center “Kurchatov Institute”, Moscow, RussiaIntroductionIt has been recognized that capripoxvirus infections have a strong cutaneous tropism with the manifestation of skin lesions in the form of nodules and scabs in the respective hosts, followed by necrosis and sloughing off. Considering that the skin microbiota is a complex community of commensal bacteria, fungi and viruses that are influenced by infections leading to pathological states, there is no evidence on how the skin microbiome is affected during capripoxvirus pathogenesis.MethodsIn this study, shotgun metagenomic sequencing was used to investigate the microbiome in pox lesions from hosts infected with lumpy skin disease virus and sheep pox virus.ResultsThe analysis revealed a high degree of variability in bacterial community structures across affected skin samples, indicating the importance of specific commensal microorganisms colonizing individual hosts. The most common and abundant bacteria found in scab samples were Fusobacterium necrophorum, Streptococcus dysgalactiae, Helcococcus ovis and Trueperella pyogenes, irrespective of host. Bacterial reads belonging to the genera Moraxella, Mannheimia, Corynebacterium, Staphylococcus and Micrococcus were identified.DiscussionThis study is the first to investigate capripox virus-associated changes in the skin microbiome using whole-genome metagenomic profiling. The findings will provide a basis for further investigation into capripoxvirus pathogenesis. In addition, this study highlights the challenge of selecting an optimal bioinformatics approach for the analysis of metagenomic data in clinical and veterinary practice. For example, direct classification of reads using a kmer-based algorithm resulted in a significant number of systematic false positives, which may be attributed to the peculiarities of the algorithm and database selection. On the contrary, the process of de novo assembly requires a large number of target reads from the symbiotic microbial community. In this work, the obtained sequencing data were processed by three different approaches, including direct classification of reads based on k-mers, mapping of reads to a marker gene database, and de novo assembly and binning of metagenomic contigs. The advantages and disadvantages of these techniques and their practicality in veterinary settings are discussed in relation to the results obtained.https://www.frontiersin.org/articles/10.3389/fvets.2024.1321202/fulllumpy skin disease virussheep pox virusmetagenomebacterial communityshotgun sequencingskin microbiome
spellingShingle Fedor S. Sharko
Ali Mazloum
Alena O. Krotova
Olga P. Byadovskaya
Larisa B. Prokhvatilova
Ilya A. Chvala
Ustin E. Zolotikov
Alexandra D. Kozlova
Anastasia S. Krylova
Erika V. Grosfeld
Erika V. Grosfeld
Anastasia V. Prokopenko
Aleksei A. Korzhenkov
Maxim V. Patrushev
Zorigto B. Namsaraev
Alexander V. Sprygin
Stepan V. Toshchakov
Metagenomic profiling of viral and microbial communities from the pox lesions of lumpy skin disease virus and sheeppox virus-infected hosts
Frontiers in Veterinary Science
lumpy skin disease virus
sheep pox virus
metagenome
bacterial community
shotgun sequencing
skin microbiome
title Metagenomic profiling of viral and microbial communities from the pox lesions of lumpy skin disease virus and sheeppox virus-infected hosts
title_full Metagenomic profiling of viral and microbial communities from the pox lesions of lumpy skin disease virus and sheeppox virus-infected hosts
title_fullStr Metagenomic profiling of viral and microbial communities from the pox lesions of lumpy skin disease virus and sheeppox virus-infected hosts
title_full_unstemmed Metagenomic profiling of viral and microbial communities from the pox lesions of lumpy skin disease virus and sheeppox virus-infected hosts
title_short Metagenomic profiling of viral and microbial communities from the pox lesions of lumpy skin disease virus and sheeppox virus-infected hosts
title_sort metagenomic profiling of viral and microbial communities from the pox lesions of lumpy skin disease virus and sheeppox virus infected hosts
topic lumpy skin disease virus
sheep pox virus
metagenome
bacterial community
shotgun sequencing
skin microbiome
url https://www.frontiersin.org/articles/10.3389/fvets.2024.1321202/full
work_keys_str_mv AT fedorssharko metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT alimazloum metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT alenaokrotova metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT olgapbyadovskaya metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT larisabprokhvatilova metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT ilyaachvala metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT ustinezolotikov metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT alexandradkozlova metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT anastasiaskrylova metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT erikavgrosfeld metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT erikavgrosfeld metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT anastasiavprokopenko metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT alekseiakorzhenkov metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT maximvpatrushev metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT zorigtobnamsaraev metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT alexandervsprygin metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts
AT stepanvtoshchakov metagenomicprofilingofviralandmicrobialcommunitiesfromthepoxlesionsoflumpyskindiseasevirusandsheeppoxvirusinfectedhosts