How to kill the honey bee larva: genomic potential and virulence mechanisms of Paenibacillus larvae
Paenibacillus larvae, a Gram positive bacterial pathogen, causes American Foulbrood (AFB), which is the most serious infectious disease of honey bees. In order to investigate the genomic potential of P. larvae, two strains belonging to two different genotypes were sequenced and used for comparative...
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description | Paenibacillus larvae, a Gram positive bacterial pathogen, causes American Foulbrood (AFB), which is the most serious infectious disease of honey bees. In order to investigate the genomic potential of P. larvae, two strains belonging to two different genotypes were sequenced and used for comparative genome analysis. The complete genome sequence of P. larvae strain DSM 25430 (genotype ERIC II) consisted of 4,056,006 bp and harbored 3,928 predicted protein-encoding genes. The draft genome sequence of P. larvae strain DSM 25719 (genotype ERIC I) comprised 4,579,589 bp and contained 4,868 protein-encoding genes. Both strains harbored a 9.7 kb plasmid and encoded a large number of virulence-associated proteins such as toxins and collagenases. In addition, genes encoding large multimodular enzymes producing nonribosomally peptides or polyketides were identified. In the genome of strain DSM 25719 seven toxin associated loci were identified and analyzed. Five of them encoded putatively functional toxins. The genome of strain DSM 25430 harbored several toxin loci that showed similarity to corresponding loci in the genome of strain DSM 25719, but were non-functional due to point mutations or disruption by transposases. Although both strains cause AFB, significant differences between the genomes were observed including genome size, number and composition of transposases, insertion elements, predicted phage regions, and strain-specific island-like regions. Transposases, integrases and recombinases are important drivers for genome plasticity. A total of 390 and 273 mobile elements were found in strain DSM 25430 and strain DSM 25719, respectively. Comparative genomics of both strains revealed acquisition of virulence factors by horizontal gene transfer and provided insights into evolution and pathogenicity. |
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In order to investigate the genomic potential of P. larvae, two strains belonging to two different genotypes were sequenced and used for comparative genome analysis. The complete genome sequence of P. larvae strain DSM 25430 (genotype ERIC II) consisted of 4,056,006 bp and harbored 3,928 predicted protein-encoding genes. The draft genome sequence of P. larvae strain DSM 25719 (genotype ERIC I) comprised 4,579,589 bp and contained 4,868 protein-encoding genes. Both strains harbored a 9.7 kb plasmid and encoded a large number of virulence-associated proteins such as toxins and collagenases. In addition, genes encoding large multimodular enzymes producing nonribosomally peptides or polyketides were identified. In the genome of strain DSM 25719 seven toxin associated loci were identified and analyzed. Five of them encoded putatively functional toxins. The genome of strain DSM 25430 harbored several toxin loci that showed similarity to corresponding loci in the genome of strain DSM 25719, but were non-functional due to point mutations or disruption by transposases. Although both strains cause AFB, significant differences between the genomes were observed including genome size, number and composition of transposases, insertion elements, predicted phage regions, and strain-specific island-like regions. Transposases, integrases and recombinases are important drivers for genome plasticity. A total of 390 and 273 mobile elements were found in strain DSM 25430 and strain DSM 25719, respectively. Comparative genomics of both strains revealed acquisition of virulence factors by horizontal gene transfer and provided insights into evolution and pathogenicity.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0090914</identifier><identifier>PMID: 24599066</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Air bases ; American foulbrood ; Animals ; Apis mellifera ; Bacteria ; Bacterial Proteins - metabolism ; Bacterial Toxins - genetics ; Base Composition - genetics ; Bees ; Bees - microbiology ; Biology ; Biosynthetic Pathways - genetics ; Chromosomes, Bacterial - genetics ; Clustered Regularly Interspaced Short Palindromic Repeats - genetics ; Collagen ; European honeybee ; Gene mutation ; Gene transfer ; Genes ; Genetic aspects ; Genetic Loci ; Genome, Bacterial - genetics ; Genomes ; Genomic Islands - genetics ; Genomics ; Genotypes ; Honey ; Infectious diseases ; Larva - microbiology ; Larvae ; Loci ; Models, Biological ; Multigene Family ; Mutation ; Nucleotide sequence ; Paenibacillus ; Paenibacillus - genetics ; Paenibacillus - pathogenicity ; Pathogenicity ; Pathogens ; Peptides ; Phages ; Polyketides ; Proteins ; Strains (organisms) ; Toxins ; Virulence ; Virulence (Microbiology) ; Virulence - genetics ; Virulence factors</subject><ispartof>PloS one, 2014-03, Vol.9 (3), p.e90914-e90914</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Djukic 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. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014 Djukic et al 2014 Djukic et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-77b60b0e97e4af3240acb2e9fd7acecd803122e3dbee86e60e27f600c07948273</citedby><cites>FETCH-LOGICAL-c692t-77b60b0e97e4af3240acb2e9fd7acecd803122e3dbee86e60e27f600c07948273</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3944939/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3944939/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24599066$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Bereswill, Stefan</contributor><creatorcontrib>Djukic, Marvin</creatorcontrib><creatorcontrib>Brzuszkiewicz, Elzbieta</creatorcontrib><creatorcontrib>Fünfhaus, Anne</creatorcontrib><creatorcontrib>Voss, Jörn</creatorcontrib><creatorcontrib>Gollnow, Kathleen</creatorcontrib><creatorcontrib>Poppinga, Lena</creatorcontrib><creatorcontrib>Liesegang, Heiko</creatorcontrib><creatorcontrib>Garcia-Gonzalez, Eva</creatorcontrib><creatorcontrib>Genersch, Elke</creatorcontrib><creatorcontrib>Daniel, Rolf</creatorcontrib><title>How to kill the honey bee larva: genomic potential and virulence mechanisms of Paenibacillus larvae</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Paenibacillus larvae, a Gram positive bacterial pathogen, causes American Foulbrood (AFB), which is the most serious infectious disease of honey bees. In order to investigate the genomic potential of P. larvae, two strains belonging to two different genotypes were sequenced and used for comparative genome analysis. The complete genome sequence of P. larvae strain DSM 25430 (genotype ERIC II) consisted of 4,056,006 bp and harbored 3,928 predicted protein-encoding genes. The draft genome sequence of P. larvae strain DSM 25719 (genotype ERIC I) comprised 4,579,589 bp and contained 4,868 protein-encoding genes. Both strains harbored a 9.7 kb plasmid and encoded a large number of virulence-associated proteins such as toxins and collagenases. In addition, genes encoding large multimodular enzymes producing nonribosomally peptides or polyketides were identified. In the genome of strain DSM 25719 seven toxin associated loci were identified and analyzed. Five of them encoded putatively functional toxins. The genome of strain DSM 25430 harbored several toxin loci that showed similarity to corresponding loci in the genome of strain DSM 25719, but were non-functional due to point mutations or disruption by transposases. Although both strains cause AFB, significant differences between the genomes were observed including genome size, number and composition of transposases, insertion elements, predicted phage regions, and strain-specific island-like regions. Transposases, integrases and recombinases are important drivers for genome plasticity. A total of 390 and 273 mobile elements were found in strain DSM 25430 and strain DSM 25719, respectively. Comparative genomics of both strains revealed acquisition of virulence factors by horizontal gene transfer and provided insights into evolution and pathogenicity.</description><subject>Air bases</subject><subject>American foulbrood</subject><subject>Animals</subject><subject>Apis mellifera</subject><subject>Bacteria</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacterial Toxins - genetics</subject><subject>Base Composition - genetics</subject><subject>Bees</subject><subject>Bees - microbiology</subject><subject>Biology</subject><subject>Biosynthetic Pathways - genetics</subject><subject>Chromosomes, Bacterial - genetics</subject><subject>Clustered Regularly Interspaced Short Palindromic Repeats - genetics</subject><subject>Collagen</subject><subject>European honeybee</subject><subject>Gene mutation</subject><subject>Gene transfer</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic Loci</subject><subject>Genome, Bacterial - genetics</subject><subject>Genomes</subject><subject>Genomic Islands - genetics</subject><subject>Genomics</subject><subject>Genotypes</subject><subject>Honey</subject><subject>Infectious diseases</subject><subject>Larva - microbiology</subject><subject>Larvae</subject><subject>Loci</subject><subject>Models, Biological</subject><subject>Multigene Family</subject><subject>Mutation</subject><subject>Nucleotide sequence</subject><subject>Paenibacillus</subject><subject>Paenibacillus - genetics</subject><subject>Paenibacillus - pathogenicity</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Peptides</subject><subject>Phages</subject><subject>Polyketides</subject><subject>Proteins</subject><subject>Strains (organisms)</subject><subject>Toxins</subject><subject>Virulence</subject><subject>Virulence (Microbiology)</subject><subject>Virulence - genetics</subject><subject>Virulence factors</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</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>eNqNk99v0zAQxyMEYmPwHyCwhITgocWxHbvmAWmagFWaNMSvV8txLo2LY3dxUth_j7tmU4P2gPxg6_y5753vfFn2PMfznIr83ToMndduvgke5hhLLHP2IDvOJSUzTjB9eHA-yp7EuMa4oAvOH2dHhBVSYs6PM3MefqM-oF_WOdQ3gJokd41KAOR0t9Xv0Qp8aK1Bm9CD7612SPsKbW03OPAGUAum0d7GNqJQoy8avC21SXJD3EvA0-xRrV2EZ-N-kv349PH72fns4vLz8uz0Yma4JP1MiJLjEoMUwHRNCcPalARkXQltwFQLTHNCgFYpuQUHjoGImmNssJBsQQQ9yV7udTcuRDXWJ6q8wKxglBCaiOWeqIJeq01nW91dq6CtujGEbqV011vjQBnMoS60kJxXjGNWAq6TrVzosmZVkSetD2O0oWyhMqk4nXYT0emNt41aha2ikjFJZRJ4Mwp04WqA2KvWRgPOaQ9huMm7IAXjdBfr1T_o_a8bqZVOD7C-Dimu2YmqUyYWQnDMcaLm91BpVZDanLpf22SfOLydOCSmhz_9Sg8xquW3r__PXv6csq8P2Aa065sY3NDb4OMUZHvQdCHGDuq7IudY7WbhthpqNwtqnIXk9uKwQXdOt5-f_gVB9wSc</recordid><startdate>20140305</startdate><enddate>20140305</enddate><creator>Djukic, Marvin</creator><creator>Brzuszkiewicz, Elzbieta</creator><creator>Fünfhaus, Anne</creator><creator>Voss, Jörn</creator><creator>Gollnow, Kathleen</creator><creator>Poppinga, Lena</creator><creator>Liesegang, Heiko</creator><creator>Garcia-Gonzalez, Eva</creator><creator>Genersch, Elke</creator><creator>Daniel, Rolf</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>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></search><sort><creationdate>20140305</creationdate><title>How to kill the honey bee larva: genomic potential and virulence mechanisms of Paenibacillus larvae</title><author>Djukic, Marvin ; Brzuszkiewicz, Elzbieta ; Fünfhaus, Anne ; Voss, Jörn ; Gollnow, Kathleen ; Poppinga, Lena ; Liesegang, Heiko ; Garcia-Gonzalez, Eva ; Genersch, Elke ; Daniel, Rolf</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-77b60b0e97e4af3240acb2e9fd7acecd803122e3dbee86e60e27f600c07948273</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Air bases</topic><topic>American foulbrood</topic><topic>Animals</topic><topic>Apis mellifera</topic><topic>Bacteria</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacterial Toxins - genetics</topic><topic>Base Composition - genetics</topic><topic>Bees</topic><topic>Bees - microbiology</topic><topic>Biology</topic><topic>Biosynthetic Pathways - genetics</topic><topic>Chromosomes, Bacterial - genetics</topic><topic>Clustered Regularly Interspaced Short Palindromic Repeats - genetics</topic><topic>Collagen</topic><topic>European honeybee</topic><topic>Gene mutation</topic><topic>Gene transfer</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genetic Loci</topic><topic>Genome, Bacterial - genetics</topic><topic>Genomes</topic><topic>Genomic Islands - genetics</topic><topic>Genomics</topic><topic>Genotypes</topic><topic>Honey</topic><topic>Infectious diseases</topic><topic>Larva - microbiology</topic><topic>Larvae</topic><topic>Loci</topic><topic>Models, Biological</topic><topic>Multigene Family</topic><topic>Mutation</topic><topic>Nucleotide sequence</topic><topic>Paenibacillus</topic><topic>Paenibacillus - genetics</topic><topic>Paenibacillus - 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In order to investigate the genomic potential of P. larvae, two strains belonging to two different genotypes were sequenced and used for comparative genome analysis. The complete genome sequence of P. larvae strain DSM 25430 (genotype ERIC II) consisted of 4,056,006 bp and harbored 3,928 predicted protein-encoding genes. The draft genome sequence of P. larvae strain DSM 25719 (genotype ERIC I) comprised 4,579,589 bp and contained 4,868 protein-encoding genes. Both strains harbored a 9.7 kb plasmid and encoded a large number of virulence-associated proteins such as toxins and collagenases. In addition, genes encoding large multimodular enzymes producing nonribosomally peptides or polyketides were identified. In the genome of strain DSM 25719 seven toxin associated loci were identified and analyzed. Five of them encoded putatively functional toxins. The genome of strain DSM 25430 harbored several toxin loci that showed similarity to corresponding loci in the genome of strain DSM 25719, but were non-functional due to point mutations or disruption by transposases. Although both strains cause AFB, significant differences between the genomes were observed including genome size, number and composition of transposases, insertion elements, predicted phage regions, and strain-specific island-like regions. Transposases, integrases and recombinases are important drivers for genome plasticity. A total of 390 and 273 mobile elements were found in strain DSM 25430 and strain DSM 25719, respectively. Comparative genomics of both strains revealed acquisition of virulence factors by horizontal gene transfer and provided insights into evolution and pathogenicity.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24599066</pmid><doi>10.1371/journal.pone.0090914</doi><tpages>e90914</tpages><oa>free_for_read</oa></addata></record> |
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recordid | cdi_plos_journals_1504543223 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
subjects | Air bases American foulbrood Animals Apis mellifera Bacteria Bacterial Proteins - metabolism Bacterial Toxins - genetics Base Composition - genetics Bees Bees - microbiology Biology Biosynthetic Pathways - genetics Chromosomes, Bacterial - genetics Clustered Regularly Interspaced Short Palindromic Repeats - genetics Collagen European honeybee Gene mutation Gene transfer Genes Genetic aspects Genetic Loci Genome, Bacterial - genetics Genomes Genomic Islands - genetics Genomics Genotypes Honey Infectious diseases Larva - microbiology Larvae Loci Models, Biological Multigene Family Mutation Nucleotide sequence Paenibacillus Paenibacillus - genetics Paenibacillus - pathogenicity Pathogenicity Pathogens Peptides Phages Polyketides Proteins Strains (organisms) Toxins Virulence Virulence (Microbiology) Virulence - genetics Virulence factors |
title | How to kill the honey bee larva: genomic potential and virulence mechanisms of Paenibacillus larvae |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-30T02%3A22%3A06IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=How%20to%20kill%20the%20honey%20bee%20larva:%20genomic%20potential%20and%20virulence%20mechanisms%20of%20Paenibacillus%20larvae&rft.jtitle=PloS%20one&rft.au=Djukic,%20Marvin&rft.date=2014-03-05&rft.volume=9&rft.issue=3&rft.spage=e90914&rft.epage=e90914&rft.pages=e90914-e90914&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0090914&rft_dat=%3Cgale_plos_%3EA478776060%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1504543223&rft_id=info:pmid/24599066&rft_galeid=A478776060&rft_doaj_id=oai_doaj_org_article_c06ef5a7966d4604be0fc06b8abf4d51&rfr_iscdi=true |