Genome-wide identification of Hfq-regulated small RNAs in the fire blight pathogen Erwinia amylovora discovered small RNAs with virulence regulatory function
Erwinia amylovora is a phytopathogenic bacterium and causal agent of fire blight disease in apples and pears. Although many virulence factors have been characterized, the coordination of expression of these virulence factors in E. amylovora is still not clear. Regulatory small RNAs (sRNAs) are impor...
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description | Erwinia amylovora is a phytopathogenic bacterium and causal agent of fire blight disease in apples and pears. Although many virulence factors have been characterized, the coordination of expression of these virulence factors in E. amylovora is still not clear. Regulatory small RNAs (sRNAs) are important post-transcriptional regulatory components in bacteria. A large number of sRNAs require the RNA chaperone Hfq for both stability and functional activation. In E. amylovora, Hfq was identified as a major regulator of virulence and various virulence traits. However, information is still lacking about Hfq-dependent sRNAs on a genome scale, including the virulence regulatory functions of these sRNAs in E. amylovora.
Using both an RNA-seq analysis and a Rho-independent terminator search, 40 candidate Hfq-dependent sRNAs were identified in E. amylovora. The expression and sizes of 12 sRNAs and the sequence boundaries of seven sRNAs were confirmed by Northern blot and 5' RACE assay respectively. Sequence conservation analysis identified sRNAs conserved only in the Erwinia genus as well as E. amylovora species-specific sRNAs. In addition, a dynamic re-patterning of expression of Hfq-dependent sRNAs was observed at 6 and 12 hours after induction in Hrp-inducing minimal medium. Furthermore, sRNAs that control virulence traits were characterized, among which ArcZ positively controls the type III secretion system (T3SS), amylovoran exopolysaccahride production, biofilm formation, and motility, and negatively modulates attachment while RmaA (Hrs6) and OmrAB both negatively regulate amylovoran production and positively regulate motility.
This study has significantly enhanced our understanding of the Hfq-dependent sRNAs in E. amylovora at the genome level. The identification of multiple virulence-regulating sRNAs also suggests that post-transcriptional regulation by sRNAs may play a role in the deployment of virulence factors needed during varying stages of pathogenesis during host invasion by E. amylovora. |
doi_str_mv | 10.1186/1471-2164-15-414 |
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Using both an RNA-seq analysis and a Rho-independent terminator search, 40 candidate Hfq-dependent sRNAs were identified in E. amylovora. The expression and sizes of 12 sRNAs and the sequence boundaries of seven sRNAs were confirmed by Northern blot and 5' RACE assay respectively. Sequence conservation analysis identified sRNAs conserved only in the Erwinia genus as well as E. amylovora species-specific sRNAs. In addition, a dynamic re-patterning of expression of Hfq-dependent sRNAs was observed at 6 and 12 hours after induction in Hrp-inducing minimal medium. Furthermore, sRNAs that control virulence traits were characterized, among which ArcZ positively controls the type III secretion system (T3SS), amylovoran exopolysaccahride production, biofilm formation, and motility, and negatively modulates attachment while RmaA (Hrs6) and OmrAB both negatively regulate amylovoran production and positively regulate motility.
This study has significantly enhanced our understanding of the Hfq-dependent sRNAs in E. amylovora at the genome level. The identification of multiple virulence-regulating sRNAs also suggests that post-transcriptional regulation by sRNAs may play a role in the deployment of virulence factors needed during varying stages of pathogenesis during host invasion by E. amylovora.</description><identifier>ISSN: 1471-2164</identifier><identifier>EISSN: 1471-2164</identifier><identifier>DOI: 10.1186/1471-2164-15-414</identifier><identifier>PMID: 24885615</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Analysis ; Bacteria ; Bacterial Proteins - metabolism ; Bacteriology ; Biofilms ; Bioinformatics ; Colleges & universities ; Disease ; E coli ; Erwinia ; Erwinia amylovora ; Erwinia amylovora - genetics ; Erwinia amylovora - physiology ; Gene Expression Regulation, Bacterial ; Genes ; Genetic aspects ; Genetic transcription ; Genomes ; Host Factor 1 Protein - metabolism ; Motility ; Pathogenesis ; Phylogeny ; Plant Diseases - microbiology ; Proteins ; Pyrus - microbiology ; RNA, Bacterial - genetics ; RNA, Bacterial - metabolism ; RNA, Small Untranslated - genetics ; RNA, Small Untranslated - metabolism ; Salmonella ; Signal transduction ; Virulence Factors - genetics ; Virulence Factors - metabolism</subject><ispartof>BMC genomics, 2014-05, Vol.15 (1), p.414-414</ispartof><rights>COPYRIGHT 2014 BioMed Central Ltd.</rights><rights>2014 Zeng and Sundin; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.</rights><rights>Zeng and Sundin; licensee BioMed Central Ltd. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b688t-3beba6f49ea78b6280fc39ea0bf6cb52f18a719b897a5236330a5ce9e3f4c4e23</citedby><cites>FETCH-LOGICAL-b688t-3beba6f49ea78b6280fc39ea0bf6cb52f18a719b897a5236330a5ce9e3f4c4e23</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/PMC4070566/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4070566/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24885615$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zeng, Quan</creatorcontrib><creatorcontrib>Sundin, George W</creatorcontrib><title>Genome-wide identification of Hfq-regulated small RNAs in the fire blight pathogen Erwinia amylovora discovered small RNAs with virulence regulatory function</title><title>BMC genomics</title><addtitle>BMC Genomics</addtitle><description>Erwinia amylovora is a phytopathogenic bacterium and causal agent of fire blight disease in apples and pears. Although many virulence factors have been characterized, the coordination of expression of these virulence factors in E. amylovora is still not clear. Regulatory small RNAs (sRNAs) are important post-transcriptional regulatory components in bacteria. A large number of sRNAs require the RNA chaperone Hfq for both stability and functional activation. In E. amylovora, Hfq was identified as a major regulator of virulence and various virulence traits. However, information is still lacking about Hfq-dependent sRNAs on a genome scale, including the virulence regulatory functions of these sRNAs in E. amylovora.
Using both an RNA-seq analysis and a Rho-independent terminator search, 40 candidate Hfq-dependent sRNAs were identified in E. amylovora. The expression and sizes of 12 sRNAs and the sequence boundaries of seven sRNAs were confirmed by Northern blot and 5' RACE assay respectively. Sequence conservation analysis identified sRNAs conserved only in the Erwinia genus as well as E. amylovora species-specific sRNAs. In addition, a dynamic re-patterning of expression of Hfq-dependent sRNAs was observed at 6 and 12 hours after induction in Hrp-inducing minimal medium. Furthermore, sRNAs that control virulence traits were characterized, among which ArcZ positively controls the type III secretion system (T3SS), amylovoran exopolysaccahride production, biofilm formation, and motility, and negatively modulates attachment while RmaA (Hrs6) and OmrAB both negatively regulate amylovoran production and positively regulate motility.
This study has significantly enhanced our understanding of the Hfq-dependent sRNAs in E. amylovora at the genome level. The identification of multiple virulence-regulating sRNAs also suggests that post-transcriptional regulation by sRNAs may play a role in the deployment of virulence factors needed during varying stages of pathogenesis during host invasion by E. amylovora.</description><subject>Analysis</subject><subject>Bacteria</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Biofilms</subject><subject>Bioinformatics</subject><subject>Colleges & universities</subject><subject>Disease</subject><subject>E coli</subject><subject>Erwinia</subject><subject>Erwinia amylovora</subject><subject>Erwinia amylovora - genetics</subject><subject>Erwinia amylovora - physiology</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic transcription</subject><subject>Genomes</subject><subject>Host Factor 1 Protein - metabolism</subject><subject>Motility</subject><subject>Pathogenesis</subject><subject>Phylogeny</subject><subject>Plant Diseases - microbiology</subject><subject>Proteins</subject><subject>Pyrus - microbiology</subject><subject>RNA, Bacterial - genetics</subject><subject>RNA, Bacterial - metabolism</subject><subject>RNA, Small Untranslated - genetics</subject><subject>RNA, Small Untranslated - metabolism</subject><subject>Salmonella</subject><subject>Signal transduction</subject><subject>Virulence Factors - genetics</subject><subject>Virulence Factors - metabolism</subject><issn>1471-2164</issn><issn>1471-2164</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><recordid>eNqNkkFv0zAUxyMEYmNw54QscYFDhp3YjntBqqqxTZpAGnC2HPc59ZTYnZ209MPwXXHUUhY0JGRZtp9_7--n_3OWvSb4nBDBPxBakbwgnOaE5ZTQJ9npMfT0wf4kexHjHcakEgV7np0UVAjGCTvNfl6C8x3kW7sElKbrrbFa9dY75A26Mvd5gGZoVQ9LFDvVtuj28zwi61C_AmRsAFS3tln1aK36lW_AoYuwtc4qpLpd6zc-KLS0UfsNhKnG1vYrtLFhaMFpQId3fNghMzg9lvAye2ZUG-HVYT3Lvn-6-La4ym--XF4v5jd5zYXo87KGWnFDZ6AqUfNCYKPLdMC14bpmhSFCVWRWi1mlWFHyssSKaZhBaaimUJRn2ce97nqoO1jqZENQrVwH26mwk15ZOb1xdiUbv5EUV5hxngQWe4Ha-n8ITG-07-TYHjm2RxImU_eSyrtDGcHfDxB72SXjoG2VAz_EhFGKCcOz_0HLGeUVZSP69i_0zg_BJT9HSghe4qr8QzWqBWmd8alOPYrKedJiFSkKlqjzR6g0ltBZ7R0Ym-KThPeThMT08KNv1BCjvP56O2XxntXBxxjAHP0jWI7__THH3jxs3DHh9wcvfwFks_x7</recordid><startdate>20140531</startdate><enddate>20140531</enddate><creator>Zeng, Quan</creator><creator>Sundin, George W</creator><general>BioMed Central Ltd</general><general>BioMed Central</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>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>7QL</scope><scope>7TM</scope><scope>5PM</scope></search><sort><creationdate>20140531</creationdate><title>Genome-wide identification of Hfq-regulated small RNAs in the fire blight pathogen Erwinia amylovora discovered small RNAs with virulence regulatory function</title><author>Zeng, Quan ; Sundin, George W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b688t-3beba6f49ea78b6280fc39ea0bf6cb52f18a719b897a5236330a5ce9e3f4c4e23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Analysis</topic><topic>Bacteria</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacteriology</topic><topic>Biofilms</topic><topic>Bioinformatics</topic><topic>Colleges & universities</topic><topic>Disease</topic><topic>E coli</topic><topic>Erwinia</topic><topic>Erwinia amylovora</topic><topic>Erwinia amylovora - genetics</topic><topic>Erwinia amylovora - physiology</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genetic transcription</topic><topic>Genomes</topic><topic>Host Factor 1 Protein - metabolism</topic><topic>Motility</topic><topic>Pathogenesis</topic><topic>Phylogeny</topic><topic>Plant Diseases - microbiology</topic><topic>Proteins</topic><topic>Pyrus - microbiology</topic><topic>RNA, Bacterial - genetics</topic><topic>RNA, Bacterial - metabolism</topic><topic>RNA, Small Untranslated - genetics</topic><topic>RNA, Small Untranslated - metabolism</topic><topic>Salmonella</topic><topic>Signal transduction</topic><topic>Virulence Factors - genetics</topic><topic>Virulence Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zeng, Quan</creatorcontrib><creatorcontrib>Sundin, George W</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</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>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Nucleic Acids Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>BMC genomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zeng, Quan</au><au>Sundin, George W</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome-wide identification of Hfq-regulated small RNAs in the fire blight pathogen Erwinia amylovora discovered small RNAs with virulence regulatory function</atitle><jtitle>BMC genomics</jtitle><addtitle>BMC Genomics</addtitle><date>2014-05-31</date><risdate>2014</risdate><volume>15</volume><issue>1</issue><spage>414</spage><epage>414</epage><pages>414-414</pages><issn>1471-2164</issn><eissn>1471-2164</eissn><abstract>Erwinia amylovora is a phytopathogenic bacterium and causal agent of fire blight disease in apples and pears. Although many virulence factors have been characterized, the coordination of expression of these virulence factors in E. amylovora is still not clear. Regulatory small RNAs (sRNAs) are important post-transcriptional regulatory components in bacteria. A large number of sRNAs require the RNA chaperone Hfq for both stability and functional activation. In E. amylovora, Hfq was identified as a major regulator of virulence and various virulence traits. However, information is still lacking about Hfq-dependent sRNAs on a genome scale, including the virulence regulatory functions of these sRNAs in E. amylovora.
Using both an RNA-seq analysis and a Rho-independent terminator search, 40 candidate Hfq-dependent sRNAs were identified in E. amylovora. The expression and sizes of 12 sRNAs and the sequence boundaries of seven sRNAs were confirmed by Northern blot and 5' RACE assay respectively. Sequence conservation analysis identified sRNAs conserved only in the Erwinia genus as well as E. amylovora species-specific sRNAs. In addition, a dynamic re-patterning of expression of Hfq-dependent sRNAs was observed at 6 and 12 hours after induction in Hrp-inducing minimal medium. Furthermore, sRNAs that control virulence traits were characterized, among which ArcZ positively controls the type III secretion system (T3SS), amylovoran exopolysaccahride production, biofilm formation, and motility, and negatively modulates attachment while RmaA (Hrs6) and OmrAB both negatively regulate amylovoran production and positively regulate motility.
This study has significantly enhanced our understanding of the Hfq-dependent sRNAs in E. amylovora at the genome level. The identification of multiple virulence-regulating sRNAs also suggests that post-transcriptional regulation by sRNAs may play a role in the deployment of virulence factors needed during varying stages of pathogenesis during host invasion by E. amylovora.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>24885615</pmid><doi>10.1186/1471-2164-15-414</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Bacteria Bacterial Proteins - metabolism Bacteriology Biofilms Bioinformatics Colleges & universities Disease E coli Erwinia Erwinia amylovora Erwinia amylovora - genetics Erwinia amylovora - physiology Gene Expression Regulation, Bacterial Genes Genetic aspects Genetic transcription Genomes Host Factor 1 Protein - metabolism Motility Pathogenesis Phylogeny Plant Diseases - microbiology Proteins Pyrus - microbiology RNA, Bacterial - genetics RNA, Bacterial - metabolism RNA, Small Untranslated - genetics RNA, Small Untranslated - metabolism Salmonella Signal transduction Virulence Factors - genetics Virulence Factors - metabolism |
title | Genome-wide identification of Hfq-regulated small RNAs in the fire blight pathogen Erwinia amylovora discovered small RNAs with virulence regulatory function |
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