Sil: a Streptococcus iniae bacteriocin with dual role as an antimicrobial and an immunomodulator that inhibits innate immune response and promotes S. iniae infection
Streptococcus iniae is a Gram-positive bacterium and a severe pathogen to a wide range of economically important fish species. In addition, S. iniae is also a zoonotic pathogen and can cause serious infections in humans. In this study, we identified from a pathogenic S. iniae strain a putative bacte...
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| description | Streptococcus iniae is a Gram-positive bacterium and a severe pathogen to a wide range of economically important fish species. In addition, S. iniae is also a zoonotic pathogen and can cause serious infections in humans. In this study, we identified from a pathogenic S. iniae strain a putative bacteriocin, Sil, and examined its biological activity. Sil is composed of 101 amino acid residues and shares 35.6% overall sequence identity with the lactococcin 972 of Lactococcus lactis. Immunoblot analysis showed that Sil was secreted by S. iniae into the extracellular milieu. Purified recombinant Sil (rSil) exhibited a dose-dependent inhibitory effect on the growth of Bacillus subtilis but had no impact on the growths of other 16 Gram-positive bacteria and 10 Gram-negative bacteria representing 23 different bacterial species. Treatment of rSil by heating at 50°C abolished the activity of rSil. rSil bound to the surface of B. subtilis but induced no killing of the target cells. Cellular study revealed that rSil interacted with turbot (Scophthalmus maximus) head kidney monocytes and inhibited the innate immune response of the cells, which led to enhanced cellular infection of S. iniae. Antibody blocking of the extracellular Sil produced by S. iniae significantly attenuated the infectivity of S. iniae. Consistent with these in vitro observations, in vivo study showed that administration of turbot with rSil prior to S. iniae infection significantly increased bacterial dissemination and colonization in fish tissues. Taken together, these results indicate that Sil is a novel virulence-associated bacteriostatic and an immunoregulator that promotes S. iniae infection by impairing the immune defense of host fish. |
| doi_str_mv | 10.1371/journal.pone.0096222 |
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In addition, S. iniae is also a zoonotic pathogen and can cause serious infections in humans. In this study, we identified from a pathogenic S. iniae strain a putative bacteriocin, Sil, and examined its biological activity. Sil is composed of 101 amino acid residues and shares 35.6% overall sequence identity with the lactococcin 972 of Lactococcus lactis. Immunoblot analysis showed that Sil was secreted by S. iniae into the extracellular milieu. Purified recombinant Sil (rSil) exhibited a dose-dependent inhibitory effect on the growth of Bacillus subtilis but had no impact on the growths of other 16 Gram-positive bacteria and 10 Gram-negative bacteria representing 23 different bacterial species. Treatment of rSil by heating at 50°C abolished the activity of rSil. rSil bound to the surface of B. subtilis but induced no killing of the target cells. Cellular study revealed that rSil interacted with turbot (Scophthalmus maximus) head kidney monocytes and inhibited the innate immune response of the cells, which led to enhanced cellular infection of S. iniae. Antibody blocking of the extracellular Sil produced by S. iniae significantly attenuated the infectivity of S. iniae. Consistent with these in vitro observations, in vivo study showed that administration of turbot with rSil prior to S. iniae infection significantly increased bacterial dissemination and colonization in fish tissues. Taken together, these results indicate that Sil is a novel virulence-associated bacteriostatic and an immunoregulator that promotes S. iniae infection by impairing the immune defense of host fish.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0096222</identifier><identifier>PMID: 24781647</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino acid sequence ; Amino acids ; Analysis ; Animal tissues ; Animals ; Antibacterial agents ; Antimicrobial agents ; Bacillus licheniformis ; Bacillus subtilis ; Bacteria ; Bacteriocins - chemistry ; Bacteriocins - immunology ; Biological activity ; Biology and Life Sciences ; Biosynthesis ; Cells, Cultured ; Colonization ; Diseases ; Distribution ; E coli ; Escherichia coli ; Fish ; Fish Diseases - immunology ; Fish Diseases - microbiology ; Fishes ; Flatfishes - immunology ; Flatfishes - microbiology ; Genomes ; Gram-negative bacteria ; Gram-positive bacteria ; Health aspects ; Immune response ; Immune system ; Immunity, Innate ; In vivo methods and tests ; Infections ; Infectivity ; Innate immunity ; Kidneys ; Killing ; Laboratories ; Lactobacillus acidophilus ; Lactobacillus rhamnosus ; Lactococcus lactis ; Listeria ; Listeria monocytogenes ; Marine biology ; Medicine and Health Sciences ; Microbiology ; Monocytes ; Monocytes - immunology ; Monocytes - microbiology ; Pathogens ; Peptides ; Probiotics ; Proteins ; Scophthalmus maximus ; Streptococcal Infections - immunology ; Streptococcal Infections - microbiology ; Streptococcal Infections - veterinary ; Streptococcus ; Streptococcus - chemistry ; Streptococcus - immunology ; Streptococcus - pathogenicity ; Streptococcus iniae ; Streptococcus salivarius ; Streptococcus thermophilus ; Virulence ; Virulence Factors - chemistry ; Virulence Factors - immunology</subject><ispartof>PloS one, 2014-04, Vol.9 (4), p.e96222-e96222</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Li 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 Li et al 2014 Li et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-a4200e57fff4766b71f89865ca52c048106c04e965ba477f94a4fd56ffaf5f633</citedby><cites>FETCH-LOGICAL-c692t-a4200e57fff4766b71f89865ca52c048106c04e965ba477f94a4fd56ffaf5f633</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/PMC4004548/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4004548/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24781647$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Li, Mo-fei</creatorcontrib><creatorcontrib>Zhang, Bao-cun</creatorcontrib><creatorcontrib>Li, Jun</creatorcontrib><creatorcontrib>Sun, Li</creatorcontrib><title>Sil: a Streptococcus iniae bacteriocin with dual role as an antimicrobial and an immunomodulator that inhibits innate immune response and promotes S. iniae infection</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Streptococcus iniae is a Gram-positive bacterium and a severe pathogen to a wide range of economically important fish species. In addition, S. iniae is also a zoonotic pathogen and can cause serious infections in humans. In this study, we identified from a pathogenic S. iniae strain a putative bacteriocin, Sil, and examined its biological activity. Sil is composed of 101 amino acid residues and shares 35.6% overall sequence identity with the lactococcin 972 of Lactococcus lactis. Immunoblot analysis showed that Sil was secreted by S. iniae into the extracellular milieu. Purified recombinant Sil (rSil) exhibited a dose-dependent inhibitory effect on the growth of Bacillus subtilis but had no impact on the growths of other 16 Gram-positive bacteria and 10 Gram-negative bacteria representing 23 different bacterial species. Treatment of rSil by heating at 50°C abolished the activity of rSil. rSil bound to the surface of B. subtilis but induced no killing of the target cells. Cellular study revealed that rSil interacted with turbot (Scophthalmus maximus) head kidney monocytes and inhibited the innate immune response of the cells, which led to enhanced cellular infection of S. iniae. Antibody blocking of the extracellular Sil produced by S. iniae significantly attenuated the infectivity of S. iniae. Consistent with these in vitro observations, in vivo study showed that administration of turbot with rSil prior to S. iniae infection significantly increased bacterial dissemination and colonization in fish tissues. Taken together, these results indicate that Sil is a novel virulence-associated bacteriostatic and an immunoregulator that promotes S. iniae infection by impairing the immune defense of host fish.</description><subject>Amino acid sequence</subject><subject>Amino acids</subject><subject>Analysis</subject><subject>Animal tissues</subject><subject>Animals</subject><subject>Antibacterial agents</subject><subject>Antimicrobial agents</subject><subject>Bacillus licheniformis</subject><subject>Bacillus subtilis</subject><subject>Bacteria</subject><subject>Bacteriocins - chemistry</subject><subject>Bacteriocins - immunology</subject><subject>Biological activity</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Cells, Cultured</subject><subject>Colonization</subject><subject>Diseases</subject><subject>Distribution</subject><subject>E coli</subject><subject>Escherichia coli</subject><subject>Fish</subject><subject>Fish Diseases - immunology</subject><subject>Fish Diseases - microbiology</subject><subject>Fishes</subject><subject>Flatfishes - immunology</subject><subject>Flatfishes - microbiology</subject><subject>Genomes</subject><subject>Gram-negative bacteria</subject><subject>Gram-positive bacteria</subject><subject>Health aspects</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunity, Innate</subject><subject>In vivo methods and tests</subject><subject>Infections</subject><subject>Infectivity</subject><subject>Innate immunity</subject><subject>Kidneys</subject><subject>Killing</subject><subject>Laboratories</subject><subject>Lactobacillus acidophilus</subject><subject>Lactobacillus rhamnosus</subject><subject>Lactococcus lactis</subject><subject>Listeria</subject><subject>Listeria monocytogenes</subject><subject>Marine biology</subject><subject>Medicine and Health Sciences</subject><subject>Microbiology</subject><subject>Monocytes</subject><subject>Monocytes - immunology</subject><subject>Monocytes - microbiology</subject><subject>Pathogens</subject><subject>Peptides</subject><subject>Probiotics</subject><subject>Proteins</subject><subject>Scophthalmus maximus</subject><subject>Streptococcal Infections - immunology</subject><subject>Streptococcal Infections - microbiology</subject><subject>Streptococcal Infections - veterinary</subject><subject>Streptococcus</subject><subject>Streptococcus - chemistry</subject><subject>Streptococcus - immunology</subject><subject>Streptococcus - pathogenicity</subject><subject>Streptococcus iniae</subject><subject>Streptococcus salivarius</subject><subject>Streptococcus thermophilus</subject><subject>Virulence</subject><subject>Virulence Factors - chemistry</subject><subject>Virulence Factors - immunology</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>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk22L1DAQx4so3nn6DUQLguiLXZM2SVtfCMfhw8LBgau-DbNpss2SJmuS-vCB_J6mt71jK_dCWkiY_OY_k8lMlj3FaInLCr_ZucFbMMu9s3KJUMOKoriXneKmLBasQOX9o_1J9iiEHUK0rBl7mJ0UpKoxI9Vp9metzdsc8nX0ch-dcEIMIddWg8w3IKL02glt8586dnk7gMm9MzKHkINNf9S9Ft5tdDoA245G3feDdb1rBwPR-Tx2EJNgpzc6jsoWojxAMvcypPSDvPbd--QVZcjXyykBbZUUUTv7OHugwAT5ZFrPsq8f3n-5-LS4vPq4uji_XAjWFHEBpEBI0kopRSrGNhVWdVMzKoAWApEaI5YW2TC6AVJVqiFAVEuZUqCoYmV5lj0_6O6NC3yqcOCY4qZumrpuErE6EK2DHd973YP_zR1ofm1wfsvBRy2M5EWbotBGAW1TvbECpBrVMlSVrSxRUSStd1O0YdPLVkgbPZiZ6PzE6o5v3Q9OECKU1Eng1STg3fdBhsh7HYQ0Bqx0w5h3entCUYUT-uIf9O7bTdQW0gVS-V2KK0ZRfl5WlNa0xGOVlndQ6Wtl6obUjkon-8zh9cwhMVH-ilsYQuCr9ef_Z6--zdmXR2wnwcQuODOMLRPmIDmAqVdD8FLdFhkjPk7TTTX4OE18mqbk9uz4gW6dbsan_Ata0B0h</recordid><startdate>20140401</startdate><enddate>20140401</enddate><creator>Li, Mo-fei</creator><creator>Zhang, Bao-cun</creator><creator>Li, Jun</creator><creator>Sun, Li</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>AEUYN</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>20140401</creationdate><title>Sil: a Streptococcus iniae bacteriocin with dual role as an antimicrobial and an immunomodulator that inhibits innate immune response and promotes S. iniae infection</title><author>Li, Mo-fei ; Zhang, Bao-cun ; Li, Jun ; Sun, Li</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-a4200e57fff4766b71f89865ca52c048106c04e965ba477f94a4fd56ffaf5f633</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Amino acid sequence</topic><topic>Amino acids</topic><topic>Analysis</topic><topic>Animal tissues</topic><topic>Animals</topic><topic>Antibacterial agents</topic><topic>Antimicrobial agents</topic><topic>Bacillus licheniformis</topic><topic>Bacillus subtilis</topic><topic>Bacteria</topic><topic>Bacteriocins - chemistry</topic><topic>Bacteriocins - immunology</topic><topic>Biological activity</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Cells, Cultured</topic><topic>Colonization</topic><topic>Diseases</topic><topic>Distribution</topic><topic>E coli</topic><topic>Escherichia coli</topic><topic>Fish</topic><topic>Fish Diseases - immunology</topic><topic>Fish Diseases - microbiology</topic><topic>Fishes</topic><topic>Flatfishes - immunology</topic><topic>Flatfishes - microbiology</topic><topic>Genomes</topic><topic>Gram-negative bacteria</topic><topic>Gram-positive bacteria</topic><topic>Health aspects</topic><topic>Immune response</topic><topic>Immune system</topic><topic>Immunity, Innate</topic><topic>In vivo methods and tests</topic><topic>Infections</topic><topic>Infectivity</topic><topic>Innate immunity</topic><topic>Kidneys</topic><topic>Killing</topic><topic>Laboratories</topic><topic>Lactobacillus acidophilus</topic><topic>Lactobacillus rhamnosus</topic><topic>Lactococcus lactis</topic><topic>Listeria</topic><topic>Listeria monocytogenes</topic><topic>Marine biology</topic><topic>Medicine and Health Sciences</topic><topic>Microbiology</topic><topic>Monocytes</topic><topic>Monocytes - 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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>Li, Mo-fei</au><au>Zhang, Bao-cun</au><au>Li, Jun</au><au>Sun, Li</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sil: a Streptococcus iniae bacteriocin with dual role as an antimicrobial and an immunomodulator that inhibits innate immune response and promotes S. iniae infection</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-04-01</date><risdate>2014</risdate><volume>9</volume><issue>4</issue><spage>e96222</spage><epage>e96222</epage><pages>e96222-e96222</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Streptococcus iniae is a Gram-positive bacterium and a severe pathogen to a wide range of economically important fish species. In addition, S. iniae is also a zoonotic pathogen and can cause serious infections in humans. In this study, we identified from a pathogenic S. iniae strain a putative bacteriocin, Sil, and examined its biological activity. Sil is composed of 101 amino acid residues and shares 35.6% overall sequence identity with the lactococcin 972 of Lactococcus lactis. Immunoblot analysis showed that Sil was secreted by S. iniae into the extracellular milieu. Purified recombinant Sil (rSil) exhibited a dose-dependent inhibitory effect on the growth of Bacillus subtilis but had no impact on the growths of other 16 Gram-positive bacteria and 10 Gram-negative bacteria representing 23 different bacterial species. Treatment of rSil by heating at 50°C abolished the activity of rSil. rSil bound to the surface of B. subtilis but induced no killing of the target cells. Cellular study revealed that rSil interacted with turbot (Scophthalmus maximus) head kidney monocytes and inhibited the innate immune response of the cells, which led to enhanced cellular infection of S. iniae. Antibody blocking of the extracellular Sil produced by S. iniae significantly attenuated the infectivity of S. iniae. Consistent with these in vitro observations, in vivo study showed that administration of turbot with rSil prior to S. iniae infection significantly increased bacterial dissemination and colonization in fish tissues. Taken together, these results indicate that Sil is a novel virulence-associated bacteriostatic and an immunoregulator that promotes S. iniae infection by impairing the immune defense of host fish.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24781647</pmid><doi>10.1371/journal.pone.0096222</doi><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_1519899889 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Amino acid sequence Amino acids Analysis Animal tissues Animals Antibacterial agents Antimicrobial agents Bacillus licheniformis Bacillus subtilis Bacteria Bacteriocins - chemistry Bacteriocins - immunology Biological activity Biology and Life Sciences Biosynthesis Cells, Cultured Colonization Diseases Distribution E coli Escherichia coli Fish Fish Diseases - immunology Fish Diseases - microbiology Fishes Flatfishes - immunology Flatfishes - microbiology Genomes Gram-negative bacteria Gram-positive bacteria Health aspects Immune response Immune system Immunity, Innate In vivo methods and tests Infections Infectivity Innate immunity Kidneys Killing Laboratories Lactobacillus acidophilus Lactobacillus rhamnosus Lactococcus lactis Listeria Listeria monocytogenes Marine biology Medicine and Health Sciences Microbiology Monocytes Monocytes - immunology Monocytes - microbiology Pathogens Peptides Probiotics Proteins Scophthalmus maximus Streptococcal Infections - immunology Streptococcal Infections - microbiology Streptococcal Infections - veterinary Streptococcus Streptococcus - chemistry Streptococcus - immunology Streptococcus - pathogenicity Streptococcus iniae Streptococcus salivarius Streptococcus thermophilus Virulence Virulence Factors - chemistry Virulence Factors - immunology |
| title | Sil: a Streptococcus iniae bacteriocin with dual role as an antimicrobial and an immunomodulator that inhibits innate immune response and promotes S. iniae infection |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-05T12%3A31%3A42IST&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=Sil:%20a%20Streptococcus%20iniae%20bacteriocin%20with%20dual%20role%20as%20an%20antimicrobial%20and%20an%20immunomodulator%20that%20inhibits%20innate%20immune%20response%20and%20promotes%20S.%20iniae%20infection&rft.jtitle=PloS%20one&rft.au=Li,%20Mo-fei&rft.date=2014-04-01&rft.volume=9&rft.issue=4&rft.spage=e96222&rft.epage=e96222&rft.pages=e96222-e96222&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0096222&rft_dat=%3Cgale_plos_%3EA375585313%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=1519899889&rft_id=info:pmid/24781647&rft_galeid=A375585313&rft_doaj_id=oai_doaj_org_article_2dba459fa5d2471fa0f9fd6073de3022&rfr_iscdi=true |