Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus
Bacterial motility is a crucial factor during the invasion and colonization processes of pathogens, which makes it an attractive therapeutic drug target. Here, we isolated a marine bacterium ( strain 178) from a seamount in the tropical West Pacific that exhibits vigorous motility on agar plates and...
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| creator | Xiu, Pengyuan Liu, Rui Zhang, Dechao Sun, Chaomin |
| description | Bacterial motility is a crucial factor during the invasion and colonization processes of pathogens, which makes it an attractive therapeutic drug target. Here, we isolated a marine bacterium (
strain 178) from a seamount in the tropical West Pacific that exhibits vigorous motility on agar plates and severe pathogenicity to zebrafish. We found that
178 motility was significantly suppressed by another marine bacterium,
sp. strain 176, isolated from the same niche. We isolated, purified, and characterized two different cyclic lipopeptides (CLPs) from
sp. 176 using high-performance liquid chromatography, mass spectrometry, and nuclear magnetic resonance spectroscopy. The two related CLPs have a pumilacidin-like structure and were both effective inhibitors of
178 motility. The CLPs differ by only one methylene group in their fatty acid chains. In addition to motility suppression, the CLPs also induced cell aggregation in the medium and reduced adherence of
178 to glass substrates. Notably, upon CLP treatment, the expression levels of two
flagellar assembly genes (
and
) dropped dramatically. Moreover, the CLPs inhibited biofilm formation in several other strains of pathogenic bacteria without inducing cell death. This study indicates that CLPs from
sp. 176 show promise as antimicrobial lead compounds targeting bacterial motility and biofilm formation with a low potential for eliciting antibiotic resistance.
Pathogenic bacteria often require motility to establish infections and subsequently spread within host organisms. Thus, motility is an attractive therapeutic target for the development of novel antibiotics. We found that cyclic lipopeptides (CLPs) produced by marine bacterium
sp. strain 176 dramatically suppress the motility of the pathogenic bacterium
strain 178, reduce biofilm formation, and promote cellular aggregation without inducing cell death. These findings suggest that CLPs hold great promise as potential drug candidates targeting bacterial motility and biofilm formation with a low overall potential for triggering antibiotic resistance. |
| doi_str_mv | 10.1128/AEM.00450-17 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5452807</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1885952909</sourcerecordid><originalsourceid>FETCH-LOGICAL-c554t-b225f252ee951078ec0b2be76c28e7ebc6450b56e60837b643b69bb23849624e3</originalsourceid><addsrcrecordid>eNqNks1v1DAQxS0EotvCjTOyxIVDs_gjduwLUinlQ9oVSAWuVuydbac4cbCTSnvkPyfblgo4cRpr_NPzm_Ej5BlnS86FeXVytl4yVitW8eYBWXBmTaWk1A_JgjFrKyFqdkAOS7liM8a0eUwOhJHGKmkW5OfnqcPYBtxgX63wO9AVDmmAYcQNFPoWMl7Dhm5z6ui6zdgDfdOGcW5P3f6EMU6FlmFJz8fcYk95o-n5NAwZSqHjJdB1GjHiuKNpS7-hz5hoGy-wT3E3YpjKE_Jo28YCT-_qEfn67uzL6Ydq9en9x9OTVRWUqsfKC6G2QgkAqzhrDATmhYdGB2GgAR_0vAKvNGhmZON1Lb223gtpaqtFDfKIvL7VHSbfwSZAPxuObsjYtXnnUovu75seL91FunaqVsKwZhZ4eSeQ048Jyug6LAFibHtIU3Hccq65kfo_UGOUVcIyO6Mv_kGv0pT7eRNOMMm1qZubt49vqZBTKRm29745c_sYuDkG7iYGju_x53_Oeg___nf5C8OWrfY</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2031684707</pqid></control><display><type>article</type><title>Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus</title><source>American Society for Microbiology</source><source>MEDLINE</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><creator>Xiu, Pengyuan ; Liu, Rui ; Zhang, Dechao ; Sun, Chaomin</creator><contributor>Nojiri, Hideaki</contributor><creatorcontrib>Xiu, Pengyuan ; Liu, Rui ; Zhang, Dechao ; Sun, Chaomin ; Nojiri, Hideaki</creatorcontrib><description>Bacterial motility is a crucial factor during the invasion and colonization processes of pathogens, which makes it an attractive therapeutic drug target. Here, we isolated a marine bacterium (
strain 178) from a seamount in the tropical West Pacific that exhibits vigorous motility on agar plates and severe pathogenicity to zebrafish. We found that
178 motility was significantly suppressed by another marine bacterium,
sp. strain 176, isolated from the same niche. We isolated, purified, and characterized two different cyclic lipopeptides (CLPs) from
sp. 176 using high-performance liquid chromatography, mass spectrometry, and nuclear magnetic resonance spectroscopy. The two related CLPs have a pumilacidin-like structure and were both effective inhibitors of
178 motility. The CLPs differ by only one methylene group in their fatty acid chains. In addition to motility suppression, the CLPs also induced cell aggregation in the medium and reduced adherence of
178 to glass substrates. Notably, upon CLP treatment, the expression levels of two
flagellar assembly genes (
and
) dropped dramatically. Moreover, the CLPs inhibited biofilm formation in several other strains of pathogenic bacteria without inducing cell death. This study indicates that CLPs from
sp. 176 show promise as antimicrobial lead compounds targeting bacterial motility and biofilm formation with a low potential for eliciting antibiotic resistance.
Pathogenic bacteria often require motility to establish infections and subsequently spread within host organisms. Thus, motility is an attractive therapeutic target for the development of novel antibiotics. We found that cyclic lipopeptides (CLPs) produced by marine bacterium
sp. strain 176 dramatically suppress the motility of the pathogenic bacterium
strain 178, reduce biofilm formation, and promote cellular aggregation without inducing cell death. These findings suggest that CLPs hold great promise as potential drug candidates targeting bacterial motility and biofilm formation with a low overall potential for triggering antibiotic resistance.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/AEM.00450-17</identifier><identifier>PMID: 28389538</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Agglomeration ; Anti-Bacterial Agents - chemistry ; Anti-Bacterial Agents - metabolism ; Anti-Bacterial Agents - pharmacology ; Antibiotic resistance ; Antibiotics ; Bacillus ; Bacillus - chemistry ; Bacillus - genetics ; Bacillus - isolation & purification ; Bacillus - metabolism ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biofilms ; Cell aggregation ; Cell death ; Colonization ; Danio rerio ; Drug development ; Drug resistance ; Environmental Microbiology ; Fatty acids ; Flagella ; Gene expression ; Gene Expression Regulation, Bacterial ; Glass substrates ; High performance liquid chromatography ; Lead compounds ; Lipopeptides ; Lipopeptides - chemistry ; Lipopeptides - metabolism ; Lipopeptides - pharmacology ; Liquid chromatography ; Magnetic resonance spectroscopy ; Mass spectrometry ; Mass spectroscopy ; NMR ; Nuclear magnetic resonance ; Pathogenicity ; Pathogens ; Seawater - microbiology ; Therapeutic applications ; Vibrio alginolyticus ; Vibrio alginolyticus - classification ; Vibrio alginolyticus - drug effects ; Waterborne diseases ; Zebrafish</subject><ispartof>Applied and environmental microbiology, 2017-06, Vol.83 (12)</ispartof><rights>Copyright © 2017 American Society for Microbiology.</rights><rights>Copyright American Society for Microbiology Jun 2017</rights><rights>Copyright © 2017 American Society for Microbiology. 2017 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c554t-b225f252ee951078ec0b2be76c28e7ebc6450b56e60837b643b69bb23849624e3</citedby><cites>FETCH-LOGICAL-c554t-b225f252ee951078ec0b2be76c28e7ebc6450b56e60837b643b69bb23849624e3</cites><orcidid>0000-0002-9296-9091</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5452807/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5452807/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,3174,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28389538$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Nojiri, Hideaki</contributor><creatorcontrib>Xiu, Pengyuan</creatorcontrib><creatorcontrib>Liu, Rui</creatorcontrib><creatorcontrib>Zhang, Dechao</creatorcontrib><creatorcontrib>Sun, Chaomin</creatorcontrib><title>Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><description>Bacterial motility is a crucial factor during the invasion and colonization processes of pathogens, which makes it an attractive therapeutic drug target. Here, we isolated a marine bacterium (
strain 178) from a seamount in the tropical West Pacific that exhibits vigorous motility on agar plates and severe pathogenicity to zebrafish. We found that
178 motility was significantly suppressed by another marine bacterium,
sp. strain 176, isolated from the same niche. We isolated, purified, and characterized two different cyclic lipopeptides (CLPs) from
sp. 176 using high-performance liquid chromatography, mass spectrometry, and nuclear magnetic resonance spectroscopy. The two related CLPs have a pumilacidin-like structure and were both effective inhibitors of
178 motility. The CLPs differ by only one methylene group in their fatty acid chains. In addition to motility suppression, the CLPs also induced cell aggregation in the medium and reduced adherence of
178 to glass substrates. Notably, upon CLP treatment, the expression levels of two
flagellar assembly genes (
and
) dropped dramatically. Moreover, the CLPs inhibited biofilm formation in several other strains of pathogenic bacteria without inducing cell death. This study indicates that CLPs from
sp. 176 show promise as antimicrobial lead compounds targeting bacterial motility and biofilm formation with a low potential for eliciting antibiotic resistance.
Pathogenic bacteria often require motility to establish infections and subsequently spread within host organisms. Thus, motility is an attractive therapeutic target for the development of novel antibiotics. We found that cyclic lipopeptides (CLPs) produced by marine bacterium
sp. strain 176 dramatically suppress the motility of the pathogenic bacterium
strain 178, reduce biofilm formation, and promote cellular aggregation without inducing cell death. These findings suggest that CLPs hold great promise as potential drug candidates targeting bacterial motility and biofilm formation with a low overall potential for triggering antibiotic resistance.</description><subject>Agglomeration</subject><subject>Anti-Bacterial Agents - chemistry</subject><subject>Anti-Bacterial Agents - metabolism</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Bacillus</subject><subject>Bacillus - chemistry</subject><subject>Bacillus - genetics</subject><subject>Bacillus - isolation & purification</subject><subject>Bacillus - metabolism</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biofilms</subject><subject>Cell aggregation</subject><subject>Cell death</subject><subject>Colonization</subject><subject>Danio rerio</subject><subject>Drug development</subject><subject>Drug resistance</subject><subject>Environmental Microbiology</subject><subject>Fatty acids</subject><subject>Flagella</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Glass substrates</subject><subject>High performance liquid chromatography</subject><subject>Lead compounds</subject><subject>Lipopeptides</subject><subject>Lipopeptides - chemistry</subject><subject>Lipopeptides - metabolism</subject><subject>Lipopeptides - pharmacology</subject><subject>Liquid chromatography</subject><subject>Magnetic resonance spectroscopy</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>NMR</subject><subject>Nuclear magnetic resonance</subject><subject>Pathogenicity</subject><subject>Pathogens</subject><subject>Seawater - microbiology</subject><subject>Therapeutic applications</subject><subject>Vibrio alginolyticus</subject><subject>Vibrio alginolyticus - classification</subject><subject>Vibrio alginolyticus - drug effects</subject><subject>Waterborne diseases</subject><subject>Zebrafish</subject><issn>0099-2240</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNks1v1DAQxS0EotvCjTOyxIVDs_gjduwLUinlQ9oVSAWuVuydbac4cbCTSnvkPyfblgo4cRpr_NPzm_Ej5BlnS86FeXVytl4yVitW8eYBWXBmTaWk1A_JgjFrKyFqdkAOS7liM8a0eUwOhJHGKmkW5OfnqcPYBtxgX63wO9AVDmmAYcQNFPoWMl7Dhm5z6ui6zdgDfdOGcW5P3f6EMU6FlmFJz8fcYk95o-n5NAwZSqHjJdB1GjHiuKNpS7-hz5hoGy-wT3E3YpjKE_Jo28YCT-_qEfn67uzL6Ydq9en9x9OTVRWUqsfKC6G2QgkAqzhrDATmhYdGB2GgAR_0vAKvNGhmZON1Lb223gtpaqtFDfKIvL7VHSbfwSZAPxuObsjYtXnnUovu75seL91FunaqVsKwZhZ4eSeQ048Jyug6LAFibHtIU3Hccq65kfo_UGOUVcIyO6Mv_kGv0pT7eRNOMMm1qZubt49vqZBTKRm29745c_sYuDkG7iYGju_x53_Oeg___nf5C8OWrfY</recordid><startdate>20170615</startdate><enddate>20170615</enddate><creator>Xiu, Pengyuan</creator><creator>Liu, Rui</creator><creator>Zhang, Dechao</creator><creator>Sun, Chaomin</creator><general>American Society for Microbiology</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>7QL</scope><scope>7QO</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9296-9091</orcidid></search><sort><creationdate>20170615</creationdate><title>Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus</title><author>Xiu, Pengyuan ; Liu, Rui ; Zhang, Dechao ; Sun, Chaomin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c554t-b225f252ee951078ec0b2be76c28e7ebc6450b56e60837b643b69bb23849624e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Agglomeration</topic><topic>Anti-Bacterial Agents - chemistry</topic><topic>Anti-Bacterial Agents - metabolism</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Antibiotic resistance</topic><topic>Antibiotics</topic><topic>Bacillus</topic><topic>Bacillus - chemistry</topic><topic>Bacillus - genetics</topic><topic>Bacillus - isolation & purification</topic><topic>Bacillus - metabolism</topic><topic>Bacteria</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Biofilms</topic><topic>Cell aggregation</topic><topic>Cell death</topic><topic>Colonization</topic><topic>Danio rerio</topic><topic>Drug development</topic><topic>Drug resistance</topic><topic>Environmental Microbiology</topic><topic>Fatty acids</topic><topic>Flagella</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Glass substrates</topic><topic>High performance liquid chromatography</topic><topic>Lead compounds</topic><topic>Lipopeptides</topic><topic>Lipopeptides - chemistry</topic><topic>Lipopeptides - metabolism</topic><topic>Lipopeptides - pharmacology</topic><topic>Liquid chromatography</topic><topic>Magnetic resonance spectroscopy</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>NMR</topic><topic>Nuclear magnetic resonance</topic><topic>Pathogenicity</topic><topic>Pathogens</topic><topic>Seawater - microbiology</topic><topic>Therapeutic applications</topic><topic>Vibrio alginolyticus</topic><topic>Vibrio alginolyticus - classification</topic><topic>Vibrio alginolyticus - drug effects</topic><topic>Waterborne diseases</topic><topic>Zebrafish</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xiu, Pengyuan</creatorcontrib><creatorcontrib>Liu, Rui</creatorcontrib><creatorcontrib>Zhang, Dechao</creatorcontrib><creatorcontrib>Sun, Chaomin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Applied and environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xiu, Pengyuan</au><au>Liu, Rui</au><au>Zhang, Dechao</au><au>Sun, Chaomin</au><au>Nojiri, Hideaki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus</atitle><jtitle>Applied and environmental microbiology</jtitle><addtitle>Appl Environ Microbiol</addtitle><date>2017-06-15</date><risdate>2017</risdate><volume>83</volume><issue>12</issue><issn>0099-2240</issn><eissn>1098-5336</eissn><abstract>Bacterial motility is a crucial factor during the invasion and colonization processes of pathogens, which makes it an attractive therapeutic drug target. Here, we isolated a marine bacterium (
strain 178) from a seamount in the tropical West Pacific that exhibits vigorous motility on agar plates and severe pathogenicity to zebrafish. We found that
178 motility was significantly suppressed by another marine bacterium,
sp. strain 176, isolated from the same niche. We isolated, purified, and characterized two different cyclic lipopeptides (CLPs) from
sp. 176 using high-performance liquid chromatography, mass spectrometry, and nuclear magnetic resonance spectroscopy. The two related CLPs have a pumilacidin-like structure and were both effective inhibitors of
178 motility. The CLPs differ by only one methylene group in their fatty acid chains. In addition to motility suppression, the CLPs also induced cell aggregation in the medium and reduced adherence of
178 to glass substrates. Notably, upon CLP treatment, the expression levels of two
flagellar assembly genes (
and
) dropped dramatically. Moreover, the CLPs inhibited biofilm formation in several other strains of pathogenic bacteria without inducing cell death. This study indicates that CLPs from
sp. 176 show promise as antimicrobial lead compounds targeting bacterial motility and biofilm formation with a low potential for eliciting antibiotic resistance.
Pathogenic bacteria often require motility to establish infections and subsequently spread within host organisms. Thus, motility is an attractive therapeutic target for the development of novel antibiotics. We found that cyclic lipopeptides (CLPs) produced by marine bacterium
sp. strain 176 dramatically suppress the motility of the pathogenic bacterium
strain 178, reduce biofilm formation, and promote cellular aggregation without inducing cell death. These findings suggest that CLPs hold great promise as potential drug candidates targeting bacterial motility and biofilm formation with a low overall potential for triggering antibiotic resistance.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>28389538</pmid><doi>10.1128/AEM.00450-17</doi><orcidid>https://orcid.org/0000-0002-9296-9091</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Agglomeration Anti-Bacterial Agents - chemistry Anti-Bacterial Agents - metabolism Anti-Bacterial Agents - pharmacology Antibiotic resistance Antibiotics Bacillus Bacillus - chemistry Bacillus - genetics Bacillus - isolation & purification Bacillus - metabolism Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Biofilms Cell aggregation Cell death Colonization Danio rerio Drug development Drug resistance Environmental Microbiology Fatty acids Flagella Gene expression Gene Expression Regulation, Bacterial Glass substrates High performance liquid chromatography Lead compounds Lipopeptides Lipopeptides - chemistry Lipopeptides - metabolism Lipopeptides - pharmacology Liquid chromatography Magnetic resonance spectroscopy Mass spectrometry Mass spectroscopy NMR Nuclear magnetic resonance Pathogenicity Pathogens Seawater - microbiology Therapeutic applications Vibrio alginolyticus Vibrio alginolyticus - classification Vibrio alginolyticus - drug effects Waterborne diseases Zebrafish |
| title | Pumilacidin-Like Lipopeptides Derived from Marine Bacterium Bacillus sp. Strain 176 Suppress the Motility of Vibrio alginolyticus |
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