Genome analysis of secondary metabolite‑biosynthetic gene clusters of Photorhabdus akhurstii subsp. akhurstii and its antibacterial activity against antibiotic-resistant bacteria
Xenorhabdus and Photorhabdus can produce a variety of secondary metabolites with broad spectrum bioactivity against microorganisms. We investigated the antibacterial activity of Xenorhabdus and Photorhabdus against 15 antibiotic-resistant bacteria strains. Photorhabdus extracts had strong inhibitory...
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| Veröffentlicht in: | PloS one 2022-09, Vol.17 (9), p.e0274956 |
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| creator | Muangpat, Paramaporn Meesil, Wipanee Ngoenkam, Jatuporn Teethaisong, Yothin Thummeepak, Rapee Sitthisak, Sutthirat Tandhavanant, Sarunporn Chantratita, Narisara Bode, Helge B Vitta, Apichat Thanwisai, Aunchalee |
| description | Xenorhabdus and Photorhabdus can produce a variety of secondary metabolites with broad spectrum bioactivity against microorganisms. We investigated the antibacterial activity of Xenorhabdus and Photorhabdus against 15 antibiotic-resistant bacteria strains. Photorhabdus extracts had strong inhibitory the growth of Methicillin-resistant Staphylococcus aureus (MRSA) by disk diffusion. The P. akhurstii s subsp. akhurstii (bNN168.5_TH) extract showed lower minimum inhibitory concentrations (MIC) and minimal bactericidal concentrations (MBC). The interaction between either P. akhurstii subsp. akhurstii (bNN141.3_TH) or P. akhurstii subsp. akhurstii (bNN168.5_TH) or P. hainanensis (bNN163.3_TH) extract in combination with oxacillin determined by checkerboard assay exhibited partially synergistic interaction with fractional inhibitory concentration index (FICI) of 0.53. Time-killing assay for P. akhurstii subsp. akhurstii (bNN168.5_TH) extract against S. aureus strain PB36 significantly decreased cell viability from 105 CFU/ml to 103 CFU/ml within 30 min (P < 0.001, t-test). Transmission electron microscopic investigation elucidated that the bNN168.5_TH extract caused treated S. aureus strain PB36 (MRSA) cell membrane damage. The biosynthetic gene clusters of the bNN168.5_TH contained non-ribosomal peptide synthetase cluster (NRPS), hybrid NRPS-type l polyketide synthase (PKS) and siderophore, which identified potentially interesting bioactive products: xenematide, luminmide, xenortide A-D, luminmycin A, putrebactin/avaroferrin and rhizomide A-C. This study demonstrates that bNN168.5_TH showed antibacterial activity by disrupting bacterial cytoplasmic membrane and the draft genome provided insights into the classes of bioactive products. This also provides a potential approach in developing a novel antibacterial agent. |
| doi_str_mv | 10.1371/journal.pone.0274956 |
| format | Article |
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We investigated the antibacterial activity of Xenorhabdus and Photorhabdus against 15 antibiotic-resistant bacteria strains. Photorhabdus extracts had strong inhibitory the growth of Methicillin-resistant Staphylococcus aureus (MRSA) by disk diffusion. The P. akhurstii s subsp. akhurstii (bNN168.5_TH) extract showed lower minimum inhibitory concentrations (MIC) and minimal bactericidal concentrations (MBC). The interaction between either P. akhurstii subsp. akhurstii (bNN141.3_TH) or P. akhurstii subsp. akhurstii (bNN168.5_TH) or P. hainanensis (bNN163.3_TH) extract in combination with oxacillin determined by checkerboard assay exhibited partially synergistic interaction with fractional inhibitory concentration index (FICI) of 0.53. Time-killing assay for P. akhurstii subsp. akhurstii (bNN168.5_TH) extract against S. aureus strain PB36 significantly decreased cell viability from 105 CFU/ml to 103 CFU/ml within 30 min (P < 0.001, t-test). Transmission electron microscopic investigation elucidated that the bNN168.5_TH extract caused treated S. aureus strain PB36 (MRSA) cell membrane damage. The biosynthetic gene clusters of the bNN168.5_TH contained non-ribosomal peptide synthetase cluster (NRPS), hybrid NRPS-type l polyketide synthase (PKS) and siderophore, which identified potentially interesting bioactive products: xenematide, luminmide, xenortide A-D, luminmycin A, putrebactin/avaroferrin and rhizomide A-C. This study demonstrates that bNN168.5_TH showed antibacterial activity by disrupting bacterial cytoplasmic membrane and the draft genome provided insights into the classes of bioactive products. This also provides a potential approach in developing a novel antibacterial agent.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0274956</identifier><identifier>PMID: 36129957</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Anti-Bacterial Agents - chemistry ; Antibacterial activity ; Antibacterial agents ; Antibiotic resistance ; Antibiotics ; Antimicrobial agents ; Bacteria ; Biological activity ; Biology and Life Sciences ; Cell membranes ; Cell viability ; Clusters ; Drug resistance ; E coli ; Gene clusters ; Genetic aspects ; Genomes ; Gram-negative bacteria ; Health aspects ; Medicine and Health Sciences ; Metabolites ; Methicillin ; Methicillin resistance ; Methicillin-Resistant Staphylococcus aureus - genetics ; Microbial Sensitivity Tests ; Microorganisms ; Minimum inhibitory concentration ; Mortality ; Multigene Family ; Nematoda ; Nematodes ; Oxacillin ; Oxacillin - pharmacology ; Peptides ; Photorhabdus ; Photorhabdus - metabolism ; Plant Extracts - pharmacology ; Plant metabolites ; Polyketide synthase ; Polyketide Synthases - genetics ; Secondary metabolites ; Siderophores - metabolism ; Staphylococcus aureus ; Staphylococcus aureus - genetics ; Staphylococcus infections ; Xenorhabdus ; Xenorhabdus - genetics</subject><ispartof>PloS one, 2022-09, Vol.17 (9), p.e0274956</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Muangpat 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. 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We investigated the antibacterial activity of Xenorhabdus and Photorhabdus against 15 antibiotic-resistant bacteria strains. Photorhabdus extracts had strong inhibitory the growth of Methicillin-resistant Staphylococcus aureus (MRSA) by disk diffusion. The P. akhurstii s subsp. akhurstii (bNN168.5_TH) extract showed lower minimum inhibitory concentrations (MIC) and minimal bactericidal concentrations (MBC). The interaction between either P. akhurstii subsp. akhurstii (bNN141.3_TH) or P. akhurstii subsp. akhurstii (bNN168.5_TH) or P. hainanensis (bNN163.3_TH) extract in combination with oxacillin determined by checkerboard assay exhibited partially synergistic interaction with fractional inhibitory concentration index (FICI) of 0.53. Time-killing assay for P. akhurstii subsp. akhurstii (bNN168.5_TH) extract against S. aureus strain PB36 significantly decreased cell viability from 105 CFU/ml to 103 CFU/ml within 30 min (P < 0.001, t-test). Transmission electron microscopic investigation elucidated that the bNN168.5_TH extract caused treated S. aureus strain PB36 (MRSA) cell membrane damage. The biosynthetic gene clusters of the bNN168.5_TH contained non-ribosomal peptide synthetase cluster (NRPS), hybrid NRPS-type l polyketide synthase (PKS) and siderophore, which identified potentially interesting bioactive products: xenematide, luminmide, xenortide A-D, luminmycin A, putrebactin/avaroferrin and rhizomide A-C. This study demonstrates that bNN168.5_TH showed antibacterial activity by disrupting bacterial cytoplasmic membrane and the draft genome provided insights into the classes of bioactive products. This also provides a potential approach in developing a novel antibacterial agent.</description><subject>Anti-Bacterial Agents - chemistry</subject><subject>Antibacterial activity</subject><subject>Antibacterial agents</subject><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Antimicrobial agents</subject><subject>Bacteria</subject><subject>Biological activity</subject><subject>Biology and Life Sciences</subject><subject>Cell membranes</subject><subject>Cell viability</subject><subject>Clusters</subject><subject>Drug resistance</subject><subject>E coli</subject><subject>Gene clusters</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Gram-negative bacteria</subject><subject>Health aspects</subject><subject>Medicine and Health Sciences</subject><subject>Metabolites</subject><subject>Methicillin</subject><subject>Methicillin resistance</subject><subject>Methicillin-Resistant Staphylococcus aureus - genetics</subject><subject>Microbial Sensitivity Tests</subject><subject>Microorganisms</subject><subject>Minimum inhibitory concentration</subject><subject>Mortality</subject><subject>Multigene Family</subject><subject>Nematoda</subject><subject>Nematodes</subject><subject>Oxacillin</subject><subject>Oxacillin - 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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>Muangpat, Paramaporn</au><au>Meesil, Wipanee</au><au>Ngoenkam, Jatuporn</au><au>Teethaisong, Yothin</au><au>Thummeepak, Rapee</au><au>Sitthisak, Sutthirat</au><au>Tandhavanant, Sarunporn</au><au>Chantratita, Narisara</au><au>Bode, Helge B</au><au>Vitta, Apichat</au><au>Thanwisai, Aunchalee</au><au>Dutta, Tushar Kanti</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome analysis of secondary metabolite‑biosynthetic gene clusters of Photorhabdus akhurstii subsp. akhurstii and its antibacterial activity against antibiotic-resistant bacteria</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2022-09-21</date><risdate>2022</risdate><volume>17</volume><issue>9</issue><spage>e0274956</spage><pages>e0274956-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Xenorhabdus and Photorhabdus can produce a variety of secondary metabolites with broad spectrum bioactivity against microorganisms. We investigated the antibacterial activity of Xenorhabdus and Photorhabdus against 15 antibiotic-resistant bacteria strains. Photorhabdus extracts had strong inhibitory the growth of Methicillin-resistant Staphylococcus aureus (MRSA) by disk diffusion. The P. akhurstii s subsp. akhurstii (bNN168.5_TH) extract showed lower minimum inhibitory concentrations (MIC) and minimal bactericidal concentrations (MBC). The interaction between either P. akhurstii subsp. akhurstii (bNN141.3_TH) or P. akhurstii subsp. akhurstii (bNN168.5_TH) or P. hainanensis (bNN163.3_TH) extract in combination with oxacillin determined by checkerboard assay exhibited partially synergistic interaction with fractional inhibitory concentration index (FICI) of 0.53. Time-killing assay for P. akhurstii subsp. akhurstii (bNN168.5_TH) extract against S. aureus strain PB36 significantly decreased cell viability from 105 CFU/ml to 103 CFU/ml within 30 min (P < 0.001, t-test). Transmission electron microscopic investigation elucidated that the bNN168.5_TH extract caused treated S. aureus strain PB36 (MRSA) cell membrane damage. The biosynthetic gene clusters of the bNN168.5_TH contained non-ribosomal peptide synthetase cluster (NRPS), hybrid NRPS-type l polyketide synthase (PKS) and siderophore, which identified potentially interesting bioactive products: xenematide, luminmide, xenortide A-D, luminmycin A, putrebactin/avaroferrin and rhizomide A-C. This study demonstrates that bNN168.5_TH showed antibacterial activity by disrupting bacterial cytoplasmic membrane and the draft genome provided insights into the classes of bioactive products. This also provides a potential approach in developing a novel antibacterial agent.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>36129957</pmid><doi>10.1371/journal.pone.0274956</doi><tpages>e0274956</tpages><orcidid>https://orcid.org/0000-0001-7842-2850</orcidid><orcidid>https://orcid.org/0000-0002-0387-8666</orcidid><orcidid>https://orcid.org/0000-0003-0261-3233</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2022-09, Vol.17 (9), p.e0274956 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2716502631 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS) Journals Open Access; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Anti-Bacterial Agents - chemistry Antibacterial activity Antibacterial agents Antibiotic resistance Antibiotics Antimicrobial agents Bacteria Biological activity Biology and Life Sciences Cell membranes Cell viability Clusters Drug resistance E coli Gene clusters Genetic aspects Genomes Gram-negative bacteria Health aspects Medicine and Health Sciences Metabolites Methicillin Methicillin resistance Methicillin-Resistant Staphylococcus aureus - genetics Microbial Sensitivity Tests Microorganisms Minimum inhibitory concentration Mortality Multigene Family Nematoda Nematodes Oxacillin Oxacillin - pharmacology Peptides Photorhabdus Photorhabdus - metabolism Plant Extracts - pharmacology Plant metabolites Polyketide synthase Polyketide Synthases - genetics Secondary metabolites Siderophores - metabolism Staphylococcus aureus Staphylococcus aureus - genetics Staphylococcus infections Xenorhabdus Xenorhabdus - genetics |
| title | Genome analysis of secondary metabolite‑biosynthetic gene clusters of Photorhabdus akhurstii subsp. akhurstii and its antibacterial activity against antibiotic-resistant bacteria |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-05T14%3A24%3A23IST&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=Genome%20analysis%20of%20secondary%20metabolite%E2%80%91biosynthetic%20gene%20clusters%20of%20Photorhabdus%20akhurstii%20subsp.%20akhurstii%20and%20its%20antibacterial%20activity%20against%20antibiotic-resistant%20bacteria&rft.jtitle=PloS%20one&rft.au=Muangpat,%20Paramaporn&rft.date=2022-09-21&rft.volume=17&rft.issue=9&rft.spage=e0274956&rft.pages=e0274956-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0274956&rft_dat=%3Cgale_plos_%3EA718803444%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=2716502631&rft_id=info:pmid/36129957&rft_galeid=A718803444&rft_doaj_id=oai_doaj_org_article_4ee67d2b0bf14c1692a01ac1cbc721fd&rfr_iscdi=true |