Membrane vesicles from a Dietzia bacterium containing multiple cargoes and their roles in iron delivery
Summary Membrane vesicles (MVs) released from bacteria act as extracellular vehicles carrying various functional cargoes between cells. MVs with different cargoes play multiple roles in stress adaptation, nutrient acquisition and microbial interactions. However, previous studies have primarily focus...
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Veröffentlicht in: | Environmental microbiology 2021-02, Vol.23 (2), p.1009-1019 |
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creator | Wang, Meng Nie, Yong Wu, Xiao‐Lei |
description | Summary
Membrane vesicles (MVs) released from bacteria act as extracellular vehicles carrying various functional cargoes between cells. MVs with different cargoes play multiple roles in stress adaptation, nutrient acquisition and microbial interactions. However, previous studies have primarily focused on MVs from Gram‐negative bacteria, while the characteristics of cargoes in MVs from Gram‐positive bacteria and their involvement in microbial interactions remain to be elucidated. Here, we used a Gram‐positive strain, Dietzia sp. DQ12‐45‐1b from Corynebacteriales, to analyse the characteristics and functions of MVs. We identified the ‘antioxidant’ canthaxanthin is stored within MVs by LC–MS/MS. In addition, nearly the entire genomic content of strain DQ12‐45‐1b are evenly distributed in MVs, suggesting that MVs from DQ12‐45‐1b might involve in horizontal gene transfer. Finally, the mycobactin‐type siderophores were detected in MVs. The iron‐loaded MVs effectively mediate iron binding and delivery to homologous bacteria from the order Corynebacteriales, but not to more distantly related species from the orders Pseudomonadales, Bacillales and Enterobacterales. These results revealed that the iron‐loaded MVs are shared between homologous species. Together, we report the Gram‐positive bacterium Dietzia sp. DQ12‐45‐1b released MVs that contain canthaxanthin, DNA and siderophores and prove that MVs act as public goods between closely related species. |
doi_str_mv | 10.1111/1462-2920.15278 |
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Membrane vesicles (MVs) released from bacteria act as extracellular vehicles carrying various functional cargoes between cells. MVs with different cargoes play multiple roles in stress adaptation, nutrient acquisition and microbial interactions. However, previous studies have primarily focused on MVs from Gram‐negative bacteria, while the characteristics of cargoes in MVs from Gram‐positive bacteria and their involvement in microbial interactions remain to be elucidated. Here, we used a Gram‐positive strain, Dietzia sp. DQ12‐45‐1b from Corynebacteriales, to analyse the characteristics and functions of MVs. We identified the ‘antioxidant’ canthaxanthin is stored within MVs by LC–MS/MS. In addition, nearly the entire genomic content of strain DQ12‐45‐1b are evenly distributed in MVs, suggesting that MVs from DQ12‐45‐1b might involve in horizontal gene transfer. Finally, the mycobactin‐type siderophores were detected in MVs. The iron‐loaded MVs effectively mediate iron binding and delivery to homologous bacteria from the order Corynebacteriales, but not to more distantly related species from the orders Pseudomonadales, Bacillales and Enterobacterales. These results revealed that the iron‐loaded MVs are shared between homologous species. Together, we report the Gram‐positive bacterium Dietzia sp. DQ12‐45‐1b released MVs that contain canthaxanthin, DNA and siderophores and prove that MVs act as public goods between closely related species.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.15278</identifier><identifier>PMID: 33048442</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Antioxidants ; Bacteria ; Cargo ; Deoxyribonucleic acid ; Dietzia ; DNA ; Extracellular ; Gene transfer ; Gram-negative bacteria ; Homology ; Horizontal transfer ; Iron ; Membrane vesicles ; Membranes ; Microbiological strains ; Microorganisms ; Siderophores ; Species ; Vesicles</subject><ispartof>Environmental microbiology, 2021-02, Vol.23 (2), p.1009-1019</ispartof><rights>2020 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>2020 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2021 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c2868-6294084db5ebd9b528dd4a0d08837f2dfd74b95d6f1f7bbb73c5c420e3e79eef3</citedby><cites>FETCH-LOGICAL-c2868-6294084db5ebd9b528dd4a0d08837f2dfd74b95d6f1f7bbb73c5c420e3e79eef3</cites><orcidid>0000-0002-9897-6903</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1462-2920.15278$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1462-2920.15278$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33048442$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Meng</creatorcontrib><creatorcontrib>Nie, Yong</creatorcontrib><creatorcontrib>Wu, Xiao‐Lei</creatorcontrib><title>Membrane vesicles from a Dietzia bacterium containing multiple cargoes and their roles in iron delivery</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Membrane vesicles (MVs) released from bacteria act as extracellular vehicles carrying various functional cargoes between cells. MVs with different cargoes play multiple roles in stress adaptation, nutrient acquisition and microbial interactions. However, previous studies have primarily focused on MVs from Gram‐negative bacteria, while the characteristics of cargoes in MVs from Gram‐positive bacteria and their involvement in microbial interactions remain to be elucidated. Here, we used a Gram‐positive strain, Dietzia sp. DQ12‐45‐1b from Corynebacteriales, to analyse the characteristics and functions of MVs. We identified the ‘antioxidant’ canthaxanthin is stored within MVs by LC–MS/MS. In addition, nearly the entire genomic content of strain DQ12‐45‐1b are evenly distributed in MVs, suggesting that MVs from DQ12‐45‐1b might involve in horizontal gene transfer. Finally, the mycobactin‐type siderophores were detected in MVs. The iron‐loaded MVs effectively mediate iron binding and delivery to homologous bacteria from the order Corynebacteriales, but not to more distantly related species from the orders Pseudomonadales, Bacillales and Enterobacterales. These results revealed that the iron‐loaded MVs are shared between homologous species. Together, we report the Gram‐positive bacterium Dietzia sp. DQ12‐45‐1b released MVs that contain canthaxanthin, DNA and siderophores and prove that MVs act as public goods between closely related species.</description><subject>Antioxidants</subject><subject>Bacteria</subject><subject>Cargo</subject><subject>Deoxyribonucleic acid</subject><subject>Dietzia</subject><subject>DNA</subject><subject>Extracellular</subject><subject>Gene transfer</subject><subject>Gram-negative bacteria</subject><subject>Homology</subject><subject>Horizontal transfer</subject><subject>Iron</subject><subject>Membrane vesicles</subject><subject>Membranes</subject><subject>Microbiological strains</subject><subject>Microorganisms</subject><subject>Siderophores</subject><subject>Species</subject><subject>Vesicles</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqFkTlPxDAQRi0E4q7pkCUamgXHsWOnRNwSiAZqy8dkMUrixU4WLb8eLwtb0ODGh948jb9B6KggZ0Ve5wWr6ITWNF85FXID7a5fNtfngu6gvZTeCClEKcg22ilLwiRjdBdNH6EzUfeA55C8bSHhJoYOa3zlYfj0GhttB4h-7LAN_aB97_sp7sZ28LMWsNVxGnKR7h0eXsFHHMNS4nvsY-ixg9bPIS4O0Faj2wSHP_s-erm5fr68mzw83d5fXjxMLJWVnFS0ZkQyZzgYVxtOpXNME0ekLEVDXeMEMzV3VVM0whgjSsstowRKEDVAU-6j05V3FsP7CGlQnU8W2jZ_MYxJUcZJJSiXLKMnf9C3MMY-d5epmlailpRn6nxF2RhSitCoWfSdjgtVELWcgVqmrJaJq-8Z5IrjH-9oOnBr_jf0DPAV8OFbWPznU9eP9yvxF7f-kVk</recordid><startdate>202102</startdate><enddate>202102</enddate><creator>Wang, Meng</creator><creator>Nie, Yong</creator><creator>Wu, Xiao‐Lei</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-9897-6903</orcidid></search><sort><creationdate>202102</creationdate><title>Membrane vesicles from a Dietzia bacterium containing multiple cargoes and their roles in iron delivery</title><author>Wang, Meng ; Nie, Yong ; Wu, Xiao‐Lei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c2868-6294084db5ebd9b528dd4a0d08837f2dfd74b95d6f1f7bbb73c5c420e3e79eef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Antioxidants</topic><topic>Bacteria</topic><topic>Cargo</topic><topic>Deoxyribonucleic acid</topic><topic>Dietzia</topic><topic>DNA</topic><topic>Extracellular</topic><topic>Gene transfer</topic><topic>Gram-negative bacteria</topic><topic>Homology</topic><topic>Horizontal transfer</topic><topic>Iron</topic><topic>Membrane vesicles</topic><topic>Membranes</topic><topic>Microbiological strains</topic><topic>Microorganisms</topic><topic>Siderophores</topic><topic>Species</topic><topic>Vesicles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Meng</creatorcontrib><creatorcontrib>Nie, Yong</creatorcontrib><creatorcontrib>Wu, Xiao‐Lei</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Aqualine</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Oceanic Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Water Resources Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 3: Aquatic Pollution & Environmental Quality</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Meng</au><au>Nie, Yong</au><au>Wu, Xiao‐Lei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Membrane vesicles from a Dietzia bacterium containing multiple cargoes and their roles in iron delivery</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2021-02</date><risdate>2021</risdate><volume>23</volume><issue>2</issue><spage>1009</spage><epage>1019</epage><pages>1009-1019</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Membrane vesicles (MVs) released from bacteria act as extracellular vehicles carrying various functional cargoes between cells. MVs with different cargoes play multiple roles in stress adaptation, nutrient acquisition and microbial interactions. However, previous studies have primarily focused on MVs from Gram‐negative bacteria, while the characteristics of cargoes in MVs from Gram‐positive bacteria and their involvement in microbial interactions remain to be elucidated. Here, we used a Gram‐positive strain, Dietzia sp. DQ12‐45‐1b from Corynebacteriales, to analyse the characteristics and functions of MVs. We identified the ‘antioxidant’ canthaxanthin is stored within MVs by LC–MS/MS. In addition, nearly the entire genomic content of strain DQ12‐45‐1b are evenly distributed in MVs, suggesting that MVs from DQ12‐45‐1b might involve in horizontal gene transfer. Finally, the mycobactin‐type siderophores were detected in MVs. The iron‐loaded MVs effectively mediate iron binding and delivery to homologous bacteria from the order Corynebacteriales, but not to more distantly related species from the orders Pseudomonadales, Bacillales and Enterobacterales. These results revealed that the iron‐loaded MVs are shared between homologous species. Together, we report the Gram‐positive bacterium Dietzia sp. DQ12‐45‐1b released MVs that contain canthaxanthin, DNA and siderophores and prove that MVs act as public goods between closely related species.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>33048442</pmid><doi>10.1111/1462-2920.15278</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-9897-6903</orcidid></addata></record> |
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subjects | Antioxidants Bacteria Cargo Deoxyribonucleic acid Dietzia DNA Extracellular Gene transfer Gram-negative bacteria Homology Horizontal transfer Iron Membrane vesicles Membranes Microbiological strains Microorganisms Siderophores Species Vesicles |
title | Membrane vesicles from a Dietzia bacterium containing multiple cargoes and their roles in iron delivery |
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