Vadesse L Noundou, Amalie Levy, Shannon Modla, Yanbao Yu, Jing Qu, Thomas E Hanson
{"title":"黄绿杆菌外膜囊泡可能运输生物源单质硫。","authors":"Vadesse L Noundou, Amalie Levy, Shannon Modla, Yanbao Yu, Jing Qu, Thomas E Hanson","doi":"10.1128/aem.01019-25","DOIUrl":null,"url":null,"abstract":"<p><p>Outer membrane-derived vesicles (OMVs) have been studied in different phyla of gram-negative bacteria, most extensively in the Pseudomonadota, where they have been shown to participate in diverse biological and environmental processes. To date, the production of OMVs has not been reported in the Chlorobiaceae within the phylum Chlorobiota. <i>Chlorobaculum tepidum</i> is the model organism for the Chlorobiaceae that synthesizes and consumes insoluble extracellular sulfur (S(0)) globules by an unknown mechanism. Here, we report evidence implicating outer membrane vesicles in biogenic S(0) globule synthesis. We demonstrate that <i>Cba. tepidum</i> secretes OMVs in the extracellular milieu and that OMV concentration and size vary with growth conditions, particularly sulfide concentration. A core of 31 proteins involved in diverse biological processes such as cell wall biogenesis, inorganic ion transport, and metabolism was found to be shared between OMVs, extracellular S(0) globules, and <i>Cba. tepidum</i>-intact cells. Multiple analytical methods indicated that OMVs contain S(0) and that OMVs and biogenic S(0) globules share protein and polysaccharide signatures, including lipooligosaccharides. Together, these lines of evidence indicate that <i>Cba. tepidum</i>'s OMVs are one component of sulfur transport between cells and extracellular sulfur globules.IMPORTANCEAll living cells must exchange material with their environment while maintaining cellular integrity. This is a particular challenge for materials that are not water-soluble; however, many bacteria utilize insoluble materials for energy conservation and as nutrients for growth. Here, we show that <i>Cba. tepidum</i> makes outer membrane vesicles, and these vesicles are likely involved in the exchange of material with extracellular elemental sulfur globules formed and consumed by <i>Cba. tepidum</i> as part of its energy metabolism based on oxidizing reduced sulfur compounds like hydrogen sulfide. These data expand our basic understanding of <i>Cba. tepidum</i>'s metabolism. As elemental sulfur is an industrial by-product with a limited number of uses, the information here may help enable the use of additional sulfur compounds by <i>Cba. tepidum</i> to drive the synthesis of biomass and/or specialty biochemicals from waste elemental sulfur by this autotrophic bacterium.</p>","PeriodicalId":8002,"journal":{"name":"Applied and Environmental Microbiology","volume":" ","pages":"e0101925"},"PeriodicalIF":3.9000,"publicationDate":"2025-06-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"<i>Chlorobaculum tepidum</i> outer membrane vesicles may transport biogenic elemental sulfur.\",\"authors\":\"Vadesse L Noundou, Amalie Levy, Shannon Modla, Yanbao Yu, Jing Qu, Thomas E Hanson\",\"doi\":\"10.1128/aem.01019-25\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Outer membrane-derived vesicles (OMVs) have been studied in different phyla of gram-negative bacteria, most extensively in the Pseudomonadota, where they have been shown to participate in diverse biological and environmental processes. To date, the production of OMVs has not been reported in the Chlorobiaceae within the phylum Chlorobiota. <i>Chlorobaculum tepidum</i> is the model organism for the Chlorobiaceae that synthesizes and consumes insoluble extracellular sulfur (S(0)) globules by an unknown mechanism. Here, we report evidence implicating outer membrane vesicles in biogenic S(0) globule synthesis. We demonstrate that <i>Cba. tepidum</i> secretes OMVs in the extracellular milieu and that OMV concentration and size vary with growth conditions, particularly sulfide concentration. A core of 31 proteins involved in diverse biological processes such as cell wall biogenesis, inorganic ion transport, and metabolism was found to be shared between OMVs, extracellular S(0) globules, and <i>Cba. tepidum</i>-intact cells. Multiple analytical methods indicated that OMVs contain S(0) and that OMVs and biogenic S(0) globules share protein and polysaccharide signatures, including lipooligosaccharides. Together, these lines of evidence indicate that <i>Cba. tepidum</i>'s OMVs are one component of sulfur transport between cells and extracellular sulfur globules.IMPORTANCEAll living cells must exchange material with their environment while maintaining cellular integrity. This is a particular challenge for materials that are not water-soluble; however, many bacteria utilize insoluble materials for energy conservation and as nutrients for growth. Here, we show that <i>Cba. tepidum</i> makes outer membrane vesicles, and these vesicles are likely involved in the exchange of material with extracellular elemental sulfur globules formed and consumed by <i>Cba. tepidum</i> as part of its energy metabolism based on oxidizing reduced sulfur compounds like hydrogen sulfide. These data expand our basic understanding of <i>Cba. tepidum</i>'s metabolism. As elemental sulfur is an industrial by-product with a limited number of uses, the information here may help enable the use of additional sulfur compounds by <i>Cba. tepidum</i> to drive the synthesis of biomass and/or specialty biochemicals from waste elemental sulfur by this autotrophic bacterium.</p>\",\"PeriodicalId\":8002,\"journal\":{\"name\":\"Applied and Environmental Microbiology\",\"volume\":\" \",\"pages\":\"e0101925\"},\"PeriodicalIF\":3.9000,\"publicationDate\":\"2025-06-18\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Applied and Environmental Microbiology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1128/aem.01019-25\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"BIOTECHNOLOGY & APPLIED MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Applied and Environmental Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/aem.01019-25","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
Chlorobaculum tepidum outer membrane vesicles may transport biogenic elemental sulfur.
Outer membrane-derived vesicles (OMVs) have been studied in different phyla of gram-negative bacteria, most extensively in the Pseudomonadota, where they have been shown to participate in diverse biological and environmental processes. To date, the production of OMVs has not been reported in the Chlorobiaceae within the phylum Chlorobiota. Chlorobaculum tepidum is the model organism for the Chlorobiaceae that synthesizes and consumes insoluble extracellular sulfur (S(0)) globules by an unknown mechanism. Here, we report evidence implicating outer membrane vesicles in biogenic S(0) globule synthesis. We demonstrate that Cba. tepidum secretes OMVs in the extracellular milieu and that OMV concentration and size vary with growth conditions, particularly sulfide concentration. A core of 31 proteins involved in diverse biological processes such as cell wall biogenesis, inorganic ion transport, and metabolism was found to be shared between OMVs, extracellular S(0) globules, and Cba. tepidum-intact cells. Multiple analytical methods indicated that OMVs contain S(0) and that OMVs and biogenic S(0) globules share protein and polysaccharide signatures, including lipooligosaccharides. Together, these lines of evidence indicate that Cba. tepidum's OMVs are one component of sulfur transport between cells and extracellular sulfur globules.IMPORTANCEAll living cells must exchange material with their environment while maintaining cellular integrity. This is a particular challenge for materials that are not water-soluble; however, many bacteria utilize insoluble materials for energy conservation and as nutrients for growth. Here, we show that Cba. tepidum makes outer membrane vesicles, and these vesicles are likely involved in the exchange of material with extracellular elemental sulfur globules formed and consumed by Cba. tepidum as part of its energy metabolism based on oxidizing reduced sulfur compounds like hydrogen sulfide. These data expand our basic understanding of Cba. tepidum's metabolism. As elemental sulfur is an industrial by-product with a limited number of uses, the information here may help enable the use of additional sulfur compounds by Cba. tepidum to drive the synthesis of biomass and/or specialty biochemicals from waste elemental sulfur by this autotrophic bacterium.
期刊介绍:
Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.