Surface-active antibiotic production as a multifunctional adaptation for postfire microorganisms
Wildfires affect soils in multiple ways, leading to numerous challenges for colonizing microorganisms. Although it is thought that fire-adapted microorganisms lie at the forefront of postfire ecosystem recovery, the specific strategies that these organisms use to thrive in burned soils remain largel...
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description | Wildfires affect soils in multiple ways, leading to numerous challenges for colonizing microorganisms. Although it is thought that fire-adapted microorganisms lie at the forefront of postfire ecosystem recovery, the specific strategies that these organisms use to thrive in burned soils remain largely unknown. Through bioactivity screening of bacterial isolates from burned soils, we discovered that several Paraburkholderia spp. isolates produced a set of unusual rhamnolipid surfactants with a natural methyl ester modification. These rhamnolipid methyl esters (RLMEs) exhibited enhanced antimicrobial activity against other postfire microbial isolates, including pyrophilous Pyronema fungi and Amycolatopsis bacteria, compared to the typical rhamnolipids made by organisms such as Pseudomonas spp. RLMEs also showed enhanced surfactant properties and facilitated bacterial motility on agar surfaces. In vitro assays further demonstrated that RLMEs improved aqueous solubilization of polycyclic aromatic hydrocarbons, which are potential carbon sources found in char. Identification of the rhamnolipid biosynthesis genes in the postfire isolate, Paraburkholderia kirstenboschensis str. F3, led to the discovery of rhlM, whose gene product is responsible for the unique methylation of rhamnolipid substrates. RhlM is the first characterized bacterial representative of a large class of integral membrane methyltransferases that are widespread in bacteria. These results indicate multiple roles for RLMEs in the postfire lifestyle of Paraburkholderia isolates, including enhanced dispersal, solubilization of potential nutrients, and inhibition of competitors. Our findings shed new light on the chemical adaptations that bacteria employ to navigate, grow, and outcompete other soil community members in postfire environments. |
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Although it is thought that fire-adapted microorganisms lie at the forefront of postfire ecosystem recovery, the specific strategies that these organisms use to thrive in burned soils remain largely unknown. Through bioactivity screening of bacterial isolates from burned soils, we discovered that several Paraburkholderia spp. isolates produced a set of unusual rhamnolipid surfactants with a natural methyl ester modification. These rhamnolipid methyl esters (RLMEs) exhibited enhanced antimicrobial activity against other postfire microbial isolates, including pyrophilous Pyronema fungi and Amycolatopsis bacteria, compared to the typical rhamnolipids made by organisms such as Pseudomonas spp. RLMEs also showed enhanced surfactant properties and facilitated bacterial motility on agar surfaces. In vitro assays further demonstrated that RLMEs improved aqueous solubilization of polycyclic aromatic hydrocarbons, which are potential carbon sources found in char. Identification of the rhamnolipid biosynthesis genes in the postfire isolate, Paraburkholderia kirstenboschensis str. F3, led to the discovery of rhlM, whose gene product is responsible for the unique methylation of rhamnolipid substrates. RhlM is the first characterized bacterial representative of a large class of integral membrane methyltransferases that are widespread in bacteria. These results indicate multiple roles for RLMEs in the postfire lifestyle of Paraburkholderia isolates, including enhanced dispersal, solubilization of potential nutrients, and inhibition of competitors. Our findings shed new light on the chemical adaptations that bacteria employ to navigate, grow, and outcompete other soil community members in postfire environments.</description><identifier>ISSN: 1751-7362</identifier><identifier>ISSN: 1751-7370</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1093/ismejo/wrae022</identifier><identifier>PMID: 38366029</identifier><language>eng</language><publisher>England: Nature Publishing Group</publisher><subject>Adaptation, Physiological ; Anti-Bacterial Agents - metabolism ; Anti-Bacterial Agents - pharmacology ; antibiotics ; Burkholderiales - genetics ; Burkholderiales - metabolism ; Environmental Sciences & Ecology ; fire ; Fires ; Glycolipids - metabolism ; interspecies interactions ; Microbiology ; mortility ; Polycyclic Aromatic Hydrocarbons - metabolism ; Soil Microbiology ; Surface-Active Agents - metabolism ; surfactants</subject><ispartof>The ISME Journal, 2024-01, Vol.18 (1)</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c317t-33845d9af96e5cc81e563c81004b0be83407f23c0361bd420064fa7e581bd9c53</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38366029$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/2345860$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Mira D</creatorcontrib><creatorcontrib>Du, Yongle</creatorcontrib><creatorcontrib>Koupaei, Sara K</creatorcontrib><creatorcontrib>Kim, Nicole R</creatorcontrib><creatorcontrib>Fischer, Monika S</creatorcontrib><creatorcontrib>Zhang, Wenjun</creatorcontrib><creatorcontrib>Traxler, Matthew F</creatorcontrib><creatorcontrib>Univ. of Wisconsin, Madison, WI (United States)</creatorcontrib><creatorcontrib>UT-Battelle LLC/ORNL, Oak Ridge, TN (United States)</creatorcontrib><creatorcontrib>Brookhaven National Laboratory (BNL), Upton, NY (United States)</creatorcontrib><creatorcontrib>Argonne National Laboratory (ANL), Argonne, IL (United States)</creatorcontrib><creatorcontrib>Univ. of California, Oakland, CA (United States)</creatorcontrib><title>Surface-active antibiotic production as a multifunctional adaptation for postfire microorganisms</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><description>Wildfires affect soils in multiple ways, leading to numerous challenges for colonizing microorganisms. Although it is thought that fire-adapted microorganisms lie at the forefront of postfire ecosystem recovery, the specific strategies that these organisms use to thrive in burned soils remain largely unknown. Through bioactivity screening of bacterial isolates from burned soils, we discovered that several Paraburkholderia spp. isolates produced a set of unusual rhamnolipid surfactants with a natural methyl ester modification. These rhamnolipid methyl esters (RLMEs) exhibited enhanced antimicrobial activity against other postfire microbial isolates, including pyrophilous Pyronema fungi and Amycolatopsis bacteria, compared to the typical rhamnolipids made by organisms such as Pseudomonas spp. RLMEs also showed enhanced surfactant properties and facilitated bacterial motility on agar surfaces. In vitro assays further demonstrated that RLMEs improved aqueous solubilization of polycyclic aromatic hydrocarbons, which are potential carbon sources found in char. Identification of the rhamnolipid biosynthesis genes in the postfire isolate, Paraburkholderia kirstenboschensis str. F3, led to the discovery of rhlM, whose gene product is responsible for the unique methylation of rhamnolipid substrates. RhlM is the first characterized bacterial representative of a large class of integral membrane methyltransferases that are widespread in bacteria. These results indicate multiple roles for RLMEs in the postfire lifestyle of Paraburkholderia isolates, including enhanced dispersal, solubilization of potential nutrients, and inhibition of competitors. Our findings shed new light on the chemical adaptations that bacteria employ to navigate, grow, and outcompete other soil community members in postfire environments.</description><subject>Adaptation, Physiological</subject><subject>Anti-Bacterial Agents - metabolism</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>antibiotics</subject><subject>Burkholderiales - genetics</subject><subject>Burkholderiales - metabolism</subject><subject>Environmental Sciences & Ecology</subject><subject>fire</subject><subject>Fires</subject><subject>Glycolipids - metabolism</subject><subject>interspecies interactions</subject><subject>Microbiology</subject><subject>mortility</subject><subject>Polycyclic Aromatic Hydrocarbons - metabolism</subject><subject>Soil Microbiology</subject><subject>Surface-Active Agents - metabolism</subject><subject>surfactants</subject><issn>1751-7362</issn><issn>1751-7370</issn><issn>1751-7370</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9UD1PwzAQtRCIlsLKiCImlrSOHTvJiBBfUiUGYDaOcwZXSRxsB8S_xzSluuHdx7unu4fQeYaXGa7oyvgONnb17SRgQg7QPCtYlha0wIf7nJMZOvF-gzErOC-O0YyWlHNMqjl6ex6dlgpSqYL5gkT2wdTGBqOSwdlmjF3bJ9InMunGNhg99tuWbBPZyCHI7VxblwzWB20cJJ1Rzlr3Lvt4nD9FR1q2Hs52uECvd7cvNw_p-un-8eZ6nSqaFSGltMxZU0ldcWBKlRkwTiNgnNe4hpLmuNCEKkx5Vjc5wZjnWhbAylhWitEFupx04xlGeGUCqA9l-x5UEITmrOQ4kq4mUvztcwQfRGe8graVPdjRC1KRkuSUx1ig5USNz3jvQIvBmU66H5Fh8We9mKwXO-vjwsVOe6w7aPb0f6_pL9J3gyo</recordid><startdate>20240108</startdate><enddate>20240108</enddate><creator>Liu, Mira D</creator><creator>Du, Yongle</creator><creator>Koupaei, Sara K</creator><creator>Kim, Nicole R</creator><creator>Fischer, Monika S</creator><creator>Zhang, Wenjun</creator><creator>Traxler, Matthew F</creator><general>Nature Publishing Group</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>7X8</scope><scope>OTOTI</scope></search><sort><creationdate>20240108</creationdate><title>Surface-active antibiotic production as a multifunctional adaptation for postfire microorganisms</title><author>Liu, Mira D ; Du, Yongle ; Koupaei, Sara K ; Kim, Nicole R ; Fischer, Monika S ; Zhang, Wenjun ; Traxler, Matthew F</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c317t-33845d9af96e5cc81e563c81004b0be83407f23c0361bd420064fa7e581bd9c53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adaptation, Physiological</topic><topic>Anti-Bacterial Agents - metabolism</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>antibiotics</topic><topic>Burkholderiales - genetics</topic><topic>Burkholderiales - metabolism</topic><topic>Environmental Sciences & Ecology</topic><topic>fire</topic><topic>Fires</topic><topic>Glycolipids - metabolism</topic><topic>interspecies interactions</topic><topic>Microbiology</topic><topic>mortility</topic><topic>Polycyclic Aromatic Hydrocarbons - metabolism</topic><topic>Soil Microbiology</topic><topic>Surface-Active Agents - metabolism</topic><topic>surfactants</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Mira D</creatorcontrib><creatorcontrib>Du, Yongle</creatorcontrib><creatorcontrib>Koupaei, Sara K</creatorcontrib><creatorcontrib>Kim, Nicole R</creatorcontrib><creatorcontrib>Fischer, Monika S</creatorcontrib><creatorcontrib>Zhang, Wenjun</creatorcontrib><creatorcontrib>Traxler, Matthew F</creatorcontrib><creatorcontrib>Univ. of Wisconsin, Madison, WI (United States)</creatorcontrib><creatorcontrib>UT-Battelle LLC/ORNL, Oak Ridge, TN (United States)</creatorcontrib><creatorcontrib>Brookhaven National Laboratory (BNL), Upton, NY (United States)</creatorcontrib><creatorcontrib>Argonne National Laboratory (ANL), Argonne, IL (United States)</creatorcontrib><creatorcontrib>Univ. of California, Oakland, CA (United States)</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Mira D</au><au>Du, Yongle</au><au>Koupaei, Sara K</au><au>Kim, Nicole R</au><au>Fischer, Monika S</au><au>Zhang, Wenjun</au><au>Traxler, Matthew F</au><aucorp>Univ. of Wisconsin, Madison, WI (United States)</aucorp><aucorp>UT-Battelle LLC/ORNL, Oak Ridge, TN (United States)</aucorp><aucorp>Brookhaven National Laboratory (BNL), Upton, NY (United States)</aucorp><aucorp>Argonne National Laboratory (ANL), Argonne, IL (United States)</aucorp><aucorp>Univ. of California, Oakland, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Surface-active antibiotic production as a multifunctional adaptation for postfire microorganisms</atitle><jtitle>The ISME Journal</jtitle><addtitle>ISME J</addtitle><date>2024-01-08</date><risdate>2024</risdate><volume>18</volume><issue>1</issue><issn>1751-7362</issn><issn>1751-7370</issn><eissn>1751-7370</eissn><abstract>Wildfires affect soils in multiple ways, leading to numerous challenges for colonizing microorganisms. Although it is thought that fire-adapted microorganisms lie at the forefront of postfire ecosystem recovery, the specific strategies that these organisms use to thrive in burned soils remain largely unknown. Through bioactivity screening of bacterial isolates from burned soils, we discovered that several Paraburkholderia spp. isolates produced a set of unusual rhamnolipid surfactants with a natural methyl ester modification. These rhamnolipid methyl esters (RLMEs) exhibited enhanced antimicrobial activity against other postfire microbial isolates, including pyrophilous Pyronema fungi and Amycolatopsis bacteria, compared to the typical rhamnolipids made by organisms such as Pseudomonas spp. RLMEs also showed enhanced surfactant properties and facilitated bacterial motility on agar surfaces. In vitro assays further demonstrated that RLMEs improved aqueous solubilization of polycyclic aromatic hydrocarbons, which are potential carbon sources found in char. Identification of the rhamnolipid biosynthesis genes in the postfire isolate, Paraburkholderia kirstenboschensis str. F3, led to the discovery of rhlM, whose gene product is responsible for the unique methylation of rhamnolipid substrates. RhlM is the first characterized bacterial representative of a large class of integral membrane methyltransferases that are widespread in bacteria. These results indicate multiple roles for RLMEs in the postfire lifestyle of Paraburkholderia isolates, including enhanced dispersal, solubilization of potential nutrients, and inhibition of competitors. Our findings shed new light on the chemical adaptations that bacteria employ to navigate, grow, and outcompete other soil community members in postfire environments.</abstract><cop>England</cop><pub>Nature Publishing Group</pub><pmid>38366029</pmid><doi>10.1093/ismejo/wrae022</doi><oa>free_for_read</oa></addata></record> |
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subjects | Adaptation, Physiological Anti-Bacterial Agents - metabolism Anti-Bacterial Agents - pharmacology antibiotics Burkholderiales - genetics Burkholderiales - metabolism Environmental Sciences & Ecology fire Fires Glycolipids - metabolism interspecies interactions Microbiology mortility Polycyclic Aromatic Hydrocarbons - metabolism Soil Microbiology Surface-Active Agents - metabolism surfactants |
title | Surface-active antibiotic production as a multifunctional adaptation for postfire microorganisms |
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