Horizontal Gene Transfer of Genes Encoding Copper-Containing Membrane-Bound Monooxygenase (CuMMO) and Soluble Di-iron Monooxygenase (SDIMO) in Ethane- and Propane-Oxidizing Rhodococcus Bacteria
The families of copper-containing membrane-bound monooxygenases (CuMMOs) and soluble di-iron monooxygenases (SDIMOs) are involved not only in methane oxidation but also in short-chain alkane oxidation. Here, we describe sp. strain ZPP, a bacterium able to grow with ethane or propane as the sole carb...
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creator | Zou, Bin Huang, Ying Zhang, Pan-Pan Ding, Xiao-Ming Op den Camp, Huub J M Quan, Zhe-Xue |
description | The families of copper-containing membrane-bound monooxygenases (CuMMOs) and soluble di-iron monooxygenases (SDIMOs) are involved not only in methane oxidation but also in short-chain alkane oxidation. Here, we describe
sp. strain ZPP, a bacterium able to grow with ethane or propane as the sole carbon and energy source, and report on the horizontal gene transfer (HGT) of actinobacterial hydrocarbon monooxygenases (HMOs) of the CuMMO family and the sMMO (soluble methane monooxygenase)-like SDIMO in the genus
. The key function of HMO in strain ZPP for propane oxidation was verified by allylthiourea inhibition. The HMO genes (designated
) and those encoding sMMO-like SDIMO (designated
) are located on a linear megaplasmid (pRZP1) of strain ZPP. Comparative genomic analysis of similar plasmids indicated the mobility of these plasmids within the genus
. The plasmid pRZP1 in strain ZPP could be conjugatively transferred to a recipient Rhodococcus erythropolis strain in a mating experiment and showed similar ethane- and propane-consuming activities. Finally, our findings demonstrate that the horizontal transfer of plasmid-based CuMMO and SDIMO genes confers the ability to use ethane and propane on the recipient.
CuMMOs and SDIMOs initiate the aerobic oxidation of alkanes in bacteria. Here, the supposition that horizontally transferred plasmid-based CuMMO and SDIMO genes confer on the recipient similar abilities to use ethane and propane was proposed and confirmed in
This study is a living example of HGT of CuMMOs and SDIMOs and outlines the plasmid-borne properties responsible for gaseous alkane degradation. Our results indicate that plasmids can support the rapid evolution of enzyme-mediated biogeochemical processes. |
doi_str_mv | 10.1128/AEM.00227-21 |
format | Article |
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sp. strain ZPP, a bacterium able to grow with ethane or propane as the sole carbon and energy source, and report on the horizontal gene transfer (HGT) of actinobacterial hydrocarbon monooxygenases (HMOs) of the CuMMO family and the sMMO (soluble methane monooxygenase)-like SDIMO in the genus
. The key function of HMO in strain ZPP for propane oxidation was verified by allylthiourea inhibition. The HMO genes (designated
) and those encoding sMMO-like SDIMO (designated
) are located on a linear megaplasmid (pRZP1) of strain ZPP. Comparative genomic analysis of similar plasmids indicated the mobility of these plasmids within the genus
. The plasmid pRZP1 in strain ZPP could be conjugatively transferred to a recipient Rhodococcus erythropolis strain in a mating experiment and showed similar ethane- and propane-consuming activities. Finally, our findings demonstrate that the horizontal transfer of plasmid-based CuMMO and SDIMO genes confers the ability to use ethane and propane on the recipient.
CuMMOs and SDIMOs initiate the aerobic oxidation of alkanes in bacteria. Here, the supposition that horizontally transferred plasmid-based CuMMO and SDIMO genes confer on the recipient similar abilities to use ethane and propane was proposed and confirmed in
This study is a living example of HGT of CuMMOs and SDIMOs and outlines the plasmid-borne properties responsible for gaseous alkane degradation. Our results indicate that plasmids can support the rapid evolution of enzyme-mediated biogeochemical processes.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/AEM.00227-21</identifier><identifier>PMID: 33962978</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Bacterial Proteins - genetics ; Environmental Microbiology ; Ethane - metabolism ; Gene Transfer, Horizontal ; Genes, Bacterial ; Mixed Function Oxygenases - genetics ; Oxidation-Reduction ; Plasmids ; Propane - metabolism ; Rhodococcus - genetics ; Rhodococcus - metabolism</subject><ispartof>Applied and environmental microbiology, 2021-06, Vol.87 (14), p.e0022721-e0022721</ispartof><rights>Copyright © 2021 American Society for Microbiology.</rights><rights>Copyright © 2021 American Society for Microbiology. 2021 American Society for Microbiology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a348t-e864079b5ecb308e85b206c9ec306822ec1c2aacc83aeddb88504595b95e9afa3</citedby><cites>FETCH-LOGICAL-a348t-e864079b5ecb308e85b206c9ec306822ec1c2aacc83aeddb88504595b95e9afa3</cites><orcidid>0000-0003-1990-9030 ; 0000-0002-7561-8572</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.asm.org/doi/pdf/10.1128/AEM.00227-21$$EPDF$$P50$$Gasm2$$H</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/AEM.00227-21$$EHTML$$P50$$Gasm2$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,3174,27903,27904,52729,52730,52731,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33962978$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Stams, Alfons J. M</contributor><contributor>Stams, Alfons J. M.</contributor><creatorcontrib>Zou, Bin</creatorcontrib><creatorcontrib>Huang, Ying</creatorcontrib><creatorcontrib>Zhang, Pan-Pan</creatorcontrib><creatorcontrib>Ding, Xiao-Ming</creatorcontrib><creatorcontrib>Op den Camp, Huub J M</creatorcontrib><creatorcontrib>Quan, Zhe-Xue</creatorcontrib><title>Horizontal Gene Transfer of Genes Encoding Copper-Containing Membrane-Bound Monooxygenase (CuMMO) and Soluble Di-iron Monooxygenase (SDIMO) in Ethane- and Propane-Oxidizing Rhodococcus Bacteria</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><addtitle>Appl Environ Microbiol</addtitle><description>The families of copper-containing membrane-bound monooxygenases (CuMMOs) and soluble di-iron monooxygenases (SDIMOs) are involved not only in methane oxidation but also in short-chain alkane oxidation. Here, we describe
sp. strain ZPP, a bacterium able to grow with ethane or propane as the sole carbon and energy source, and report on the horizontal gene transfer (HGT) of actinobacterial hydrocarbon monooxygenases (HMOs) of the CuMMO family and the sMMO (soluble methane monooxygenase)-like SDIMO in the genus
. The key function of HMO in strain ZPP for propane oxidation was verified by allylthiourea inhibition. The HMO genes (designated
) and those encoding sMMO-like SDIMO (designated
) are located on a linear megaplasmid (pRZP1) of strain ZPP. Comparative genomic analysis of similar plasmids indicated the mobility of these plasmids within the genus
. The plasmid pRZP1 in strain ZPP could be conjugatively transferred to a recipient Rhodococcus erythropolis strain in a mating experiment and showed similar ethane- and propane-consuming activities. Finally, our findings demonstrate that the horizontal transfer of plasmid-based CuMMO and SDIMO genes confers the ability to use ethane and propane on the recipient.
CuMMOs and SDIMOs initiate the aerobic oxidation of alkanes in bacteria. Here, the supposition that horizontally transferred plasmid-based CuMMO and SDIMO genes confer on the recipient similar abilities to use ethane and propane was proposed and confirmed in
This study is a living example of HGT of CuMMOs and SDIMOs and outlines the plasmid-borne properties responsible for gaseous alkane degradation. Our results indicate that plasmids can support the rapid evolution of enzyme-mediated biogeochemical processes.</description><subject>Bacterial Proteins - genetics</subject><subject>Environmental Microbiology</subject><subject>Ethane - metabolism</subject><subject>Gene Transfer, Horizontal</subject><subject>Genes, Bacterial</subject><subject>Mixed Function Oxygenases - genetics</subject><subject>Oxidation-Reduction</subject><subject>Plasmids</subject><subject>Propane - metabolism</subject><subject>Rhodococcus - genetics</subject><subject>Rhodococcus - metabolism</subject><issn>0099-2240</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1ksFO3DAQhqOqVVlobz1XPoLUUMdOsvalEoQtIBFtVejZcpzJrlHWE-ykAt6ON2uyS1FbqaeRZ775RzO_o-hDQo-ThInPJ4vymFLG5jFLXkWzhEoRZ5znr6MZpVLGjKV0L9oP4ZZSmtJcvI32OJc5k3Mxi54u0NtHdL1uyTk4IDdeu9CAJ9hsE4EsnMHauhUpsOvAx8VEWzdlSthUIw_xKQ6uJiU6xPuHFTgdgBwWQ1kuj4geK9fYDlUL5MzG1qP7l7w-u5xI68iiX09626ZvHrvpsby3tX2c5n1fY40GjRkCOdWmB2_1u-hNo9sA75_jQfTj6-KmuIivlueXxclVrHkq-hhEntK5rDIwFacCRFYxmhsJho83YQxMYpjWxgiuoa4rITKaZjKrZAZSN5ofRF92ut1QbaA24HqvW9V5u9H-QaG26u-Ks2u1wp9KMJ6kKRsFDp8FPN4NEHq1scFA24474hAUy1jKc5rIfEQ_7VDjMQQPzcuYhKrJdTW6rrauK5aM-NEO12HD1C0O3o2X-B_78c81XoR_fwn-C5rkuB4</recordid><startdate>20210625</startdate><enddate>20210625</enddate><creator>Zou, Bin</creator><creator>Huang, Ying</creator><creator>Zhang, Pan-Pan</creator><creator>Ding, Xiao-Ming</creator><creator>Op den Camp, Huub J M</creator><creator>Quan, Zhe-Xue</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-1990-9030</orcidid><orcidid>https://orcid.org/0000-0002-7561-8572</orcidid></search><sort><creationdate>20210625</creationdate><title>Horizontal Gene Transfer of Genes Encoding Copper-Containing Membrane-Bound Monooxygenase (CuMMO) and Soluble Di-iron Monooxygenase (SDIMO) in Ethane- and Propane-Oxidizing Rhodococcus Bacteria</title><author>Zou, Bin ; Huang, Ying ; Zhang, Pan-Pan ; Ding, Xiao-Ming ; Op den Camp, Huub J M ; Quan, Zhe-Xue</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a348t-e864079b5ecb308e85b206c9ec306822ec1c2aacc83aeddb88504595b95e9afa3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Bacterial Proteins - genetics</topic><topic>Environmental Microbiology</topic><topic>Ethane - metabolism</topic><topic>Gene Transfer, Horizontal</topic><topic>Genes, Bacterial</topic><topic>Mixed Function Oxygenases - genetics</topic><topic>Oxidation-Reduction</topic><topic>Plasmids</topic><topic>Propane - metabolism</topic><topic>Rhodococcus - genetics</topic><topic>Rhodococcus - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zou, Bin</creatorcontrib><creatorcontrib>Huang, Ying</creatorcontrib><creatorcontrib>Zhang, Pan-Pan</creatorcontrib><creatorcontrib>Ding, Xiao-Ming</creatorcontrib><creatorcontrib>Op den Camp, Huub J M</creatorcontrib><creatorcontrib>Quan, Zhe-Xue</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>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>Zou, Bin</au><au>Huang, Ying</au><au>Zhang, Pan-Pan</au><au>Ding, Xiao-Ming</au><au>Op den Camp, Huub J M</au><au>Quan, Zhe-Xue</au><au>Stams, Alfons J. M</au><au>Stams, Alfons J. M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Horizontal Gene Transfer of Genes Encoding Copper-Containing Membrane-Bound Monooxygenase (CuMMO) and Soluble Di-iron Monooxygenase (SDIMO) in Ethane- and Propane-Oxidizing Rhodococcus Bacteria</atitle><jtitle>Applied and environmental microbiology</jtitle><stitle>Appl Environ Microbiol</stitle><addtitle>Appl Environ Microbiol</addtitle><date>2021-06-25</date><risdate>2021</risdate><volume>87</volume><issue>14</issue><spage>e0022721</spage><epage>e0022721</epage><pages>e0022721-e0022721</pages><issn>0099-2240</issn><eissn>1098-5336</eissn><abstract>The families of copper-containing membrane-bound monooxygenases (CuMMOs) and soluble di-iron monooxygenases (SDIMOs) are involved not only in methane oxidation but also in short-chain alkane oxidation. Here, we describe
sp. strain ZPP, a bacterium able to grow with ethane or propane as the sole carbon and energy source, and report on the horizontal gene transfer (HGT) of actinobacterial hydrocarbon monooxygenases (HMOs) of the CuMMO family and the sMMO (soluble methane monooxygenase)-like SDIMO in the genus
. The key function of HMO in strain ZPP for propane oxidation was verified by allylthiourea inhibition. The HMO genes (designated
) and those encoding sMMO-like SDIMO (designated
) are located on a linear megaplasmid (pRZP1) of strain ZPP. Comparative genomic analysis of similar plasmids indicated the mobility of these plasmids within the genus
. The plasmid pRZP1 in strain ZPP could be conjugatively transferred to a recipient Rhodococcus erythropolis strain in a mating experiment and showed similar ethane- and propane-consuming activities. Finally, our findings demonstrate that the horizontal transfer of plasmid-based CuMMO and SDIMO genes confers the ability to use ethane and propane on the recipient.
CuMMOs and SDIMOs initiate the aerobic oxidation of alkanes in bacteria. Here, the supposition that horizontally transferred plasmid-based CuMMO and SDIMO genes confer on the recipient similar abilities to use ethane and propane was proposed and confirmed in
This study is a living example of HGT of CuMMOs and SDIMOs and outlines the plasmid-borne properties responsible for gaseous alkane degradation. Our results indicate that plasmids can support the rapid evolution of enzyme-mediated biogeochemical processes.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>33962978</pmid><doi>10.1128/AEM.00227-21</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0003-1990-9030</orcidid><orcidid>https://orcid.org/0000-0002-7561-8572</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacterial Proteins - genetics Environmental Microbiology Ethane - metabolism Gene Transfer, Horizontal Genes, Bacterial Mixed Function Oxygenases - genetics Oxidation-Reduction Plasmids Propane - metabolism Rhodococcus - genetics Rhodococcus - metabolism |
title | Horizontal Gene Transfer of Genes Encoding Copper-Containing Membrane-Bound Monooxygenase (CuMMO) and Soluble Di-iron Monooxygenase (SDIMO) in Ethane- and Propane-Oxidizing Rhodococcus Bacteria |
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