Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater
Abstract Background Ubiquitous and diverse marine microorganisms utilise the abundant organosulfur molecule dimethylsulfoniopropionate (DMSP), the main precursor of the climate-active gas dimethylsulfide (DMS), as a source of carbon, sulfur and/or signalling molecules. However, it is currently diffi...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-07-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-022-01304-0 |
| _version_ | 1811222383166488576 |
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| author | Jingli Liu Chun-Xu Xue Jinyan Wang Andrew T. Crombie Ornella Carrión Andrew W. B. Johnston J. Colin Murrell Ji Liu Yanfen Zheng Xiao-Hua Zhang Jonathan D. Todd |
| author_facet | Jingli Liu Chun-Xu Xue Jinyan Wang Andrew T. Crombie Ornella Carrión Andrew W. B. Johnston J. Colin Murrell Ji Liu Yanfen Zheng Xiao-Hua Zhang Jonathan D. Todd |
| author_sort | Jingli Liu |
| collection | DOAJ |
| description | Abstract Background Ubiquitous and diverse marine microorganisms utilise the abundant organosulfur molecule dimethylsulfoniopropionate (DMSP), the main precursor of the climate-active gas dimethylsulfide (DMS), as a source of carbon, sulfur and/or signalling molecules. However, it is currently difficult to discern which microbes actively catabolise DMSP in the environment, why they do so and the pathways used. Results Here, a novel DNA-stable isotope probing (SIP) approach, where only the propionate and not the DMS moiety of DMSP was 13C-labelled, was strategically applied to identify key microorganisms actively using DMSP and also likely DMS as a carbon source, and their catabolic enzymes, in North Sea water. Metagenomic analysis of natural seawater suggested that Rhodobacterales (Roseobacter group) and SAR11 bacteria were the major microorganisms degrading DMSP via demethylation and, to a lesser extent, DddP-driven DMSP lysis pathways. However, neither Rhodobacterales and SAR11 bacteria nor their DMSP catabolic genes were prominently labelled in DNA-SIP experiments, suggesting they use DMSP as a sulfur source and/or in signalling pathways, and not primarily for carbon requirements. Instead, DNA-SIP identified gammaproteobacterial Oceanospirillales, e.g. Amphritea, and their DMSP lyase DddD as the dominant microorganisms/enzymes using DMSP as a carbon source. Supporting this, most gammaproteobacterial (with DddD) but few alphaproteobacterial seawater isolates grew on DMSP as sole carbon source and produced DMS. Furthermore, our DNA-SIP strategy also identified Methylophaga and other Piscirickettsiaceae as key bacteria likely using the DMS, generated from DMSP lysis, as a carbon source. Conclusions This is the first study to use DNA-SIP with 13C-labelled DMSP and, in a novel way, it identifies the dominant microbes utilising DMSP and DMS as carbon sources. It highlights that whilst metagenomic analyses of marine environments can predict microorganisms/genes that degrade DMSP and DMS based on their abundance, it cannot disentangle those using these important organosulfur compounds for their carbon requirements. Note, the most abundant DMSP degraders, e.g. Rhodobacterales with DmdA, are not always the key microorganisms using DMSP for carbon and releasing DMS, which in this coastal system were Oceanospirillales containing DddD. Video abstract. |
| first_indexed | 2024-04-12T08:14:51Z |
| format | Article |
| id | doaj.art-ca419f3c1bd04ed79d256484fdb4ae30 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-04-12T08:14:51Z |
| publishDate | 2022-07-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-ca419f3c1bd04ed79d256484fdb4ae302022-12-22T03:40:50ZengBMCMicrobiome2049-26182022-07-0110112110.1186/s40168-022-01304-0Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawaterJingli Liu0Chun-Xu Xue1Jinyan Wang2Andrew T. Crombie3Ornella Carrión4Andrew W. B. Johnston5J. Colin Murrell6Ji Liu7Yanfen Zheng8Xiao-Hua Zhang9Jonathan D. Todd10Frontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences , Ocean University of ChinaFrontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences , Ocean University of ChinaFrontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences , Ocean University of ChinaSchool of Environmental Sciences, University of East Anglia, Norwich Research ParkSchool of Biological Sciences, University of East Anglia, Norwich Research ParkSchool of Biological Sciences, University of East Anglia, Norwich Research ParkSchool of Environmental Sciences, University of East Anglia, Norwich Research ParkFrontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences , Ocean University of ChinaFrontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences , Ocean University of ChinaFrontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences , Ocean University of ChinaSchool of Biological Sciences, University of East Anglia, Norwich Research ParkAbstract Background Ubiquitous and diverse marine microorganisms utilise the abundant organosulfur molecule dimethylsulfoniopropionate (DMSP), the main precursor of the climate-active gas dimethylsulfide (DMS), as a source of carbon, sulfur and/or signalling molecules. However, it is currently difficult to discern which microbes actively catabolise DMSP in the environment, why they do so and the pathways used. Results Here, a novel DNA-stable isotope probing (SIP) approach, where only the propionate and not the DMS moiety of DMSP was 13C-labelled, was strategically applied to identify key microorganisms actively using DMSP and also likely DMS as a carbon source, and their catabolic enzymes, in North Sea water. Metagenomic analysis of natural seawater suggested that Rhodobacterales (Roseobacter group) and SAR11 bacteria were the major microorganisms degrading DMSP via demethylation and, to a lesser extent, DddP-driven DMSP lysis pathways. However, neither Rhodobacterales and SAR11 bacteria nor their DMSP catabolic genes were prominently labelled in DNA-SIP experiments, suggesting they use DMSP as a sulfur source and/or in signalling pathways, and not primarily for carbon requirements. Instead, DNA-SIP identified gammaproteobacterial Oceanospirillales, e.g. Amphritea, and their DMSP lyase DddD as the dominant microorganisms/enzymes using DMSP as a carbon source. Supporting this, most gammaproteobacterial (with DddD) but few alphaproteobacterial seawater isolates grew on DMSP as sole carbon source and produced DMS. Furthermore, our DNA-SIP strategy also identified Methylophaga and other Piscirickettsiaceae as key bacteria likely using the DMS, generated from DMSP lysis, as a carbon source. Conclusions This is the first study to use DNA-SIP with 13C-labelled DMSP and, in a novel way, it identifies the dominant microbes utilising DMSP and DMS as carbon sources. It highlights that whilst metagenomic analyses of marine environments can predict microorganisms/genes that degrade DMSP and DMS based on their abundance, it cannot disentangle those using these important organosulfur compounds for their carbon requirements. Note, the most abundant DMSP degraders, e.g. Rhodobacterales with DmdA, are not always the key microorganisms using DMSP for carbon and releasing DMS, which in this coastal system were Oceanospirillales containing DddD. Video abstract.https://doi.org/10.1186/s40168-022-01304-0Dimethylsulfoniopropionate (DMSP)Dimethylsulfide (DMS)DNA-stable isotope probing (DNA-SIP)OceanospirillalesDddD DMSP lyaseSeawater |
| spellingShingle | Jingli Liu Chun-Xu Xue Jinyan Wang Andrew T. Crombie Ornella Carrión Andrew W. B. Johnston J. Colin Murrell Ji Liu Yanfen Zheng Xiao-Hua Zhang Jonathan D. Todd Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater Microbiome Dimethylsulfoniopropionate (DMSP) Dimethylsulfide (DMS) DNA-stable isotope probing (DNA-SIP) Oceanospirillales DddD DMSP lyase Seawater |
| title | Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater |
| title_full | Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater |
| title_fullStr | Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater |
| title_full_unstemmed | Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater |
| title_short | Oceanospirillales containing the DMSP lyase DddD are key utilisers of carbon from DMSP in coastal seawater |
| title_sort | oceanospirillales containing the dmsp lyase dddd are key utilisers of carbon from dmsp in coastal seawater |
| topic | Dimethylsulfoniopropionate (DMSP) Dimethylsulfide (DMS) DNA-stable isotope probing (DNA-SIP) Oceanospirillales DddD DMSP lyase Seawater |
| url | https://doi.org/10.1186/s40168-022-01304-0 |
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