Novel, active, and uncultured hydrocarbon-degrading microbes in the ocean
Given the vast quantity of oil and gas input to the marine environment annually, hydrocarbon degradation by marine microorganisms is an essential ecosystem service. Linkages between taxonomy and hydrocarbon degradation capabilities are largely based on cultivation studies, leaving a knowledge gap re...
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description | Given the vast quantity of oil and gas input to the marine environment annually, hydrocarbon degradation by marine microorganisms is an essential ecosystem service. Linkages between taxonomy and hydrocarbon degradation capabilities are largely based on cultivation studies, leaving a knowledge gap regarding the intrinsic ability of uncultured marine microbes to degrade hydrocarbons. To address this knowledge gap, metagenomic sequence data from the Deepwater Horizon (DWH) oil spill deep-sea plume was assembled to which metagenomic and metatranscriptomic reads were mapped. Assembly and binning produced new DWH metagenome-assembled genomes that were evaluated along with their close relatives, all of which are from the marine environment (38 total). These analyses revealed globally distributed hydrocarbon-degrading microbes with clade-specific substrate degradation potentials that have not been reported previously. For example, methane oxidation capabilities were identified in all
. Furthermore, all
encoded and expressed genes for non-gaseous
-alkane degradation; however, DWH
encoded alkane hydroxylase, not alkane 1-monooxygenase. All but one previously unrecognized DWH plume member in the SAR324 and UBA11654 have the capacity for aromatic hydrocarbon degradation. In contrast,
were diverse in the hydrocarbon substrates they could degrade. All clades encoded nutrient acquisition strategies and response to cold temperatures, while sensory and acquisition capabilities were clade specific. These novel insights regarding hydrocarbon degradation by uncultured planktonic microbes provides missing data, allowing for better prediction of the fate of oil and gas when hydrocarbons are input to the ocean, leading to a greater understanding of the ecological consequences to the marine environment.IMPORTANCEMicrobial degradation of hydrocarbons is a critically important process promoting ecosystem health, yet much of what is known about this process is based on physiological experiments with a few hydrocarbon substrates and cultured microbes. Thus, the ability to degrade the diversity of hydrocarbons that comprise oil and gas by microbes in the environment, particularly in the ocean, is not well characterized. Therefore, this study aimed to utilize non-cultivation-based 'omics data to explore novel genomes of uncultured marine microbes involved in degradation of oil and gas. Analyses of newly assembled metagenomic data and previously existing genomes from other marine data s |
doi_str_mv | 10.1128/aem.01224-24 |
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. Furthermore, all
encoded and expressed genes for non-gaseous
-alkane degradation; however, DWH
encoded alkane hydroxylase, not alkane 1-monooxygenase. All but one previously unrecognized DWH plume member in the SAR324 and UBA11654 have the capacity for aromatic hydrocarbon degradation. In contrast,
were diverse in the hydrocarbon substrates they could degrade. All clades encoded nutrient acquisition strategies and response to cold temperatures, while sensory and acquisition capabilities were clade specific. These novel insights regarding hydrocarbon degradation by uncultured planktonic microbes provides missing data, allowing for better prediction of the fate of oil and gas when hydrocarbons are input to the ocean, leading to a greater understanding of the ecological consequences to the marine environment.IMPORTANCEMicrobial degradation of hydrocarbons is a critically important process promoting ecosystem health, yet much of what is known about this process is based on physiological experiments with a few hydrocarbon substrates and cultured microbes. Thus, the ability to degrade the diversity of hydrocarbons that comprise oil and gas by microbes in the environment, particularly in the ocean, is not well characterized. Therefore, this study aimed to utilize non-cultivation-based 'omics data to explore novel genomes of uncultured marine microbes involved in degradation of oil and gas. Analyses of newly assembled metagenomic data and previously existing genomes from other marine data sets, with metagenomic and metatranscriptomic read recruitment, revealed globally distributed hydrocarbon-degrading marine microbes with clade-specific substrate degradation potentials that have not been previously reported. This new understanding of oil and gas degradation by uncultured marine microbes suggested that the global ocean harbors a diversity of hydrocarbon-degrading bacteria, which can act as primary agents regulating ecosystem health.</description><identifier>ISSN: 0099-2240</identifier><identifier>ISSN: 1098-5336</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/aem.01224-24</identifier><identifier>PMID: 39177328</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Alkane 1-monooxygenase ; Alkanes ; Aromatic hydrocarbons ; Bacteria - classification ; Bacteria - genetics ; Bacteria - isolation & purification ; Bacteria - metabolism ; Biodegradation ; Biodegradation, Environmental ; Deep sea ; Degradation ; Ecological effects ; Ecosystem services ; Environmental degradation ; Environmental Microbiology ; Hydrocarbon-degrading bacteria ; Hydrocarbons ; Hydrocarbons - metabolism ; Marine ecosystems ; Marine environment ; Marine microorganisms ; Metagenome ; Metagenomics ; Microorganisms ; Missing data ; Oceans and Seas ; Oil spills ; Oils & fats ; Oxidation ; Petroleum Pollution ; Phylogeny ; Seawater - microbiology ; Taxonomy</subject><ispartof>Applied and environmental microbiology, 2024-09, Vol.90 (9), p.e0122424</ispartof><rights>Copyright © 2024 Howe et al.</rights><rights>Copyright American Society for Microbiology Sep 2024</rights><rights>Copyright © 2024 Howe et al. 2024 Howe et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a361t-af739463d498dce68ff5707c49a230bd72077f62132399d4f3d8aa6a9379b21c3</cites><orcidid>0009-0000-4586-0694 ; 0000-0002-3027-4876 ; 0009000045860694 ; 0000000230274876</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.01224-24$$EPDF$$P50$$Gasm2$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/aem.01224-24$$EHTML$$P50$$Gasm2$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,3175,27901,27902,52726,52727,52728,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39177328$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/2434336$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><contributor>Glass, Jennifer B.</contributor><creatorcontrib>Howe, Kathryn L</creatorcontrib><creatorcontrib>Zaugg, Julian</creatorcontrib><creatorcontrib>Mason, Olivia U</creatorcontrib><title>Novel, active, and uncultured hydrocarbon-degrading microbes in the ocean</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><addtitle>Appl Environ Microbiol</addtitle><description>Given the vast quantity of oil and gas input to the marine environment annually, hydrocarbon degradation by marine microorganisms is an essential ecosystem service. Linkages between taxonomy and hydrocarbon degradation capabilities are largely based on cultivation studies, leaving a knowledge gap regarding the intrinsic ability of uncultured marine microbes to degrade hydrocarbons. To address this knowledge gap, metagenomic sequence data from the Deepwater Horizon (DWH) oil spill deep-sea plume was assembled to which metagenomic and metatranscriptomic reads were mapped. Assembly and binning produced new DWH metagenome-assembled genomes that were evaluated along with their close relatives, all of which are from the marine environment (38 total). These analyses revealed globally distributed hydrocarbon-degrading microbes with clade-specific substrate degradation potentials that have not been reported previously. For example, methane oxidation capabilities were identified in all
. Furthermore, all
encoded and expressed genes for non-gaseous
-alkane degradation; however, DWH
encoded alkane hydroxylase, not alkane 1-monooxygenase. All but one previously unrecognized DWH plume member in the SAR324 and UBA11654 have the capacity for aromatic hydrocarbon degradation. In contrast,
were diverse in the hydrocarbon substrates they could degrade. All clades encoded nutrient acquisition strategies and response to cold temperatures, while sensory and acquisition capabilities were clade specific. These novel insights regarding hydrocarbon degradation by uncultured planktonic microbes provides missing data, allowing for better prediction of the fate of oil and gas when hydrocarbons are input to the ocean, leading to a greater understanding of the ecological consequences to the marine environment.IMPORTANCEMicrobial degradation of hydrocarbons is a critically important process promoting ecosystem health, yet much of what is known about this process is based on physiological experiments with a few hydrocarbon substrates and cultured microbes. Thus, the ability to degrade the diversity of hydrocarbons that comprise oil and gas by microbes in the environment, particularly in the ocean, is not well characterized. Therefore, this study aimed to utilize non-cultivation-based 'omics data to explore novel genomes of uncultured marine microbes involved in degradation of oil and gas. Analyses of newly assembled metagenomic data and previously existing genomes from other marine data sets, with metagenomic and metatranscriptomic read recruitment, revealed globally distributed hydrocarbon-degrading marine microbes with clade-specific substrate degradation potentials that have not been previously reported. 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Linkages between taxonomy and hydrocarbon degradation capabilities are largely based on cultivation studies, leaving a knowledge gap regarding the intrinsic ability of uncultured marine microbes to degrade hydrocarbons. To address this knowledge gap, metagenomic sequence data from the Deepwater Horizon (DWH) oil spill deep-sea plume was assembled to which metagenomic and metatranscriptomic reads were mapped. Assembly and binning produced new DWH metagenome-assembled genomes that were evaluated along with their close relatives, all of which are from the marine environment (38 total). These analyses revealed globally distributed hydrocarbon-degrading microbes with clade-specific substrate degradation potentials that have not been reported previously. For example, methane oxidation capabilities were identified in all
. Furthermore, all
encoded and expressed genes for non-gaseous
-alkane degradation; however, DWH
encoded alkane hydroxylase, not alkane 1-monooxygenase. All but one previously unrecognized DWH plume member in the SAR324 and UBA11654 have the capacity for aromatic hydrocarbon degradation. In contrast,
were diverse in the hydrocarbon substrates they could degrade. All clades encoded nutrient acquisition strategies and response to cold temperatures, while sensory and acquisition capabilities were clade specific. These novel insights regarding hydrocarbon degradation by uncultured planktonic microbes provides missing data, allowing for better prediction of the fate of oil and gas when hydrocarbons are input to the ocean, leading to a greater understanding of the ecological consequences to the marine environment.IMPORTANCEMicrobial degradation of hydrocarbons is a critically important process promoting ecosystem health, yet much of what is known about this process is based on physiological experiments with a few hydrocarbon substrates and cultured microbes. Thus, the ability to degrade the diversity of hydrocarbons that comprise oil and gas by microbes in the environment, particularly in the ocean, is not well characterized. Therefore, this study aimed to utilize non-cultivation-based 'omics data to explore novel genomes of uncultured marine microbes involved in degradation of oil and gas. Analyses of newly assembled metagenomic data and previously existing genomes from other marine data sets, with metagenomic and metatranscriptomic read recruitment, revealed globally distributed hydrocarbon-degrading marine microbes with clade-specific substrate degradation potentials that have not been previously reported. This new understanding of oil and gas degradation by uncultured marine microbes suggested that the global ocean harbors a diversity of hydrocarbon-degrading bacteria, which can act as primary agents regulating ecosystem health.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>39177328</pmid><doi>10.1128/aem.01224-24</doi><tpages>22</tpages><orcidid>https://orcid.org/0009-0000-4586-0694</orcidid><orcidid>https://orcid.org/0000-0002-3027-4876</orcidid><orcidid>https://orcid.org/0009000045860694</orcidid><orcidid>https://orcid.org/0000000230274876</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alkane 1-monooxygenase Alkanes Aromatic hydrocarbons Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Bacteria - metabolism Biodegradation Biodegradation, Environmental Deep sea Degradation Ecological effects Ecosystem services Environmental degradation Environmental Microbiology Hydrocarbon-degrading bacteria Hydrocarbons Hydrocarbons - metabolism Marine ecosystems Marine environment Marine microorganisms Metagenome Metagenomics Microorganisms Missing data Oceans and Seas Oil spills Oils & fats Oxidation Petroleum Pollution Phylogeny Seawater - microbiology Taxonomy |
title | Novel, active, and uncultured hydrocarbon-degrading microbes in the ocean |
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