Chemical Profiling Provides Insights into the Metabolic Machinery of Hydrocarbon-Degrading Deep-Sea Microbes

ABSTRACT Marine microbes are known to degrade hydrocarbons; however, microbes inhabiting deep-sea sediments remain largely unexplored. Previous studies into the classical pathways of marine microbial metabolism reveal diverse chemistries; however, metabolic profiling of marine microbes cultured with...

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Autores principales: Aldo Moreno-Ulloa, Victoria Sicairos Diaz, Javier A. Tejeda-Mora, Marla I. Macias Contreras, Fernando Díaz Castillo, Abraham Guerrero, Ricardo Gonzalez Sanchez, Omar Mendoza-Porras, Rafael Vazquez Duhalt, Alexei Licea-Navarro
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:ea0ed0dc6a8646d18ecb3ae5e4952c472021-12-02T18:15:46ZChemical Profiling Provides Insights into the Metabolic Machinery of Hydrocarbon-Degrading Deep-Sea Microbes10.1128/mSystems.00824-202379-5077https://doaj.org/article/ea0ed0dc6a8646d18ecb3ae5e4952c472020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00824-20https://doaj.org/toc/2379-5077ABSTRACT Marine microbes are known to degrade hydrocarbons; however, microbes inhabiting deep-sea sediments remain largely unexplored. Previous studies into the classical pathways of marine microbial metabolism reveal diverse chemistries; however, metabolic profiling of marine microbes cultured with hydrocarbons is limited. In this study, taxonomic (amplicon sequencing) profiles of two environmental deep-sea sediments (>1,200 m deep) were obtained, along with taxonomic and metabolomic (mass spectrometry-based metabolomics) profiles of microbes harbored in deep-sea sediments cultured with hydrocarbons as the sole energy source. Samples were collected from the Gulf of México (GM) and cultured for 28 days using simple (toluene, benzene, hexadecane, and naphthalene) and complex (petroleum API 40) hydrocarbon mixtures as the sole energy sources. The sediment samples harbored diverse microbial communities predominantly classified into Woeseiaceae and Kiloniellaceae families, whereas Pseudomonadaceae and Enterobacteriaceae families prevailed after sediments were cultured with hydrocarbons. Chemical profiling of microbial metabolomes revealed diverse chemical groups belonging primarily to the lipids and lipid-like molecules superclass, as well as the organoheterocyclic compound superclass (ClassyFire annotation). Metabolomic data and prediction of functional profiles indicated an increase in aromatic and alkane degradation in samples cultured with hydrocarbons. Previously unreported metabolites, identified as intermediates in the degradation of hydrocarbons, were annotated as hydroxylated polyunsaturated fatty acids and carboxylated benzene derivatives. In summary, this study used mass spectrometry-based metabolomics coupled to chemoinformatics to demonstrate how microbes from deep-sea sediments could be cultured in the presence of hydrocarbons. This study also highlights how this experimental approach can be used to increase the understanding of hydrocarbon degradation by deep-sea sediment microbes. IMPORTANCE High-throughput technologies and emerging informatics tools have significantly advanced knowledge of hydrocarbon metabolism by marine microbes. However, research into microbes inhabiting deep-sea sediments (>1,000 m) is limited compared to those found in shallow waters. In this study, a nontargeted and nonclassical approach was used to examine the diversity of bacterial taxa and the metabolic profiles of hydrocarbon-degrading deep-sea microbes. In conclusion, this study used metabolomics and chemoinformatics to demonstrate that microbes from deep-sea sediment origin thrive in the presence of toxic and difficult-to-metabolize hydrocarbons. Notably, this study provides evidence of previously unreported metabolites and the global chemical repertoire associated with the metabolism of hydrocarbons by deep-sea microbes.Aldo Moreno-UlloaVictoria Sicairos DiazJavier A. Tejeda-MoraMarla I. Macias ContrerasFernando Díaz CastilloAbraham GuerreroRicardo Gonzalez SanchezOmar Mendoza-PorrasRafael Vazquez DuhaltAlexei Licea-NavarroAmerican Society for Microbiologyarticle16S rRNAdeep-sea microbeshydrocarbon degradationmarine bacteriamass spectrometrymetabolomicsMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution DOAJ
collection DOAJ
language EN
topic 16S rRNA
deep-sea microbes
hydrocarbon degradation
marine bacteria
mass spectrometry
metabolomics
Microbiology
QR1-502
spellingShingle 16S rRNA
deep-sea microbes
hydrocarbon degradation
marine bacteria
mass spectrometry
metabolomics
Microbiology
QR1-502
Aldo Moreno-Ulloa
Victoria Sicairos Diaz
Javier A. Tejeda-Mora
Marla I. Macias Contreras
Fernando Díaz Castillo
Abraham Guerrero
Ricardo Gonzalez Sanchez
Omar Mendoza-Porras
Rafael Vazquez Duhalt
Alexei Licea-Navarro
Chemical Profiling Provides Insights into the Metabolic Machinery of Hydrocarbon-Degrading Deep-Sea Microbes
description ABSTRACT Marine microbes are known to degrade hydrocarbons; however, microbes inhabiting deep-sea sediments remain largely unexplored. Previous studies into the classical pathways of marine microbial metabolism reveal diverse chemistries; however, metabolic profiling of marine microbes cultured with hydrocarbons is limited. In this study, taxonomic (amplicon sequencing) profiles of two environmental deep-sea sediments (>1,200 m deep) were obtained, along with taxonomic and metabolomic (mass spectrometry-based metabolomics) profiles of microbes harbored in deep-sea sediments cultured with hydrocarbons as the sole energy source. Samples were collected from the Gulf of México (GM) and cultured for 28 days using simple (toluene, benzene, hexadecane, and naphthalene) and complex (petroleum API 40) hydrocarbon mixtures as the sole energy sources. The sediment samples harbored diverse microbial communities predominantly classified into Woeseiaceae and Kiloniellaceae families, whereas Pseudomonadaceae and Enterobacteriaceae families prevailed after sediments were cultured with hydrocarbons. Chemical profiling of microbial metabolomes revealed diverse chemical groups belonging primarily to the lipids and lipid-like molecules superclass, as well as the organoheterocyclic compound superclass (ClassyFire annotation). Metabolomic data and prediction of functional profiles indicated an increase in aromatic and alkane degradation in samples cultured with hydrocarbons. Previously unreported metabolites, identified as intermediates in the degradation of hydrocarbons, were annotated as hydroxylated polyunsaturated fatty acids and carboxylated benzene derivatives. In summary, this study used mass spectrometry-based metabolomics coupled to chemoinformatics to demonstrate how microbes from deep-sea sediments could be cultured in the presence of hydrocarbons. This study also highlights how this experimental approach can be used to increase the understanding of hydrocarbon degradation by deep-sea sediment microbes. IMPORTANCE High-throughput technologies and emerging informatics tools have significantly advanced knowledge of hydrocarbon metabolism by marine microbes. However, research into microbes inhabiting deep-sea sediments (>1,000 m) is limited compared to those found in shallow waters. In this study, a nontargeted and nonclassical approach was used to examine the diversity of bacterial taxa and the metabolic profiles of hydrocarbon-degrading deep-sea microbes. In conclusion, this study used metabolomics and chemoinformatics to demonstrate that microbes from deep-sea sediment origin thrive in the presence of toxic and difficult-to-metabolize hydrocarbons. Notably, this study provides evidence of previously unreported metabolites and the global chemical repertoire associated with the metabolism of hydrocarbons by deep-sea microbes.
format article
author Aldo Moreno-Ulloa
Victoria Sicairos Diaz
Javier A. Tejeda-Mora
Marla I. Macias Contreras
Fernando Díaz Castillo
Abraham Guerrero
Ricardo Gonzalez Sanchez
Omar Mendoza-Porras
Rafael Vazquez Duhalt
Alexei Licea-Navarro
author_facet Aldo Moreno-Ulloa
Victoria Sicairos Diaz
Javier A. Tejeda-Mora
Marla I. Macias Contreras
Fernando Díaz Castillo
Abraham Guerrero
Ricardo Gonzalez Sanchez
Omar Mendoza-Porras
Rafael Vazquez Duhalt
Alexei Licea-Navarro
author_sort Aldo Moreno-Ulloa
title Chemical Profiling Provides Insights into the Metabolic Machinery of Hydrocarbon-Degrading Deep-Sea Microbes
title_short Chemical Profiling Provides Insights into the Metabolic Machinery of Hydrocarbon-Degrading Deep-Sea Microbes
title_full Chemical Profiling Provides Insights into the Metabolic Machinery of Hydrocarbon-Degrading Deep-Sea Microbes
title_fullStr Chemical Profiling Provides Insights into the Metabolic Machinery of Hydrocarbon-Degrading Deep-Sea Microbes
title_full_unstemmed Chemical Profiling Provides Insights into the Metabolic Machinery of Hydrocarbon-Degrading Deep-Sea Microbes
title_sort chemical profiling provides insights into the metabolic machinery of hydrocarbon-degrading deep-sea microbes
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/ea0ed0dc6a8646d18ecb3ae5e4952c47
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