Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples

Tan, BoonFei; Fowler, Jane; Laban, Nidal Abu; Dong, Xiaoli; Sensen, Christoph Wilhelm; Foght, Julia M.; Gieg, Lisa M.

doi:10.1038/ismej.2015.22

Cited by 94 publications

(82 citation statements)

References 88 publications

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“…Although the application of the latter has not been reported to date for an anoxic, aromatic compoundcontaminated aquifer, respective reports for other hydrocarbon-impacted systems are available Kimes et al, 2013;Luo et al, 2014;Tan et al, 2015]. Such non-target, non-PCR amplification-based sequencing approaches have the potential to further enhance our perspective of anaerobic hydrocarbon degrader microbiomes.…”

Section: Discussionmentioning

confidence: 99%

Functional Gene Markers for Fumarate-Adding and Dearomatizing Key Enzymes in Anaerobic Aromatic Hydrocarbon Degradation in Terrestrial Environments

et al. 2016

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Anaerobic degradation is a key process in many environments either naturally or anthropogenically exposed to petroleum hydrocarbons. Considerable advances into the biochemistry and physiology of selected anaerobic degraders have been achieved over the last decades, especially for the degradation of aromatic hydrocarbons. However, researchers have only recently begun to explore the ecology of complex anaerobic hydrocarbon degrader communities directly in their natural habitats, as well as in complex laboratory systems using tools of molecular biology. These approaches have mainly been facilitated by the establishment of a suite of targeted marker gene assays, allowing for rapid and directed insights into the diversity as well as the identity of intrinsic degrader populations and degradation potentials established at hydrocarbon-impacted sites. These are based on genes encoding either peripheral or central key enzymes in aromatic compound breakdown, such as fumarate-adding benzylsuccinate synthases or dearomatizing aryl-coenzyme A reductases, or on aromatic ring-cleaving hydrolases. Here, we review recent advances in this field, explain the different detection methodologies applied, and discuss how the detection of site-specific catabolic gene markers has improved the understanding of processes at contaminated sites. Functional marker gene-based strategies may be vital for the development of a more elaborate population-based assessment and prediction of aromatic degradation potentials in hydrocarbon-impacted environments.

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Section: Discussionmentioning

confidence: 99%

Functional Gene Markers for Fumarate-Adding and Dearomatizing Key Enzymes in Anaerobic Aromatic Hydrocarbon Degradation in Terrestrial Environments

et al. 2016

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“…This was subsequently disputed by Tan et al [2014], who came to the opposite conclusion based on reanalysis of the Smithella draft genome and metatranscriptomes. In a couple of metagenomic studies, these authors provided evidence that methanogenic communities originating from oil sands tailings ponds and gas condensate-contaminated aquifer sediments harbor fermentative syntrophs and sulfate reducers capable of degrading n -, iso-and cycloalkanes via their addition to fumarate [Tan et al, 2013[Tan et al, , 2015a. The tentative identification of substituted succinates deriving from C 6 , C 7 and C 8 isoalkanes and methylcyclopentane formed under methanogenic conditions appears to further support these conclusions [Abu Laban et al, 2014;Tan et al, 2015b].…”

Section: Insights From Genomic and Proteomic Studiesmentioning

confidence: 50%

Metabolism of Hydrocarbons in <b><i>n</i></b>-Alkane-Utilizing Anaerobic Bacteria

Wilkes

Buckel

Golding³

et al. 2016

Microb Physiol

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The glycyl radical enzyme-catalyzed addition of n-alkanes to fumarate creates a C-C-bond between two concomitantly formed stereogenic carbon centers. The configurations of the two diastereoisomers of the product resulting from n-hexane activation by the n-alkane-utilizing denitrifying bacterium strain HxN1, i.e. (1-methylpentyl)succinate, were assigned as (2S,1′R) and (2R,1′R). Experiments with stereospecifically deuterated n-(2,5-²H₂)hexanes revealed that exclusively the pro-S hydrogen atom is abstracted from C2 of the n-alkane by the enzyme and later transferred back to C3 of the alkylsuccinate formed. These results indicate that the alkylsuccinate-forming reaction proceeds with an inversion of configuration at the carbon atom (C2) of the n-alkane forming the new C-C-bond, and thus stereochemically resembles a S_N2-type reaction. Therefore, the reaction may occur in a concerted manner, which may avoid the highly energetic hex-2-yl radical as an intermediate. The reaction is associated with a significant primary kinetic isotope effect (kH/kD ≥3) for hydrogen, indicating that the homolytic C-H-bond cleavage is involved in the first irreversible step of the reaction mechanism. The (1-methylalkyl)succinate synthases of n-alkane-utilizing anaerobic bacteria apparently have very broad substrate ranges enabling them to activate not only aliphatic but also alkyl-aromatic hydrocarbons. Thus, two denitrifiers and one sulfate reducer were shown to convert the nongrowth substrate toluene to benzylsuccinate and further to the dead-end product benzoyl-CoA. For this purpose, however, the modified β-oxidation pathway known from alkylbenzene-utilizing bacteria was not employed, but rather the pathway used for n-alkane degradation involving CoA ligation, carbon skeleton rearrangement and decarboxylation. Furthermore, various n-alkane- and alkylbenzene-utilizing denitrifiers and sulfate reducers were found to be capable of forming benzyl alcohols from diverse alkylbenzenes, putatively via dehydrogenases. The thermophilic sulfate reducer strain TD3 forms n-alkylsuccinates during growth with n-alkanes or crude oil, which, based on the observed patterns of homologs, do not derive from a terminal activation of n-alkanes.

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“…The ARHDs are present in environmental microbial communities and play a crucial role in the aromatic compound degradation (including phenol, naphthalene, phenanthrene, pyrene, benzopyrene, among others), especially in oil‐contaminated sediments or soils (Lu et al., ; Mrozik & Piotrowska‐Seget, ; Olajire & Essien, ; Seo, Keum, & Li, ). The contaminated environments exert a strong selective pressure on the microbial community, altering its taxonomic composition and defining its ARHDs gene diversity (Gutierrez et al., ; Liang et al., ; Tan et al., ). The description of the structural and functional diversity of ARHD genes has been important in the establishment of genetic markers for contaminated environments followed by new insights for bioremediation processes (Gutierrez et al., ; Liang et al., ; Tan et al., ).…”

Section: Introductionmentioning

confidence: 99%

“…The contaminated environments exert a strong selective pressure on the microbial community, altering its taxonomic composition and defining its ARHDs gene diversity (Gutierrez et al., ; Liang et al., ; Tan et al., ). The description of the structural and functional diversity of ARHD genes has been important in the establishment of genetic markers for contaminated environments followed by new insights for bioremediation processes (Gutierrez et al., ; Liang et al., ; Tan et al., ).…”

Section: Introductionmentioning

confidence: 99%

Diversity of aromatic hydroxylating dioxygenase genes in mangrove microbiome and their biogeographic patterns across global sites

et al. 2017

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Aromatic hydrocarbons (AH), such as polycyclic aromatic hydrocarbons, are compounds largely found in nature. Aromatic‐ring‐hydroxylating dioxygenases (ARHD) are proteins involved in AH degradation pathways. We used ARHD functional genes from an oil‐impacted mangrove area and compared their diversity with other sites around the world to understand the ARHD biogeographic distribution patterns. For this, a comprehensive database was established with 166 operational protein families (OPFs) from 1,758 gene sequences obtained from 15 different sites worldwide, of which twelve are already published studies and three are unpublished. Based on a deduced ARHD peptide sequences consensus phylogeny, we examined trends and divergences in the sequence phylogenetic clustering from the different sites. The taxonomic affiliation of the OPF revealed that Pseudomonas, Streptomyces, Variovorax, Bordetella and Rhodococcus were the five most abundant genera, considering all sites. The functional diversity analysis showed the enzymatic prevalence of benzene 1,2‐dioxygenase, 3‐phenylpropionate dioxygenase and naphthalene 1,2‐dioxygenase, in addition to 10.98% of undefined category ARHDs. The ARHD gene correlation analysis among different sites was essentially important to gain insights on spatial distribution patterns, genetic congruence and ecological coherence of the bacterial groups found. This work revealed the genetic potential from the mangrove sediment for AH biodegradation and a considerable evolutionary proximity among the dioxygenase OPFs found in Antarctica and South America sites, in addition to high level of endemism in each continental region.

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Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples

Cited by 94 publications

References 88 publications

Functional Gene Markers for Fumarate-Adding and Dearomatizing Key Enzymes in Anaerobic Aromatic Hydrocarbon Degradation in Terrestrial Environments

Functional Gene Markers for Fumarate-Adding and Dearomatizing Key Enzymes in Anaerobic Aromatic Hydrocarbon Degradation in Terrestrial Environments

Metabolism of Hydrocarbons in <b><i>n</i></b>-Alkane-Utilizing Anaerobic Bacteria

Diversity of aromatic hydroxylating dioxygenase genes in mangrove microbiome and their biogeographic patterns across global sites

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