Identification of putative benzene-degrading bacteria in methanogenic enrichment cultures

Sakai, Nobuyuki; Kurisu, Futoshi; Yagi, Osami; Nakajima, Fumiyuki; Yamamoto, Kazuo

doi:10.1016/j.jbiosc.2009.06.005

Cited by 50 publications

(65 citation statements)

References 29 publications

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“…The high abundance of Firmicutes in TOLDC and NAPDC is consistent with recent reports of anaerobic monoaromatic hydrocarbon-degrading cultures that implicate Firmicutes (for example, Peptococcaceae) as primary hydrocarbon degraders (Abu Laban et al, 2009;Winderl et al, 2010;Sun and Cupples, 2012;Fowler et al, 2014) or playing key roles alongside Deltaproteobacteria (Ficker et al, 1999;Ulrich and Edwards, 2003;Sakai et al, 2009). In contrast, members of the Deltaproteobacteria, particularly Syntrophus/Smithella sp., have been implicated in methanogenic alkane degradation, particularly of longer-chain alkanes (Zengler et al, 1999;Gray et al, 2011;Cheng et al, 2013).…”

Section: Community Compositions Of Methanogenic Hydrocarbon-degradingsupporting

confidence: 88%

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

et al. 2015

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Methanogenic hydrocarbon metabolism is a key process in subsurface oil reservoirs and hydrocarbon-contaminated environments and thus warrants greater understanding to improve current technologies for fossil fuel extraction and bioremediation. In this study, three hydrocarbondegrading methanogenic cultures established from two geographically distinct environments and incubated with different hydrocarbon substrates (added as single hydrocarbons or as mixtures) were subjected to metagenomic and 16S rRNA gene pyrosequencing to test whether these differences affect the genetic potential and composition of the communities. Enrichment of different putative hydrocarbon-degrading bacteria in each culture appeared to be substrate dependent, though all cultures contained both acetate-and H 2 -utilizing methanogens. Despite differing hydrocarbon substrates and inoculum sources, all three cultures harbored genes for hydrocarbon activation by fumarate addition (bssA, assA, nmsA) and carboxylation (abcA, ancA), along with those for associated downstream pathways (bbs, bcr, bam), though the cultures incubated with hydrocarbon mixtures contained a broader diversity of fumarate addition genes. A comparative metagenomic analysis of the three cultures showed that they were functionally redundant despite their enrichment backgrounds, sharing multiple features associated with syntrophic hydrocarbon conversion to methane. In addition, a comparative analysis of the culture metagenomes with those of 41 environmental samples (containing varying proportions of methanogens) showed that the three cultures were functionally most similar to each other but distinct from other environments, including hydrocarbon-impacted environments (for example, oil sands tailings ponds and oil-affected marine sediments). This study provides a basis for understanding key functions and environmental selection in methanogenic hydrocarbon-associated communities.

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Section: Community Compositions Of Methanogenic Hydrocarbon-degradingsupporting

confidence: 88%

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

et al. 2015

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“…Benzene biodegrades anaerobically much less readily than other monoaromatic compounds due to the absence of a substituent on the aromatic ring. Nevertheless, the past 2 decades of research have shown that benzene can be metabolized under nitrate-reducing (3,4), sulfate-reducing (5-7), iron-reducing (8)(9)(10), and methanogenic (11,12) conditions. Despite the interest in this process, the benzene-activating mechanism has remained elusive.…”

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confidence: 99%

“…Across enrichment cultures, bacteria from the classes Deltaproteobacteria and Clostridia have been suggested as key microorganisms that activate the benzene ring (5,7,12,(28)(29)(30). In this study, a comparative metatranscriptomic analysis was performed on a benzene-degrading, nitrate-reducing enrichment culture.…”

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confidence: 99%

Metatranscriptome of an Anaerobic Benzene-Degrading, Nitrate-Reducing Enrichment Culture Reveals Involvement of Carboxylation in Benzene Ring Activation

Luo

Gitiafroz

Devine

et al. 2014

Appl Environ Microbiol

106

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The enzymes involved in the initial steps of anaerobic benzene catabolism are not known. To try to elucidate this critical step, a metatranscriptomic analysis was conducted to compare the genes transcribed during the metabolism of benzene and benzoate by an anaerobic benzene-degrading, nitrate-reducing enrichment culture. RNA was extracted from the mixed culture and sequenced without prior mRNA enrichment, allowing simultaneous examination of the active community composition and the differential gene expression between the two treatments. Ribosomal and mRNA sequences attributed to a member of the family Peptococcaceae from the order Clostridiales were essentially only detected in the benzene-amended culture samples, implicating this group in the initial catabolism of benzene. Genes similar to each of two subunits of a proposed benzene-carboxylating enzyme were transcribed when the culture was amended with benzene. Anaerobic benzoate degradation genes from strict anaerobes were transcribed only when the culture was amended with benzene. Genes for other benzoate catabolic enzymes and for nitrate respiration were transcribed in both samples, with those attributed to an Azoarcus species being most abundant. These findings indicate that the mineralization of benzene starts with its activation by a strict anaerobe belonging to the Peptococcaceae, involving a carboxylation step to form benzoate. These data confirm the previously hypothesized syntrophic association between a benzene-degrading Peptococcaceae strain and a benzoate-degrading denitrifying Azoarcus strain for the complete catabolism of benzene with nitrate as the terminal electron acceptor.

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“…Benzene was anaerobically degraded in sediments coupled to the reduction of Fe(III) (4,10,43,44,53), Mn(IV) (61), sulfate (3,20,23,27,34,35,40,64), carbon dioxide (17,65), and graphite electrodes (67). Enrichment cultures capable of anaerobic oxidation of benzene with either sulfate (1,7,18,19,(49)(50)(51), carbon dioxide (26,54,59), or Fe(III) (11,31,37,53) as the electron acceptor have been described. A number of different species appear to be involved in benzene degradation in these enrichment cultures.…”

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confidence: 99%

Anaerobic Oxidation of Benzene by the Hyperthermophilic Archaeon Ferroglobus placidus

Holmes

Risso

Smith

et al. 2011

Appl Environ Microbiol

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Anaerobic benzene oxidation coupled to the reduction of Fe(III) was studied inFerroglobus placidusin order to learn more about how such a stable molecule could be metabolized under strict anaerobic conditions.F. placidusconserved energy to support growth at 85°C in a medium with benzene provided as the sole electron donor and Fe(III) as the sole electron acceptor. The stoichiometry of benzene loss and Fe(III) reduction, as well as the conversion of [14C]benzene to [14C]carbon dioxide, was consistent with complete oxidation of benzene to carbon dioxide with electron transfer to Fe(III). Benzoate, but not phenol or toluene, accumulated at low levels during benzene metabolism, and [14C]benzoate was produced from [14C]benzene. Analysis of gene transcript levels revealed increased expression of genes encoding enzymes for anaerobic benzoate degradation during growth on benzene versus growth on acetate, but genes involved in phenol degradation were not upregulated during growth on benzene. A gene for a putative carboxylase that was more highly expressed in benzene- than in benzoate-grown cells was identified. These results suggest that benzene is carboxylated to benzoate and that phenol is not an important intermediate in the benzene metabolism ofF. placidus. This is the first demonstration of a microorganism in pure culture that can grow on benzene under strict anaerobic conditions and for which there is strong evidence for degradation of benzene via clearly defined anaerobic metabolic pathways. Thus,F. placidusprovides a much-needed pure culture model for further studies on the anaerobic activation of benzene in microorganisms.

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Identification of putative benzene-degrading bacteria in methanogenic enrichment cultures

Cited by 50 publications

References 29 publications

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

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

Metatranscriptome of an Anaerobic Benzene-Degrading, Nitrate-Reducing Enrichment Culture Reveals Involvement of Carboxylation in Benzene Ring Activation

Anaerobic Oxidation of Benzene by the Hyperthermophilic Archaeon Ferroglobus placidus

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