Organohalide-respiring <i>Desulfoluna</i> species isolated from marine environments

Peng, Peng; Goris, Tobias; Lu, Yue; Nijsse, Bart; Burrichter, Anna; Schleheck, David; Koehorst, Jasper J.; Liu, Jie; Sipkema, Detmer; Damsté, Jaap S Sinninghe; Stams, Alfons Johannes Maria; Häggblom, Max M.; Smidt, Hauke; Atashgahi, Siavash

doi:10.1038/s41396-019-0573-y

Cited by 27 publications

(32 citation statements)

References 81 publications

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“…The resulting genome of strain G5G6 consisted of two contigs: a long contig of 3 465 762 bp and a short contig of 36 233 bp (accession number ERZ1938153). Proteomic analysis was done from triplicate cultures grown on toluene (0.4 mM) and nitrate (5 mM) or toluene (0.4 mM) and Fe(III) citrate (20 mM) using procedures described previously (Peng et al ., 2020 ). All cultures had been adapted to the respective growth condition by at least three previous transfers (5% v/v) to fresh media, and three spikes of toluene (0.4 mM at each spike) during each transfer.…”

Section: Resultsmentioning

confidence: 99%

Proteogenomic analysis of Georgfuchsia toluolica revealed unexpected concurrent aerobic and anaerobic toluene degradation

Atashgahi

Oosterkamp

Peng

et al. 2021

Environ Microbiol Rep

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Denitrifying Betaproteobacteria play a key role in the anaerobic degradation of monoaromatic hydrocarbons. We performed a multi-omics study to better understand the metabolism of the representative organism Georgfuchsia toluolica strain G5G6 known as a strict anaerobe coupling toluene oxidation with dissimilatory nitrate and Fe(III) reduction. Despite the genomic potential for degradation of different carbon sources, we did not find sugar or organic acid transporters, in line with the inability of strain G5G6 to use these substrates. Using a proteomics analysis, we detected proteins of fumarate-dependent toluene activation, membrane-bound nitrate reductase, and key components of the metal-reducing (Mtr) pathway under both nitrate-and Fe(III)-reducing conditions. High abundance of the multiheme cytochrome MtrC implied that a porin-cytochrome complex was used for respiratory Fe(III) reduction. Remarkably, strain G5G6 contains a full set of genes for aerobic toluene degradation, and we detected enzymes of aerobic toluene degradation under both nitrate-and Fe(III)reducing conditions. We further detected an ATPdependent benzoyl-CoA reductase, reactive oxygen species detoxification proteins, and cytochrome c oxidase indicating a facultative anaerobic lifestyle of strain G5G6. Correspondingly, we found diffusion through the septa a substantial source of oxygen in the cultures enabling concurrent aerobic and anaerobic toluene degradation by strain G5G6.

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Section: Resultsmentioning

confidence: 99%

Proteogenomic analysis of Georgfuchsia toluolica revealed unexpected concurrent aerobic and anaerobic toluene degradation

Atashgahi

Oosterkamp

Peng

et al. 2021

Environ Microbiol Rep

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“…Focusing exclusively on OHRB belonging to the Firmicutes, proteomic analyses of Rdh proteins were reported in twelve studies (Prat et al, 2011 ; Rupakula et al, 2013 , 2015 ; Tang and Edwards, 2013 ; Kruse et al, 2015 ; Jugder et al, 2016 ; Alfán-Guzmán et al, 2017 ; Kleindienst et al, 2019 ; Liu et al, 2019 ; Low et al, 2019 ; Peng et al, 2020 ; Chen et al, 2021 ). The different methodologies that were applied in those studies (1 or 2D native or denaturing gels, and in-solution LC-MS/MS analyses) render their comparison very difficult.…”

Section: Discussionmentioning

confidence: 99%

“…The analysis of cell-free extracts revealed an apparent stoichiometry of PceA to PceB of 2:1 or 3:1, while PceC and PceT were less abundant. It was especially pronounced for PceC, which is in agreement with recent studies on the rdhABC gene cluster of Desulfoluna sp., where the C subunit was not detected at all (Liu et al, 2019 ; Peng et al, 2020 ). In the soluble fraction, a 1:1 ratio between PceA and PceT suggests that most of the PceA that is not yet associated with the membrane is likely accompanied by PceT, giving additional evidence of the role of PceT as a molecular chaperone specifically dedicated to the maturation of PceA (Morita et al, 2009 ; Maillard et al, 2011 ).…”

Section: Discussionmentioning

confidence: 99%

Stoichiometry of the Gene Products From the Tetrachloroethene Reductive Dehalogenase Operon pceABCT

et al. 2022

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Organohalide respiration (OHR) is a bacterial anaerobic process that uses halogenated compounds, e.g., tetrachloroethene (PCE), as terminal electron acceptors. Our model organisms are Dehalobacter restrictus strain PER-K23, an obligate OHR bacterium (OHRB), and Desulfitobacterium hafniense strain TCE1, a bacterium with a versatile metabolism. The key enzyme is the PCE reductive dehalogenase (PceA) that is encoded in the highly conserved gene cluster (pceABCT) in both above-mentioned strains, and in other Firmicutes OHRB. To date, the functions of PceA and PceT, a dedicated molecular chaperone for the maturation of PceA, are well defined. However, the role of PceB and PceC are still not elucidated. We present a multilevel study aiming at deciphering the stoichiometry of pceABCT individual gene products. The investigation was assessed at RNA level by reverse transcription and (quantitative) polymerase chain reaction, while at protein level, proteomic analyses based on parallel reaction monitoring were performed to quantify the Pce proteins in cell-free extracts as well as in soluble and membrane fractions of both strains using heavy-labeled reference peptides. At RNA level, our results confirmed the co-transcription of all pce genes, while the quantitative analysis revealed a relative stoichiometry of the gene transcripts of pceA, pceB, pceC, and pceT at ~ 1.0:3.0:0.1:0.1 in D. restrictus. This trend was not observed in D. hafniense strain TCE1, where no substantial difference was measured for the four genes. At proteomic level, an apparent 2:1 stoichiometry of PceA and PceB was obtained in the membrane fraction, and a low abundance of PceC in comparison to the other two proteins. In the soluble fraction, a 1:1 stoichiometry of PceA and PceT was identified. In summary, we show that the pce gene cluster is transcribed as an operon with, however, a level of transcription that differs for individual genes, an observation that could be explained by post-transcriptional events. Despite challenges in the quantification of integral membrane proteins such as PceB and PceC, the similar abundance of PceA and PceB invites to consider them as forming a membrane-bound PceA2B protein complex, which, in contrast to the proposed model, seems to be devoid of PceC.

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“…Indeed, only two obligate OHRB strains (i.e., D. mccartyi MB and “Dehalobium chlorocoercia” DF-1) have been isolated from coastal sediments. , Nonetheless, nearly 10% Deltaproteobacteria from the marine environment were recently found to possess putative RDase genes in their genomes, a few of which (e.g., Halodesulfovibrio, Desulfuromusa, Desulfovibrio, and Desulfoluna) were confirmed with dehalogenation activity of brominated compounds . Additionally, the marine environment is the greatest repository of microorganisms among all biospheres, harboring ∼10 10 microbial species; therefore, it is reasonable to predict that marine systems are an underexplored pool of OHRB.…”

Section: Introductionmentioning

confidence: 99%

Offshore Marine Sediment Microbiota Respire Structurally Distinct Organohalide Pollutants

Zhang

Zhao

et al. 2022

Environ. Sci. Technol.

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Marine sediments are a major sink of organohalide pollutants, but the potential for offshore marine microbiota to transform these pollutants remains underexplored. Here, we report dehalogenation of diverse organohalide pollutants by offshore marine microbiota. Dechlorination of polychlorinated biphenyls (PCBs) was observed in four marine sediment microcosms, which was positively correlated with in situ PCB contamination. Three distinct enrichment cultures were enriched from these PCB-dechlorinating microcosms using tetrachloroethene (PCE) as the sole organohalide. All enrichment cultures also dehalogenated polybrominated diphenyl ethers (PBDEs), tetrabromobisphenol A (TBBPA), and 2,4,6-trichlorophenol (2,4,6-TCP). Particularly, two enrichments completely debrominated penta-BDEs, the first observation of complete debromination of penta-BDEs in marine cultures. Multiple Dehalococcoides and uncultivated Dehalococcoidia were identified in the initial sediment microcosms, but only Dehalococcoides was dominant in all enrichments. Transcription of a gene encoding a PcbA5-like reductive dehalogenase (RDase) was observed during dehalogenation of different organohalides in each enrichment culture. When induced by a single organohalide substrate, the PcbA5-like RDase dehalogenated all tested organohalides (PCE, PCBs, PBDEs, TBBPA, and 2,4,6-TCP) in in vitro tests, suggesting its involvement in dehalogenation of structurally distinct organohalides. Our results demonstrate the versatile dehalogenation capacity of marine Dehalococcoidia and contribute to a better understanding of the fate of these pollutants in marine systems.

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Organohalide-respiring Desulfoluna species isolated from marine environments

Cited by 27 publications

References 81 publications

Proteogenomic analysis of Georgfuchsia toluolica revealed unexpected concurrent aerobic and anaerobic toluene degradation

Proteogenomic analysis of Georgfuchsia toluolica revealed unexpected concurrent aerobic and anaerobic toluene degradation

Stoichiometry of the Gene Products From the Tetrachloroethene Reductive Dehalogenase Operon pceABCT

Offshore Marine Sediment Microbiota Respire Structurally Distinct Organohalide Pollutants

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