Dataset Information

Roles of Organohalide-Respiring Dehalococcoidia in Carbon Cycling.

ABSTRACT: The class Dehalococcoidia within the Chloroflexi phylum comprises the obligate organohalide-respiring genera Dehalococcoides, Dehalogenimonas, and "Candidatus Dehalobium." Knowledge of the unique ecophysiology and biochemistry of Dehalococcoidia has been largely derived from studies with enrichment cultures and isolates from sites impacted with chlorinated pollutants; however, culture-independent surveys found Dehalococcoidia sequences in marine, freshwater, and terrestrial biomes considered to be pristine (i.e., not impacted with organohalogens of anthropogenic origin). The broad environmental distribution of Dehalococcoidia, as well as other organohalide-respiring bacteria, supports the concept of active halogen cycling and the natural formation of organohalogens in various ecosystems. Dechlorination reduces recalcitrance and renders organics susceptible to metabolic oxidation by diverse microbial taxa. During reductive dechlorination, hydrogenotrophic organohalide-respiring bacteria, in particular Dehalococcoidia, can consume hydrogen to low consumption threshold concentrations (<0.3?nM) and enable syntrophic oxidation processes. These functional attributes and the broad distribution imply that Dehalococcoidia play relevant roles in carbon cycling in anoxic ecosystems.

SUBMITTER: Yang Y

PROVIDER: S-EPMC7289593 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Roles of Organohalide-Respiring Dehalococcoidia in Carbon Cycling.

Yang Yi Y Sanford Robert R Yan Jun J Chen Gao G Cápiro Natalie L NL Li Xiuying X Löffler Frank E FE

mSystems 20200609 3

The class Dehalococcoidia within the Chloroflexi phylum comprises the obligate organohalide-respiring genera Dehalococcoides, Dehalogenimonas, and "Candidatus Dehalobium." Knowledge of the unique ecophysiology and biochemistry of Dehalococcoidia has been largely derived from studies with enrichment cultures and isolates from sites impacted with chlorinated pollutants; however, culture-independent surveys found Dehalococcoidia sequences in marine, ...[more]

PMID: 32518199

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Project description:BackgroundMicrobial reductive dechlorination of polychlorinated biphenyls (PCBs) plays a major role in detoxifying anoxic contaminated freshwater and marine sediments from PCBs. Known members of the phylum Chloroflexi are typically responsible for this activity in freshwater sediments, whereas less is known about the microorganisms responsible for this activity in marine sediments. PCB-respiring activities were detected in PCB-impacted marine sediments of the Venice Lagoon. The aim of this work was to identify the indigenous organohalide-respiring microorganisms in such environments and assess their dechlorination specificity against spiked Aroclor™ 1254 PCBs under laboratory conditions resembling the in situ biogeochemistry.ResultsHigh PCB dechlorination activities (from 150 ± 7 to 380 ± 44 μmol of chlorine removed kg-1 week-1) were detected in three out of six sediments sampled from different locations of the lagoon. An uncultured non-Dehalococcoides phylotype of the class Dehalococcoidia closely related to Dehalobium chlorocoercia DF-1, namely phylotype VLD-1, was detected and enriched up to 109 16S rRNA gene copies per gram of sediment where dechlorination activities were higher and 25-4/24-4 and 25-2/24-2/4-4 chlorobiphenyls (CB) accumulated as the main tri-/dichlorinated products. Conversely, a different phylotype closely related to the SF1/m-1 clade, namely VLD-2, also enriched highly where lower dechlorination activity and the accumulation of 25-3 CB as main tri-chlorinated product occurred, albeit in the simultaneous presence of VLD-1. Both phylotypes showed growth yields higher or comparable to known organohalide respirers and neither phylotypes enriched in sediment cultures not exhibiting dechlorination.ConclusionsThese findings confirm the presence of different PCB-respiring microorganisms in the indigenous microbial communities of Venice Lagoon sediments and relate two non-Dehalococcoides phylotypes of the class Dehalococcoidia to different PCB dechlorination rates and specificities.

Project description:BackgroundMassive amounts of sewage sludge are generated during biological sewage treatment and are commonly subjected to anaerobic digestion, land application, and landfill disposal. Concurrently, persistent organic pollutants (POPs) are frequently found in sludge treatment and disposal systems, posing significant risks to both human health and wildlife. Metabolically versatile microorganisms originating from sewage sludge are inevitably introduced to sludge treatment and disposal systems, potentially affecting the fate of POPs. However, there is currently a dearth of comprehensive assessments regarding the capability of sewage sludge microbiota from geographically disparate regions to attenuate POPs and the underpinning microbiomes.ResultsHere we report the global prevalence of organohalide-respiring bacteria (OHRB) known for their capacity to attenuate POPs in sewage sludge, with an occurrence frequency of ~50% in the investigated samples (605 of 1186). Subsequent laboratory tests revealed microbial reductive dechlorination of polychlorinated biphenyls (PCBs), one of the most notorious categories of POPs, in 80 out of 84 sludge microcosms via various pathways. Most chlorines were removed from the para- and meta-positions of PCBs; nevertheless, ortho-dechlorination of PCBs also occurred widely, although to lower extents. Abundances of several well-characterized OHRB genera (Dehalococcoides, Dehalogenimonas, and Dehalobacter) and uncultivated Dehalococcoidia lineages increased during incubation and were positively correlated with PCB dechlorination, suggesting their involvement in dechlorinating PCBs. The previously identified PCB reductive dehalogenase (RDase) genes pcbA4 and pcbA5 tended to coexist in most sludge microcosms, but the low ratios of these RDase genes to OHRB abundance also indicated the existence of currently undescribed RDases in sewage sludge. Microbial community analyses revealed a positive correlation between biodiversity and PCB dechlorination activity although there was an apparent threshold of community co-occurrence network complexity beyond which dechlorination activity decreased.ConclusionsOur findings that sludge microbiota exhibited nearly ubiquitous dechlorination of PCBs indicate widespread and nonnegligible impacts of sludge microbiota on the fate of POPs in sludge treatment and disposal systems. The existence of diverse OHRB also suggests sewage sludge as an alternative source to obtain POP-attenuating consortia and calls for further exploration of OHRB populations in sewage sludge. Video Abstract.

Project description:While in situ chemical oxidation is often used to remediate tetrachloroethene (PCE) contaminated locations, very little is known about its influence on microbial composition and organohalide respiration (OHR) activity. Here, we investigate the impact of oxidation with permanganate on OHR rates, the abundance of organohalide respiring bacteria (OHRB) and reductive dehalogenase (rdh) genes using quantitative PCR, and microbial community composition through sequencing of 16S rRNA genes. A PCE degrading enrichment was repeatedly treated with low (25 μmol), medium (50 μmol), or high (100 μmol) permanganate doses, or no oxidant treatment (biotic control). Low and medium treatments led to higher OHR rates and enrichment of several OHRB and rdh genes, as compared to the biotic control. Improved degradation rates can be attributed to enrichment of (1) OHRB able to also utilize Mn oxides as a terminal electron acceptor and (2) non-dechlorinating community members of the Clostridiales and Deltaproteobacteria possibly supporting OHRB by providing essential co-factors. In contrast, high permanganate treatment disrupted dechlorination beyond cis-dichloroethene and caused at least a 2-4 orders of magnitude reduction in the abundance of all measured OHRB and rdh genes, as compared to the biotic control. High permanganate treatments resulted in a notably divergent microbial community, with increased abundances of organisms affiliated with Campylobacterales and Oceanospirillales capable of dissimilatory Mn reduction, and decreased abundance of presumed supporters of OHRB. Although OTUs classified within the OHR-supportive order Clostridiales and OHRB increased in abundance over the course of 213 days following the final 100 μmol permanganate treatment, only limited regeneration of PCE dechlorination was observed in one of three microcosms, suggesting strong chemical oxidation treatments can irreversibly disrupt OHR. Overall, this detailed investigation into dose-dependent changes of microbial composition and activity due to permanganate treatment provides insight into the mechanisms of OHR stimulation or disruption upon chemical oxidation.

Dataset Information

Roles of Organohalide-Respiring Dehalococcoidia in Carbon Cycling.

Publications

Roles of Organohalide-Respiring <i>Dehalococcoidia</i> in Carbon Cycling.

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