Anaerobic microbial methanol conversion in marine sediments.
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ABSTRACT:
SUBMITTER: Fischer PQ
PROVIDER: S-EPMC8048578 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The flux of methane, a potent greenhouse gas, from the seabed is largely controlled by anaerobic oxidation of methane (AOM) coupled to sulfate reduction (S-AOM) in the sulfate methane transition (SMT). S-AOM is estimated to oxidize 90% of the methane produced in marine sediments and is mediated by a consortium of anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria. An additional methane sink, i.e., iron oxide coupled AOM (Fe-AOM), has been suggested to be active in the methanic zone of marine sediments. Geochemical signatures below the SMT such as high dissolved iron, low to undetectable sulfate and high methane concentrations, together with the presence of iron oxides are taken as prerequisites for this process. So far, Fe-AOM has neither been proven in marine sediments nor have the governing key microorganisms been identified. Here, using a multidisciplinary approach, we show that Fe-AOM occurs in iron oxide-rich methanic sediments of the Helgoland Mud Area (North Sea). When sulfate reduction was inhibited, different iron oxides facilitated AOM in long-term sediment slurry incubations but manganese oxide did not. Especially magnetite triggered substantial Fe-AOM activity and caused an enrichment of ANME-2a archaea. Methane oxidation rates of 0.095 ± 0.03 nmol cm-3 d-1 attributable to Fe-AOM were obtained in short-term radiotracer experiments. The decoupling of AOM from sulfate reduction in the methanic zone further corroborated that AOM was iron oxide-driven below the SMT. Thus, our findings prove that Fe-AOM occurs in methanic marine sediments containing mineral-bound ferric iron and is a previously overlooked but likely important component in the global methane budget. This process has the potential to sustain microbial life in the deep biosphere.
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Project description:Chitin is massively produced by freshwater plankton species as a structural element of their exoskeleton or cell wall. At the same time, chitin does not accumulate in the predominantly anoxic sediments, underlining its importance as carbon and nitrogen sources for sedimentary microorganisms. We studied chitin degradation in littoral sediment of Lake Constance, Central Europe's third largest lake. Turnover of the chitin analog methyl-umbelliferyl-N,N-diacetylchitobioside (MUF-DC) was highest in the upper oxic sediment layer, with 5.4?nmol MUF-DC h-1 (g sediment [dry weight])-1 In the underlying anoxic sediment layers, chitin hydrolysis decreased with depth from 1.1 to 0.08?nmol MUF-DC h-1 (g sediment [dry weight])-1 Bacteria involved in chitin degradation were identified by 16S rRNA (gene) amplicon sequencing of anoxic microcosms incubated in the presence of chitin compared to microcosms amended either with N-acetylglucosamine as the monomer of chitin or no substrate. Chitin degradation was driven by a succession of bacteria responding specifically to chitin only. The early phase (0 to 9?days) was dominated by Chitinivibrio spp. (Fibrobacteres). The intermediate phase (9 to 21?days) was characterized by a higher diversity of chitin responders, including, besides Chitinivibrio spp., also members of the phyla Bacteroidetes, Proteobacteria, Spirochaetes, and Chloroflexi In the late phase (21 to 43?days), the Chitinivibrio populations broke down with a parallel strong increase of Ruminiclostridium spp. (formerly Clostridium cluster III, Firmicutes), which became the dominating chitin responders. Our study provides quantitative insights into anaerobic chitin degradation in lake sediments and linked this to a model of microbial succession associated with this activity.IMPORTANCE Chitin is the most abundant biopolymer in aquatic environments, with a direct impact on the carbon and nitrogen cycles. Despite its massive production as a structural element of crustaceans, insects, or algae, it does not accumulate in sediments. Little is known about its turnover in predominantly anoxic freshwater sediments and the responsible microorganisms. We proved that chitin is readily degraded under anoxic conditions and linked this to a succession of the members of the responsible microbial community over a 43-day period. While Fibrobacteres and Firmicutes members were driving the early and late phases of chitin degradation, respectively, a more diverse community was involved in chitin degradation in the intermediate phase. Entirely different microorganisms responded toward the chitin monomer N-acetylglucosamine, which underscores that soluble monomers are poor and misleading substrates to study polymer-utilizing microorganisms. Our study provides quantitative insights into the microbial ecology driving anaerobic chitin degradation in freshwater sediments.
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Project description:Little is known about the diversity and succession of indigenous microbial community during debromination of polybrominated diphenyl ethers (PBDEs). This study examined the diversity and dynamics of microbial community structure in eight saline (mangrove and marine) and freshwater sediment microcosms exhibiting different debrominating capabilities for hexa-BDE 153, a common congener in sediments, using terminal restriction fragment length polymorphism (T-RFLP) and clone library analyses. The results showed that microbial community structure greatly differed between the saline and freshwater microcosms, likely leading to distinct variations in their debrominating capabilities and pathways. Higher relative abundances of Chloroflexi and Deltaproteobacteria succeed by Alphaproteobacteria and Betaproteobacteria were detected in the two mangrove microcosms with the fastest debrominating capabilities mainly via para pathway, respectively; the dominance of Alphaproteobacteria resulted in less accumulation of tetra-BDEs and more complete debromination of lower brominated congeners (from di- to tetra-BDEs). Meanwhile, the shifts in both microbial community structure and PBDE profiles were relatively small in the less efficient freshwater microcosms, with relatively more ortho and meta brominated products of BDE-153 resulted. Coincidently, one of the freshwater microcosms showed sudden increases of Chloroflexi and Deltaproteobacteria by the end of incubation, which synchronized with the increase in the removal rate of BDE-153. The significant relationship between microbial community structure and PBDEs was confirmed by redundancy analysis (18.7% of total variance explained, P = 0.002). However, the relative abundance of the well-known dechlorinator Dehalococcoides showed no clear correlation with the debrominating capability across different microcosms. These findings shed light in the significance of microbial community network in different saline environments on enhancement of PBDE intrinsic debromination.
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Project description:Alkanes comprise a substantial fraction of crude oil and are prevalent at marine seeps. These environments are typically anoxic and host diverse microbial communities that grow on alkanes. The most widely distributed mechanism of anaerobic alkane activation is the addition of alkanes to fumarate by (1-methylalkyl)succinate synthase (Mas). Here we studied the diversity of MasD, the catalytic subunit of the enzyme, in 12 marine sediments sampled at seven seeps. We aimed to identify cosmopolitan species as well as to identify factors structuring the alkane-degrading community. Using next generation sequencing we obtained a total of 420 MasD species-level operational taxonomic units (OTU0.96) at 96% amino acid identity. Diversity analysis shows a high richness and evenness of alkane-degrading bacteria. Sites with similar hydrocarbon composition harbored similar alkane-degrading communities based on MasD genes; the MasD community structure is clearly driven by the hydrocarbon source available at the various seeps. Two of the detected OTU0.96 were cosmopolitan and abundant while 75% were locally restricted, suggesting the presence of few abundant and globally distributed alkane degraders as well as specialized variants that have developed under specific conditions at the diverse seep environments. Of the three MasD clades identified, the most diverse was affiliated with Deltaproteobacteria. A second clade was affiliated with both Deltaproteobacteria and Firmicutes likely indicating lateral gene transfer events. The third clade was only distantly related to known alkane-degrading organisms and comprises new divergent lineages of MasD homologs, which might belong to an overlooked phylum of alkane-degrading bacteria. In addition, masD geneFISH allowed for the in situ identification and quantification of the target guild in alkane-degrading enrichment cultures. Altogether, these findings suggest an unexpectedly high number of yet unknown groups of anaerobic alkane degraders and underline the need for comprehensive surveys of microbial diversity based on metabolic genes in addition to ribosomal genes.
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Project description:Hydrocarbons released during oil spills are persistent in marine sediments due to the absence of suitable electron acceptors below the oxic zone. Here, we investigated an alternative bioremediation strategy to remove toluene, a model monoaromatic hydrocarbon, using a bioanode. Bioelectrochemical reactors were inoculated with sediment collected from a hydrocarbon-contaminated marine site, and anodes were polarized at 0 mV and +300 mV (versus an Ag/AgCl [3 M KCl] reference electrode). The degradation of toluene was directly linked to current generation of up to 301 mA m(-2) and 431 mA m(-2) for the bioanodes polarized at 0 mV and +300 mV, respectively. Peak currents decreased over time even after periodic spiking with toluene. The monitoring of sulfate concentrations during bioelectrochemical experiments suggested that sulfur metabolism was involved in toluene degradation at bioanodes. 16S rRNA gene-based Illumina sequencing of the bulk anolyte and anode samples revealed enrichment with electrocatalytically active microorganisms, toluene degraders, and sulfate-reducing microorganisms. Quantitative PCR targeting the α-subunit of the dissimilatory sulfite reductase (encoded by dsrA) and the α-subunit of the benzylsuccinate synthase (encoded by bssA) confirmed these findings. In particular, members of the family Desulfobulbaceae were enriched concomitantly with current production and toluene degradation. Based on these observations, we propose two mechanisms for bioelectrochemical toluene degradation: (i) direct electron transfer to the anode and/or (ii) sulfide-mediated electron transfer.
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Project description:The anaerobic oxidation of methane (AOM) with sulfate controls the emission of the greenhouse gas methane from the ocean floor. AOM is performed by microbial consortia of archaea (ANME) associated with partners related to sulfate-reducing bacteria. In vitro enrichments of AOM were so far only successful at temperatures ?25?°C; however, energy gain for growth by AOM with sulfate is in principle also possible at higher temperatures. Sequences of 16S rRNA genes and core lipids characteristic for ANME as well as hints of in situ AOM activity were indeed reported for geothermally heated marine environments, yet no direct evidence for thermophilic growth of marine ANME consortia was obtained to date. To study possible thermophilic AOM, we investigated hydrothermally influenced sediment from the Guaymas Basin. In vitro incubations showed activity of sulfate-dependent methane oxidation between 5 and 70?°C with an apparent optimum between 45 and 60?°C. AOM was absent at temperatures ?75?°C. Long-term enrichment of AOM was fastest at 50?°C, yielding a 13-fold increase of methane-dependent sulfate reduction within 250 days, equivalent to an apparent doubling time of 68 days. The enrichments were dominated by novel ANME-1 consortia, mostly associated with bacterial partners of the deltaproteobacterial HotSeep-1 cluster, a deeply branching phylogenetic group previously found in a butane-amended 60?°C-enrichment culture of Guaymas sediments. The closest relatives (Desulfurella spp.; Hippea maritima) are moderately thermophilic sulfur reducers. Results indicate that AOM and ANME archaea could be of biogeochemical relevance not only in cold to moderate but also in hot marine habitats.
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Project description:A large proportion of prokaryotic microbes in marine sediments remains uncultured, hindering our understanding of their ecological functions and metabolic features. Recent environmental metagenomic studies suggested that many of these uncultured microbes contribute to the degradation of organic matter, accompanied by acetogenesis, but the supporting experimental evidence is limited. Estuarine sediments were incubated with different types of organic matters under anaerobic conditions, and the increase of uncultured bacterial populations was monitored. We found that (1) lignin stimulated the increase of uncultured bacteria within the class Dehalococcoidia. Their ability to metabolize lignin was further supported by the presence of genes associated with a nearly complete degradation pathway of phenolic monomers in the Dehalococcoidia metagenome-assembled genomes (MAGs). (2) The addition of cellulose stimulated the increase of bacteria in the phylum Ca. Fermentibacterota and family Fibrobacterales, a high copy number of genes encoding extracellular endoglucanase or/and 1,4-beta-cellobiosidase for cellulose decomposition and multiple sugar transporters were present in their MAGs. (3) Uncultured lineages in the order Bacteroidales and the family Leptospiraceae were enriched by the addition of casein and oleic acid, respectively, a high copy number of genes encoding extracellular peptidases, and the complete β-oxidation pathway were found in those MAGs of Bacteroidales and Leptospiraceae, respectively. (4) The growth of unclassified bacteria of the order Clostridiales was found after the addition of both casein and cellulose. Their MAGs contained multiple copies of genes for extracellular peptidases and endoglucanase. Additionally, 13C-labeled acetate was produced in the incubations when 13C-labeled dissolved inorganic carbon was provided. Our results provide new insights into the roles of microorganisms during organic carbon degradation in anaerobic estuarine sediments and suggest that these macro and single molecular organic carbons support the persistence and increase of uncultivated bacteria. Acetogenesis is an additional important microbial process alongside organic carbon degradation. Video Abstract.
| S-EPMC10116835 | biostudies-literature
Project description:Alkanes are major constituents of crude oil and are released to the marine environment by natural seepage and from anthropogenic sources. Due to their chemical inertness, their removal from anoxic marine sediments is primarily controlled by the activity of anaerobic alkane-degrading microorganisms. To facilitate comprehensive cultivation-independent surveys of the diversity and distribution of anaerobic alkane degraders, we designed novel PCR primers that cover all known diversity of the 1-methylalkyl succinate synthase gene (masD/assA), which catalyzes the initial activation of alkanes. We studied masD/assA gene diversity in pristine and seepage-impacted Danish coastal sediments, as well as in sediments and alkane-degrading enrichment cultures from the Middle Valley (MV) hydrothermal vent system in the Pacific Northwest. MasD/assA genes were ubiquitously present, and the primers captured the diversity of both known and previously undiscovered masD/assA gene diversity. Seepage sediments were dominated by a single masD/assA gene cluster, which is presumably indicative of a substrate-adapted community, while pristine sediments harbored a diverse range of masD/assA phylotypes including those present in seepage sediments. This rare biosphere of anaerobic alkane degraders will likely increase in abundance in the event of seepage or accidental oil spillage. Nanomolar concentrations of short-chain alkanes (SCA) were detected in pristine and seepage sediments. Interestingly, anaerobic alkane degraders closely related to strain BuS5, the only SCA degrader in pure culture, were found in mesophilic MV enrichments, but not in cold sediments from Danish waters. We propose that the new masD/assA gene lineages in these sediments represent novel phylotypes that are either fueled by naturally occurring low levels of SCA or that metabolize medium- to long-chain alkanes. Our study highlights that masD/assA genes are a relevant diagnostic marker to identify seepage and microseepage, e.g., during prospecting for oil and gas, and may act as an indicator of anthropogenic oil spills in marine sediments.
| S-EPMC4681840 | biostudies-literature
Project description:The fate of cyclohexane, often used as a model compound for the biodegradation of cyclic alkanes due to its abundance in crude oils, in anoxic marine sediments has been poorly investigated. In the present study, we obtained an enrichment culture of cyclohexane-degrading sulfate-reducing bacteria from hydrocarbon-contaminated intertidal marine sediments. Microscopic analyses showed an apparent dominance by oval cells of 1.5 × 0.8 μm. Analysis of a 16S rRNA gene library, followed by whole-cell hybridization with group- and sequence-specific oligonucleotide probes showed that these cells belonged to a single phylotype, and were accounting for more than 80% of the total cell number. The dominant phylotype, affiliated with the Desulfosarcina-Desulfococcus cluster of the Deltaproteobacteria, is proposed to be responsible for the degradation of cyclohexane. Quantitative growth experiments showed that cyclohexane degradation was coupled with the stoichiometric reduction of sulfate to sulfide. Substrate response tests corroborated with hybridization with a sequence-specific oligonucleotide probe suggested that the dominant phylotype apparently was able to degrade other cyclic and n-alkanes, including the gaseous alkane n-butane. Based on GC-MS analyses of culture extracts cyclohexylsuccinate was identified as a metabolite, indicating an activation of cyclohexane by addition to fumarate. Other metabolites detected were 3-cyclohexylpropionate and cyclohexanecarboxylate providing evidence that the overall degradation pathway of cyclohexane under anoxic conditions is analogous to that of n-alkanes.
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Project description:Disturbance strongly impacts patterns of community diversity, yet the shape of the diversity-disturbance relationship remains a matter of debate. The topic has been of interest in theoretical ecology for decades as it has practical implications for the understanding of ecosystem services in nature. One of these processes is the remineralization of organic matter by microorganisms in coastal marine sediments, which are periodically impacted by disturbances across the sediment-water interface. Here we set up an experiment to test the hypothesis that disturbance impacts microbial diversity and function during the anaerobic degradation of organic matter in coastal sediments. We show that during the first 3 weeks of the experiment, disturbance increased both microbial production, derived from the increase in microbial abundance, and diversity of the active fraction of the community. Both community diversity and phylogenetic diversity increased, which suggests that disturbance promoted the cohabitation of ecologically different microorganisms. Metagenome analysis also showed that disturbance increased the relative abundance of genes diagnostic of metabolism associated with the sequential anaerobic degradation of organic matter. However, community composition was not impacted in a systematic way and changed over time. In nature, we can hypothesize that moderate storm disturbances, which impact coastal sediments, promote diverse, and productive communities. These events, rather than altering the decomposition of organic matter, may increase the substrate turnover and, ultimately, remineralization rates.
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