Temperature Controls Crystalline Iron Oxide Utilization by Microbial Communities in Methanic Ferruginous Marine Sediment Incubations

Aromokeye, David A.; Richter-Heitmann, Tim; Oni, Oluwatobi Emmanuel; Kulkarni, Ajinkya; Yin, Xiuran; Kasten, Sabine; Friedrich, Michael W.

doi:10.3389/fmicb.2018.02574

Cited by 28 publications

(27 citation statements)

References 90 publications

(114 reference statements)

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“…Methane concentrations in incubation headspace samples (100 µl) were monitored over time as previously described [26]. Because of the difficulty of getting an accurate determination of iron reduction kinetics by measuring total Fe(II) produced in sediment incubations [26], Fe 2+ formation in aqueous phase of sediment incubations was monitored spectrophotometrically [40]. However in the sediment-free enrichment cultures, total Fe(II) was measured as described previously [26].…”

Section: Methodsmentioning

confidence: 99%

“…Geochemical profiles and depositional history of sampling site, the HMA were previously described [6,19,28]. For the current study, sediments were taken during RV HEINCKE research expedition HE443 (54°05.23′N; 007°58.04′E) in May 2015 and preserved prior to incubation set up as described elsewhere [26]. In order to study benzoate degradation in the presence of iron oxides (lepidocrocite, hematite, and magnetite, Table S1), sediment samples from the methanic zone (247-279 cm) were used.…”

Section: Benzoate Degradation Experiments Within Sediment Slurrymentioning

confidence: 99%

“…Fermentative iron reduction of poorly crystalline iron oxide phases accounts for up to 5% of electrons during organic matter degradation in pure culture studies [20,22,23]. On the other hand, crystalline iron oxide phases accelerate organic carbon degradation to methane as primary electron sink (i.e., methanogenic degradation) in rice field soils, lake, and marine sediments by serving as conduits for direct electron transfer [24][25][26][27]. Given these previous findings, a hitherto unexplored strategy for microbes to efficiently degrade recalcitrant organic matter may rely on crystalline iron oxides acting concurrently as electron acceptors while serving as conduits.…”

Section: Introductionmentioning

confidence: 99%

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Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures

et al. 2020

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Elevated dissolved iron concentrations in the methanic zone are typical geochemical signatures of rapidly accumulating marine sediments. These sediments are often characterized by co-burial of iron oxides with recalcitrant aromatic organic matter of terrigenous origin. Thus far, iron oxides are predicted to either impede organic matter degradation, aiding its preservation, or identified to enhance organic carbon oxidation via direct electron transfer. Here, we investigated the effect of various iron oxide phases with differing crystallinity (magnetite, hematite, and lepidocrocite) during microbial degradation of the aromatic model compound benzoate in methanic sediments. In slurry incubations with magnetite or hematite, concurrent iron reduction, and methanogenesis were stimulated during accelerated benzoate degradation with methanogenesis as the dominant electron sink. In contrast, with lepidocrocite, benzoate degradation, and methanogenesis were inhibited. These observations were reproducible in sediment-free enrichments, even after five successive transfers. Genes involved in the complete degradation of benzoate were identified in multiple metagenome assembled genomes. Four previously unknown benzoate degraders of the genera Thermincola (Peptococcaceae, Firmicutes), Dethiobacter (Syntrophomonadaceae, Firmicutes), Deltaproteobacteria bacteria SG8_13 (Desulfosarcinaceae, Deltaproteobacteria), and Melioribacter (Melioribacteraceae, Chlorobi) were identified from the marine sediment-derived enrichments. Scanning electron microscopy (SEM) and catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH) images showed the ability of microorganisms to colonize and concurrently reduce magnetite likely stimulated by the observed methanogenic benzoate degradation. These findings explain the possible contribution of organoclastic reduction of iron oxides to the elevated dissolved Fe2+ pool typically observed in methanic zones of rapidly accumulating coastal and continental margin sediments.

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Section: Methodsmentioning

confidence: 99%

Section: Benzoate Degradation Experiments Within Sediment Slurrymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures

et al. 2020

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“…The concentration of methane in the headspace was measured by gas chromatography as previously described [39]. Headspace H 2 was determined with a reduction gas detector (Trace Analytical, Menlo Park, CA, USA).…”

Section: Gas Analysismentioning

confidence: 99%

“…S1) and previously reported density shifts in SIP fractions [41], "heavy" (1.803-1.823 g mL −1 , combination of fraction 3, 4, and 5) and "light" (1.777-1.780 g mL −1 , fraction 11) fractions of RNA-SIP samples were selected. Library construction and sequence read processing were as described previously [39].…”

Section: Sequencing and Bioinformatics Analysismentioning

confidence: 99%

CO2 conversion to methane and biomass in obligate methylotrophic methanogens in marine sediments

Yin

Maeke

et al. 2019

The ISME Journal

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Methyl substrates are important compounds for methanogenesis in marine sediments but diversity and carbon utilization by methylotrophic methanogenic archaea have not been clarified. Here, we demonstrate that RNA-stable isotope probing (SIP) requires 13 C-labeled bicarbonate as co-substrate for identification of methylotrophic methanogens in sediment samples of the Helgoland mud area, North Sea. Using lipid-SIP, we found that methylotrophic methanogens incorporate 60-86% of dissolved inorganic carbon (DIC) into lipids, and thus considerably more than what can be predicted from known metabolic pathways (~40% contribution). In slurry experiments amended with the marine methylotroph Methanococcoides methylutens, up to 12% of methane was produced from CO 2 , indicating that CO 2-dependent methanogenesis is an alternative methanogenic pathway and suggesting that obligate methylotrophic methanogens grow in fact mixotrophically on methyl compounds and DIC. Although methane formation from methanol is the primary pathway of methanogenesis, the observed high DIC incorporation into lipids is likely linked to CO 2-dependent methanogenesis, which was triggered when methane production rates were low. Since methylotrophic methanogenesis rates are much lower in marine sediments than under optimal conditions in pure culture, CO 2 conversion to methane is an important but previously overlooked methanogenic process in sediments for methylotrophic methanogens.

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Microbial community composition and functional potential in Bothnian Sea sediments is linked to Fe and S dynamics and the quality of organic matter

Rasigraf

Helmond

Frank

et al. 2019

Limnology & Oceanography

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The Bothnian Sea is an oligotrophic brackish basin characterized by low salinity and high concentrations of reactive iron, methane, and ammonium in its sediments, enabling the activity and interactions of many microbial guilds. Here, we studied the microbial network in these sediments by analyzing geochemical and microbial community depth profiles at one offshore and two near coastal sites. Analysis of 16S rRNA gene amplicons revealed a distinct depth stratification of both archaeal and bacterial taxa. The microbial communities at the two near coastal sites were more similar to each other than the offshore site, which is likely due to differences in the quality and rate of organic matter degradation. The abundance of methanotrophic archaea of the ANME-2a clade was shown to be related to the presence of methane and varied with sediment iron content. Metagenomic sequencing of sediment-derived DNA from below the sulfate-methane transition zone revealed a broad potential for respiratory sulfur metabolism via partially reduced sulfur species. The potential for nitrogen cycling was dominated by reductive processes via a truncated denitrification pathway encoded exclusively by bacterial lineages. Gene-centric fermentative metabolism analysis indicated a potential importance for acetate, formate, alcohol, and hydrogen metabolism. Methanogenic/-trophic pathways were dominated by Methanosaetaceae, Methanosarcinaceae, Methanomassiliicoccaceae, Methanoregulaceae, and ANME-2 archaea. Our results indicated flexible metabolic capabilities of core microbial community taxa, which could adapt to changing redox conditions, and with a spatial and depth distribution that is likely governed by the quality and input of available organic substrates and, for ANME-2, of iron oxides.

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Temperature Controls Crystalline Iron Oxide Utilization by Microbial Communities in Methanic Ferruginous Marine Sediment Incubations

Cited by 28 publications

References 90 publications

Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures

Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures

CO2 conversion to methane and biomass in obligate methylotrophic methanogens in marine sediments

Microbial community composition and functional potential in Bothnian Sea sediments is linked to Fe and S dynamics and the quality of organic matter

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