Evidence for microbial iron reduction in the methanic sediments of the oligotrophic southeastern Mediterranean continental shelf

Abstract

Abstract. Dissimilatory iron reduction is probably one of the oldest types of metabolisms that still participates in important biogeochemical cycles, such as those of carbon and sulfur. It is one of the more energetically favorable anaerobic microbial respiration processes and is usually coupled to the oxidation of organic matter. Traditionally this process is thought to be limited to the shallow part of the sedimentary column in most aquatic systems. However, iron reduction has also been observed in the methanic zone of many marine and freshwater sediments, well below its expected zone and occasionally accompanied by decreases in methane, suggesting a link between the iron and the methane cycles. Nevertheless, the mechanistic nature of this link (competition, redox or other) has yet to be established and has not been studied in oligotrophic shallow marine sediments. In this study we present combined geochemical and molecular evidences for microbial iron reduction in the methanic zone of the oligotrophic southeastern (SE) Mediterranean continental shelf. Geochemical porewater profiles indicate iron reduction in two zones, the uppermost part of the sediment, and the deeper zone, in the layer of high methane concentration. Results from a slurry incubation experiment indicate that the deep methanic iron reduction is microbially mediated. The sedimentary profiles of microbial abundance and quantitative PCR (qPCR) of the mcrA gene, together with Spearman correlation between the microbial data and Fe(II) concentrations in the porewater, suggest types of potential microorganisms that may be involved in the iron reduction via several potential pathways: H2 or organic matter oxidation, an active sulfur cycle, or iron-driven anaerobic oxidation of methane. We suggest that significant upward migration of methane in the sedimentary column and its oxidation by sulfate may fuel the microbial activity in the sulfate methane transition zone (SMTZ). The biomass created by this microbial activity can be used by the iron reducers below, in the methanic zone of the sediments of the SE Mediterranean.

Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane Seeps

“…However, various chemical compounds are thermodynamically more favorable electron acceptors than sulfate for catalyzing anaerobic methane oxidation, such as nitrite ( Raghoebarsing et al, 2006 ), nitrate ( Haroon et al, 2013 ), ferric iron, and manganese ( Ettwig et al, 2016 ; Cai et al, 2018 ). For instance, biogeochemical profiling evidences indicated the widespread presence of Fe-anaerobic oxidation of methane (AOM) in the ocean, such as in Argentine Basin ( Riedinger et al, 2014 ), Alaskan Beaufort Sea ( Treude et al, 2014 ), North Sea Helgoland mud ( Oni et al, 2015 ), Baltic Sea ( Egger et al, 2017 ), and Mediterranean Sea ( Vigderovich et al, 2019 ). Targeted enrichment with ferrihydrite provides strong evidence for AOM coupled with iron reduction, and ANME-1, Methanococcoides /ANME-3 ( Beal et al, 2009 ), ANME-2a and -2c ( Scheller et al, 2016 ), ANME-2d ( Methanoperedens nitroreducens ) ( Ettwig et al, 2016 ; Shen et al, 2019 ), Candidatus Methanoperedens ferrireducens ( Cai et al, 2018 ), and Methanosarcina acetivorans ( Yan et al, 2018 ) might be involved in Fe-AOM.…”

Mechanism of silicate elution by hydrogen sulfide from bottom sediment in a brackish lake

“…Dissolved silicate adsorbs onto ferric hydroxide precipitates at neutral pH values (Iler 1979;Swedlund and Webster 1999; Lehtimäki et al 2016). In addition, ferric hydroxide is abundant in oxidative sediment found in brackish lakes along coastal sea areas (Kostka and Luther III 1994;Vigderovich et al 2019). Based on this, we propose the following mechanisms as a hypothesis to explain the phenomenon observed in Lake Nakaumi.…”

Metagenomic insights into the metabolism of microbial communities that mediate iron and methane cycling in Lake Kinneret iron-rich methanic sediments

“…These environments are usually low in sulfate, and thus other terminal electron acceptors such as metals, iron (Fe) in particular; nitrate; nitrite; and humic acids become available for this process, as explored in recent studies (Raghoebarsing et al, 2006;Ettwig et al, 2010;Adler et al, 2011;Haroon et al, 2013;Norði et al, 2013;Scheller et al, 2016;Bai et al, 2019). However, the diversity and metabolic potential of the microbial communities in natural anoxic ferruginous sediments are not fully understood (Vuillemin et al, 2018).…”

“…Complex microbial consortia mediate the biogeochemical transformations in anoxic lake sediments (Vuillemin et al, 2018). These include methylotrophic and hydrogenotrophic methanogens from the Thermoplasmata, Methanomicrobia, Methanobacteria, and Bathyarchaeota clades, as well as potential sulfate or iron reducers, such as Deltaproteobacteria, Firmicutes, and Nitrospirae lineages (Vuillemin et al, 2018).…”

“…Complex microbial consortia mediate the biogeochemical transformations in anoxic lake sediments (Vuillemin et al, 2018). These include methylotrophic and hydrogenotrophic methanogens from the Thermoplasmata, Methanomicrobia, Methanobacteria, and Bathyarchaeota clades, as well as potential sulfate or iron reducers, such as Deltaproteobacteria, Firmicutes, and Nitrospirae lineages (Vuillemin et al, 2018). Alongside the abovementioned lineages, Bar-Or et al (2015) identified acetoclastic methanogens such as Methanothrix (formerly Methanosaeta, Methanosarcinales, recently reclassified as Methanothrichales by the Genome Taxonomy Database, GTDB;Parks et al, 2018), as well as the H 2 and CO 2 -using methanogenic Methanomicrobiales genera Methanolinea and Methanoregula in Lake Kinneret sediments.…”