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

Abstract

Abstract. Complex microbial communities facilitate iron and methane transformations in anoxic methanic sediments of freshwater lakes, such as Lake Kinneret (the Sea of Galilee, Israel). The phylogenetic and functional diversity of these consortia are not fully understood, and it is not clear which lineages perform iron reduction and anaerobic oxidation of methane (AOM). Here, we investigated microbial communities from both natural Lake Kinneret iron-rich methanic sediments (>20 cm depth) and iron-amended slurry incubations from this zone using metagenomics, focusing on functions associated with iron reduction and methane cycling. Analyses of the phylogenetic and functional diversity indicate that consortia of archaea (mainly Bathyarchaeia, Methanomicrobia, Thermoplasmata, and Thermococci) and bacteria (mainly Chloroflexi (Chloroflexota), Nitrospirae (Nitrospirota), and Proteobacteria) perform key metabolic reactions such as amino acid uptake and dissimilation, organic matter fermentation, and methanogenesis. The Deltaproteobacteria, especially Desulfuromondales (Desulfuromonadota), have the potential to transfer electrons extracellularly either to iron mineral particles or to microbial syntrophs, including methanogens. This is likely via transmembrane cytochromes, outer-membrane hexaheme c-type cytochrome (OmcS) in particular, or pilin monomers (PilA), all of which were attributed to this lineage. Bona fide anaerobic oxidizers of methane (ANME) and denitrifying methanotrophs Methylomirabilia (NC10) may mediate AOM in these methanogenic sediments; however we also consider the role of methanogens in active AOM or back flux of methanogenesis. Putative aerobes, such as methane-oxidizing bacteria Methylomonas and their methylotrophic syntrophs Methylotenera, are found among the anaerobic lineages in Lake Kinneret iron-amended slurries and are also involved in the oxidation of methane or its intermediates, as suggested previously. We propose a reaction model for the metabolic interactions in these sediments, linking the potential players that interact via intricate metabolic tradeoffs and direct electron transfer between species. Our results highlight the metabolic complexity of microbial communities in an energy-limited environment, where aerobe and anaerobe communities may co-exist and facilitate AOM as one strategy for survival.

Organic sulfur from source to sink in low-sulfate Lake Superior

“…Most (14%) of this sulfate reducing community were canonical Desulfobacterota. Other sulfate reducers included Thermodesulfovibrionales, which have been previously found in freshwater, iron-rich lake sediments (Elul et al 2021). We also identified dsrAB in thus-far uncultured Binatota, which appears to be genetically capable of degrading simple methane sulfones and sulfides (Murphy et al 2023).…”

Organic sulfur from source to sink in low‐sulfate Lake Superior

“…Most (14%) of this sulfate reducing community were canonical Desulfobacterota. Other sulfate reducers included Thermodesulfovibrionales, which have been previously found in freshwater, iron‐rich lake sediments (Elul et al 2021). We also identified dsrAB in thus‐far uncultured Binatota, which appear to be genetically capable of metabolizing simple methane sulfones and sulfides (Murphy et al 2023).…”

The reduction of environmentally abundant iron oxides by the methanogen Methanosarcina barkeri

“…Iron reduction by lowly reactive iron minerals in the methanogenic zone was previously demonstrated ( Gault et al, 2011 ; Egger et al, 2017 ; Vigderovich et al, 2019 ; Amiel et al, 2020 ) but the involved dominant microbes have not been identified yet. It has been suggested that archaeal methanogens may play a role in this reduction, based on geochemical and microbial studies in natural sediments ( Elul et al, 2021 ). Here, we indeed established that the naturally abundant archaeon methanogen M. barkeri might actually switch its metabolic pathway from methanogenesis to iron reduction, with abundant and low-reactivity minerals such as magnetite and hematite, and in the absence of hydrogen.…”

“…Among them is a switch of the archaeal methanogens from methanogenesis to iron reduction at the expense of methanogenesis, outcompeting iron-reducing bacteria. The potential role of methanogens from the Methanosarcinales order to reduce iron has been indeed suggested based on geochemical and microbial works on natural sediments ( Van Bodegom et al, 2004 ; Sivan et al, 2016 ; Bar-Or et al, 2017 ; Vigderovich et al, 2019 ; Elul et al, 2021 ). Previous studies with pure cultures of methanogens showed that it could reduce iron oxides with several external substrates (such as acetate, methanol, or hydrogen; Bond and Lovley, 2002 ; Liu et al, 2011a ; Sivan et al, 2016 ; Wang et al, 2020 ).…”