Metagenomic insights into the metabolism of microbial communities that mediate iron and methane cycling in Lake Kinneret sediments
Michal Elul, Maxim Rubin‐Blum, Zeev Ronen, Itay Bar-Or, Werner Eckert, Orit Sivan
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, anaerobic oxidation of methane (AOM) or both (Fe-AOM). Here, we investigated microbial communities from both natural Lake Kinneret sediments and iron-amended slurry incubations 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 intrinsic 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 monomer, PilA, which were attributed to this lineage. The bonafide anaerobic oxidizers of methane (ANME) and denitrifying methanotrophs Methylomirabilia (NC10) were scarce, and we consider the role of the lineage Methanothrix (Methanothrichales) in Fe-AOM. We show that putative aerobes, such as methane-oxidizing bacteria Methylomonas and their methylotrophic synthrophs Methylotenera are found among the anaerobic lineages in Lake Kinneret iron amended slurries and can be involved in the oxidation of methane or its intermediates, as suggested previously. We propose a reaction model for metabolic interactions in the lake 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 Fe-AOM as one strategy for survival.