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Permanently cold marine sediments are heavily influenced by increased input of iron as a result of accelerated glacial melt, weathering, and erosion. The impact of such environmental changes on microbial communities in coastal sediments is poorly understood. We investigated geochemical parameters that shape microbial community compositions in anoxic surface sediments of four geochemically differing sites (Annenkov Trough, Church Trough, Cumberland Bay, Drygalski Trough) around South Georgia, Southern Ocean. Sulfate reduction prevails in Church Trough and iron reduction at the other sites, correlating with differing local microbial communities. Within the order Desulfuromonadales, the family Sva1033, not previously recognized for being capable of dissimilatory iron reduction, was detected at rather high relative abundances (up to 5%) while other members of Desulfuromonadales were less abundant (, Facultad de Ciencias Exactas

Colonization of newly ice-free areas by marine benthic organisms intensifies burial of macroalgae detritus in Potter Cove coastal surface sediments (Western Antarctic Peninsula). Thus, fresh and labile macroalgal detritus serves as primary organic matter (OM) source for microbial degradation. Here, we investigated the effects on post-depositional microbial iron reduction in Potter Cove using sediment incubations amended with pulverized macroalgal detritus as OM source, acetate as primary product of OM degradation and lepidocrocite as reactive iron oxide to mimic in situ conditions. Humic substances analogue anthraquinone-2,6-disulfonic acid (AQDS) was also added to some treatments to simulate potential for electron shuttling. Microbial iron reduction was promoted by macroalgae and further enhanced by up to 30-folds with AQDS. Notably, while acetate amendment alone did not stimulate iron reduction, adding macroalgae alone did. Acetate, formate, lactate, butyrate and propionate were detected as fermentation products from macroalgae degradation. By combining 16S rRNA gene sequencing and RNA stable isotope probing, we reconstructed the potential microbial food chain from macroalgae degraders to iron reducers. Psychromonas, Marinifilum, Moritella, and Colwellia were detected as potential fermenters of macroalgae and fermentation products such as lactate. Members of class deltaproteobacteria including Sva1033, Desulfuromonas, and Desulfuromusa together with Arcobacter (former phylum Epsilonbacteraeota, now Campylobacterota) acted as dissimilatory iron reducers. Our findings demonstrate that increasing burial of macroalgal detritus in an Antarctic fjord affected by glacier retreat intensifies early diagenetic processes such as iron reduction. Under scenarios of global warming, the active microbial populations identified above will expand their environmental function, facilitate OM remineralisation, and contribute to an increased release of iron and CO2 from sediments. Such indirect consequences of glacial retreat are often overlooked but might, on a regional scale, be relevant for the assessment of future nutrient and carbon fluxes.

Metagenomic analysis has facilitated prediction of a variety of carbon utilization potentials by uncultivated archaea including degradation of protein, which is a wide-spread carbon polymer in marine sediments. However, the activity of detrital catabolic protein degradation is mostly unknown for the vast majority of archaea. Here, we show actively executed protein catabolism in three archaeal phyla (uncultivated Thermoplasmata, SG8-5; Bathyarchaeota subgroup 15; Lokiarchaeota subgroup 2c) by RNA- and lipid-stable isotope probing in incubations with different marine sediments. However, highly abundant potential protein degraders Thermoprofundales (MBG-D) and Lokiarchaeota subgroup 3 were not incorporating 13C-label from protein during incubations. Nonetheless, we found that the pathway for protein utilization was present in metagenome associated genomes (MAGs) of active and inactive archaea. This finding was supported by screening extracellular peptidases in 180 archaeal MAGs, which appeared to be widespread but not correlated to organisms actively executing this process in our incubations. Thus, our results have important implications: (i) multiple low-abundant archaeal groups are actually catabolic protein degraders; (ii) the functional role of widespread extracellular peptidases is not an optimal tool to identify protein catabolism, and (iii) catabolic degradation of sedimentary protein is not a common feature of the abundant archaeal community in temperate and permanently cold marine sediments.

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 Fe

Asgard is a recently discovered archaeal superphylum, closely linked to the emergence of eukaryotes. Among Asgard archaea, Lokiarchaeota are abundant in marine sediments, but their in situ activities are largely unknown except for Candidatus ‘Prometheoarchaeum syntrophicum’. Here, we tracked the activity of Lokiarchaeota in incubations with Helgoland mud area sediments (North Sea) by stable isotope probing (SIP) with organic polymers, 13C-labelled inorganic carbon, fermentation intermediates and proteins. Within the active archaea, we detected members of the Lokiarchaeota class Loki-3, which appeared to mixotrophically participate in the degradation of lignin and humic acids while assimilating CO2, or heterotrophically used lactate. In contrast, members of the Lokiarchaeota class Loki-2 utilized protein and inorganic carbon, and degraded bacterial biomass formed in incubations. Metagenomic analysis revealed pathways for lactate degradation, and involvement in aromatic compound degradation in Loki-3, while the less globally distributed Loki-2 instead rely on protein degradation. We conclude that Lokiarchaeotal subgroups vary in their metabolic capabilities despite overlaps in their genomic equipment, and suggest that these subgroups occupy different ecologic niches in marine sediments.

Asgard is an archaeal superphylum that might hold the key to understand the origin of eukaryotes, but its diversity and ecological roles remain poorly understood. Here, we reconstructed 15 metagenomic-assembled genomes from coastal sediments covering most known Asgard archaea and a novel group, which is proposed as a new Asgard phylum named as the "Gerdarchaeota". Genomic analyses predict that Gerdarchaeota are facultative anaerobes in utilizing both organic and inorganic carbon. Unlike their closest relatives Heimdallarchaeota, Gerdarchaeota have genes encoding for cellulase and enzymes involved in the tetrahydromethanopterin-based Wood-Ljungdahl pathway. Transcriptomics showed that most of our identified Asgard archaea are capable of degrading organic matter, including peptides, amino acids and fatty acids, occupying ecological niches in different depths of layers of the sediments. Overall, this study broadens the diversity of the mysterious Asgard archaea and provides evidence for their ecological roles in coastal sediments.

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 13C-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 CO2, indicating that CO2-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 CO2-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, CO2 conversion to methane is an important but previously overlooked methanogenic process in sediments for methylotrophic methanogens.

Asgard is a newly proposed archaeal superphylum, which has been suggested to hold the key to decipher the origin of Eukaryotes. However, their ecology remains largely unknown. Here, we conducted a meta-analysis of publicly available Asgard-associated 16S rRNA gene fragments, and found that just three previously proposed clades (Lokiarchaeota, Thorarchaeota, and Asgard clade 4) are widely distributed, whereas the other seven clades (phylum or class level) are restricted to the sediment biosphere. Asgard archaea, especially Loki- and Thorarchaeota, seem to adapt to marine sediments, and water depth (the depth of the sediment below water surface) and salinity might be crucial factors for the proportion of these microorganisms as revealed by multivariate regression analyses. However, the abundance of Asgard archaea exhibited distinct environmental drivers at the clade-level; for instance, the proportion of Asgard clade 4 was higher in less saline environments (salinity6.35 psu), while higher for Heimdallarchaeota-AAG and Asgard clade 2 in more saline environment (salinity ≥35 psu). Furthermore, co-occurrence analysis allowed us to find a significant non-random association of different Asgard clades with other groups (e.g., Lokiarchaeota with Deltaproteobacteria and Anaerolineae; Odinarchaeota with Bathyarchaeota), suggesting different interaction potentials among these clades. Overall, these findings reveal Asgard archaea as a ubiquitous group worldwide and provide initial insights into their ecological features on a global scale.

The genomes of two Rhodopirellula europaea strains were sequenced as permanent drafts to study the genomic diversity within this genus, especially in comparison with the closed genome of the type strain Rhodopirellula baltica SH1(T). The isolates are part of a larger study to infer the biogeography of Rhodopirellula species in European marine waters, as well as to amend the genus description of R. baltica. This genomics resource article is the second of a series of five publications describing a total of eight new permanent daft genomes of Rhodopirellula species.

The genomes of three Rhodopirellula baltica strains were sequenced as permanent drafts to complement the full genome sequence of the type strain R. baltica SH1 T . The isolates are part of a larger study to infer the biogeography of Rhodopirellula species in European marine waters, as well as to amend the genus description of R. baltica . This genomics resource article is the first of a series of five publications reporting in total eight new permanent daft genomes of Rhodopirellula species.

The genome of Rhodopirellula sallentina SM41 was sequenced as a permanent draft to supplement the full genome sequence of the type strain Rhodopirellula baltica SH1(T). This isolate is part of a larger study to gain insights into the biogeography of Rhodopirellula species in European marine waters, as well as to amend the genus description of R. baltica. This genomics resource article is the third of a series of five publications reporting in total eight new permanent daft genomes of Rhodopirellula species.