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Slomp, C. P.

Publications and source records attributed to Slomp, C. P..

13 recordsLinked to original sources

ANME-2a drive methane oxidation in brackish coastal sediments via multiple pathways

Methane is a powerful greenhouse gas. Typically, a large fraction of the methane formed in coastal sediments is removed via anaerobic methane oxidation (AOM). Here, we demonstrate the potential for a range of AOM pathways in brackish coastal sediments by ANME-2a archaea. At our study site, geochemical profiles indicate that AOM is primarily restricted to a shallow, metal-oxide-rich sulfate-methane transition zone (SMTZ). ANME-2a were the sole methanotrophs detected, and metatranscriptomics showed the highest expression levels of the ANME-2a genes in the SMTZ. AOM activity was observed in sediment incubations with various electron acceptors, including sulfate, metal oxides, and the organic matter analogue graphene oxide. Highest potential rates were observed in sediments from below the SMTZ, pointing towards fast stimulation of the deeper methanotrophic community when alleviating the electron acceptor limitation. The variety of AOM pathways and persistence of methanotrophs below the SMTZ likely contribute to the resilience of the microbial methane filter in brackish coastal sediments.

microbiology↗

Potential for metal-coupled methane oxidation by Candidatus Methanocomedenaceae in coastal sediments

Anaerobic methanotrophic (ANME) archaea are important players in the microbial methane cycle, mitigating methane emissions from anoxic environments. ANME are found ubiquitously in methane-rich sediments, where they can couple anaerobic methane oxidation (AOM) to different electron acceptors such as sulfate, metal oxides, and natural organic matter (NOM). However, we still lack understanding of the geochemical niches and preferred metabolic pathways of most ANME subclades. Here, we investigated the genomic potential and ecophysiology of ANME-2a with respect to metal-dependent AOM in brackish metal-rich coastal sediments. We assembled several high-quality ANME MAGs from subclades with high strain heterogeneity and analyzed the genomic potential for metal-AOM. Additionally, we monitored long-term enrichments with various electron acceptors from the same sediments. Ultimately, we recovered 8 novel genomes of ANME-2a that clustered with an uncharacterized genus with only 2 representatives in public databases for which we propose the name Candidatus Methanoborealis. The analysis of the MAGs showed two different clusters within this genus; one comprising of MAGs from the Baltic Sea that showed high potential for extracellular electron transfer (EET) required for metal-AOM, and another cluster form more diverse environments with less EET potential. The Baltic Sea Ca. Methanoborealis were the only canonical methanotrophs in the incubations during active methane oxidation and metal reduction. Our results contribute to the understanding of the phylogenomic and metabolic diversity in ANME subclades, which will help to further characterize novel ANME lineages from complex sediment samples.

microbiology↗

Coastal sediments maintain potential for N2O cycling under seasonally varying redox conditions

Coastal eutrophication can lead to deoxygenation and sulfide accumulation in sediments, which could strongly impact the dynamics of the potent greenhouse gas nitrous oxide (N2O). Here, we investigated the effects of oxygen (O2) and sulfide on microbial N2O production and consumption in surface sediments of a seasonally euxinic (anoxic and sulfidic) coastal basin. In spring, these surface sediments are oxygenated, while they are highly sulfidic during stratification of the water column in summer. During oxygenated spring conditions, rapid depletion of the substrates O2 and nitrate (NO3-) in the surface sediment limited net in situ N2O production, despite potential for nitrification and for N2O production through incomplete denitrification as observed in batch incubations. Based on metagenome and metatranscriptome analyses the N2O-consuming microbial community was shown to be highly diverse and dominated by clade II nosZ-possessing Flavobacteriia. Assessing the summer sulfidic conditions in surface sediments via batch incubations, we found that moderate sulfide concentrations (0.2-1 mM) enhanced N2O consumption, whereas high concentrations (4 mM) inhibited all steps of denitrification. These findings highlight the redox controls on N2O dynamics, by indicating that coastal sediments can maintain significant N2O turnover potential despite substrate limitations and elevated sulfide concentrations. Consequently, ecosystem restoration strategies that alter O2, NO3- and sulfide availability may fundamentally impact coastal N2O budgets.

microbiology↗

Long-term euxinia hinders microbial ammonium removal in brackish coastal waters

Anthropogenic activities are key drivers of eutrophication and deoxygenation in coastal marine ecosystems. This stimulates the anaerobic degradation of organic matter and the release of reduced products, such as ammonium, methane, and hydrogen sulfide, which may, in turn, exacerbate eutrophication and deoxygenation. In this study, using a combination of chemical and microbial analyses, we assess the nitrogen dynamics in the water column of a eutrophic coastal system (Stockholm Archipelago) at three sites with contrasting redox conditions (oxic to long-term euxinic). At the oxic site, counter gradients of ammonium and oxygen in the water column, low nitrate {delta}15N values in bottom waters, and the 16S rRNA gene-based presence of nitrifiers indicate nitrification near the sediment-water interface. At the seasonally and long-term euxinic sites, nitrification, as inferred from the water column oxygen and nutrient profiles and the relative abundance of nitrifiers, primarily occurred near the oxycline. At these two sites, nitrate was removed below the oxycline through denitrification linked to sulfide oxidation by Sulfurimonas. Nitrous oxide emissions from surface waters in the archipelago reached up to 40 {micro}mol m-2 d-1 and were not directly related to water column redox conditions, indicating that multiple factors control coastal emissions of this greenhouse gas to the atmosphere. The relative abundance of 16S rRNA genes and of N-cycle genes in metagenomes was highest at the seasonally euxinic site. Importantly, nitrifiers were significantly less abundant at the long-term euxinic site. Our results highlight that prolonged euxinia promotes recycling of ammonium over its removal, likely due to sulfide inhibition of nitrification, which sustains eutrophication and deoxygenation of coastal systems.

microbiology↗

Seasonal dynamics of nitrification in the water column of marine Lake Grevelingen

Coastal ecosystems serve as vital connectors between land and ocean, and their nitrogen cycle and ammonium removal can be affected by various factors. During our seasonal sampling campaign in 2021, the eutrophic marine Lake Grevelingen exhibited high ammonium concentrations and low nitrification rates in the water column, except for a brief period in late summer. Our study revealed ammonium accumulation in the anoxic middle and bottom water layers due to restricted transport caused by water column stratification. Only when ammonium reached the oxic part of the water column, was a short-lived peak in nitrification activity and nitrifier abundance observed at the end of August. Amplicon sequencing indicated very low abundances of Nitrosococcus and Nitrospira (<0.2%) in March, while Nitrosomonas and Nitrospina peaked at the end of August with relative abundances of 2.5% and 1.3%, respectively. Archaea and archaeal ammonium oxidizers were found in very low abundances. Anammox 16S rRNA genes were not detected. Together, these observations suggest a limited role for nitrification in ammonium removal in marine Lake Grevelingen.

microbiology↗

Sediments from a seasonally euxinic coastal ecosystem show high nitrogen cycling potential

Coastal ecosystems are susceptible to eutrophication and deoxygenation, which may alter their nitrogen cycle dynamics. Here, we investigated the microbial nitrogen cycling potential in the sediment of a seasonally euxinic coastal ecosystem (Lake Grevelingen, NL), in winter and summer. Porewater profiles showed ammonium (NH4+) concentrations exceeding 10 mM and rapid depletion of electron acceptors with depth. Activity tests revealed NH4+ oxidation potential up to 53 {micro}mol g-1 day-1, even in anoxic sediment layers. A nitrifying microbial community was present in both oxic and anoxic sediment sections (up to 1.4% relative abundance). NO-, nitrite (NO2-) and nitrous oxide (N2O) reduction potential were prominent across all sediment sections, with the highest rates (167 {micro}mol NO3- g-1 day-1) in the surface sediment in summer. Denitrification (79.3-98.4%) and dissimilatory nitrate reduction to ammonium (DNRA; 1.6-20.7%) were the major NO3- removal pathways, as supported by the detection of the narG/napA, nirK/nirS, norB, nosZ and nrfA/otr genes in all sediment sections. The DNRA contribution increased with depth and with the addition of electron donors, such as monomethylamine. Anaerobic ammonium oxidation (anammox) was not detected in these eutrophic sediments. Combined, our results show that there is high potential for nitrogen removal in eutrophic coastal ecosystems which may help further restoration measures.

microbiology↗

Metagenomic analysis of age-dependent microbial dynamics in dual-media rapid sand filters treating groundwater

Biofiltration using rapid sand filters is an often used and highly effective method to produce drinking water from anoxic groundwater, yet the microbial processes underlying contaminant removal remain poorly understood. This study used metagenomic sequencing to analyze the microbial communities of dual-media filters of varying ages, yielding 34 high-quality and 177 medium-quality metagenome-assembled genomes (MAGs), including 102 MAGs harboring genes involved in methane, iron or manganese oxidation, and nitrification. Methanotrophic bacteria from the Methylomonadaceae family were abundant in both the youngest and oldest anthracite layers. The dominant methanotroph shifted from a MAG possessing both soluble and particulate methane monooxygenases in the two-month-old filters to MAGs only containing particulate methane monooxygenases in older filters, possibly due to changes in copper availability. Iron oxidation was restricted to the anthracite layer and linked predominantly to Gallionella, which encoded cluster 1 outer membrane cytochromes Cyc2. Gallionella MAGs also became more abundant with filter age, indicating increasing relevance of biological iron oxidation in mature filters. The nitrifying community was dominated by Nitrosomonas and Candidatus Nitrotoga in the two-month-old filter, with the latter being replaced by Nitrospira as the most abundant NOB in older filters. Canonical Nitrospira far exceeded comammox Nitrospira in abundance, except in the oldest sand layers. These results challenge the previously posed assumption that Nitrospira dominance in rapid sand filters is primarily due to comammox activity. Furthermore, it indicates that long operational times are required for comammox Nitrospira to achieve significant abundance. Intriguingly, Nitrospira MAGs contained multi-copper oxidase-type putative manganese oxidases and cluster 3 cyc2 genes. Phylogenetic analysis could not conclusively link the Nitrospira Cyc2 to iron or manganese oxidation, warranting further study of their role in the removal of these compounds. Overall, these findings reveal dynamic, age-dependent changes in microbial communities and their functions within rapid sand filters, offering new targets for physiological studies of bacteria involved in contaminant removal from anoxic groundwater during drinking water production. HIGHLIGHTSO_LIMethanotrophic community shifts between young and mature rapid sand filters. C_LIO_LICluster 1 Cyc2-encoding Gallionella mediate biological iron oxidation. C_LIO_LICandidatus Nitrotoga and Nitrosomonas dominate nitrification in young filters. C_LIO_LIComammox Nitrospira become abundant after prolonged operational periods. C_LIO_LICanonical Nitrospira, not comammox, constitute high Nitrospira abundances. C_LIO_LIAbundant cluster 3 Cyc2-containing Nitrospira might catalyze metal oxidation. C_LI

microbiology↗

A ubiquitous and diverse methanogenic community drives microbial methane cycling in eutrophic coastal sediments

Coastal areas are responsible for over 75% of global marine methane emissions and this proportion is predicted to grow due to an increase in anthropogenically induced eutrophication and deoxygenation. Prolonged periods of low oxygen and high organic matter input have been put forward to cause an imbalanced microbial methane cycle, as methane oxidation cannot keep up with methane production. However, it is still unclear what factors affect each process and which microorganisms are responsible. Here we show that methanogenic processes dominate microbial methane cycling in the anoxic sediments of marine Lake Grevelingen (NL) after summer stratification with bottom water anoxia. We observed a shallow and narrow sulfate-methane transition zone between 5 and 15 cm depth, with high methane concentrations (> 5 mM) below this zone. Methanogenesis was dominant over methanotrophy in all investigated layers as active methanogenesis potential was detected down to 60 cm below sea floor, but methane oxidation was only observed in a narrow section of the sulfate-methane transition zone. Based on amplicon sequencing and sediment incubations, we uncovered a metabolically and phylogenetically diverse methanogenic community with distinct niche separation in different sediment layers. ANME archaea and their putative syntrophic sulfate-reducing bacteria were restricted to a narrow zone and were co-occurring with the detected methane oxidation activity. Our results suggest that eutrophication and deoxygenation will further contribute to rising methane emissions in coastal areas, as the microbial methane cycle will be tilted towards increased methanogenesis while the efficiency of the microbial methane filter is expected to decline.

microbiology↗

Seasonal dynamics of the microbial methane filter in the water column of a eutrophic coastal basin

In the water column of coastal waters, methane-oxidizing bacteria (MOB) can form a methane biofilter. This filter can counteract high benthic methane fluxes and thereby lower methane emissions to the atmosphere. Recent metagenomic studies revealed that the metabolism of the MOB in the filter is versatile, and could quickly respond to changing oxygen concentrations. Changes in oxygen availability in coastal basins are largely driven by seasonal stratification and mixing. However, it is still unclear how well the methane biofilter functions throughout the seasons, and how this relates to MOB community composition. Here, we determined water column methane and oxygen depth profiles and the methanotrophic community structure, methane oxidation potential, and methane fluxes of the Scharendijke basin in marine Lake Grevelingen between March and October 2021. In this period, the methane filter mainly consisted of three MOB belonging to Methylomonadaceae. Although in low relative abundance, the methanotrophic community was present in the mixed water column in March and had increased to 9 % by July in the stratified water column, with a distinct vertical niche partitioning in the redoxcline. The methane and oxygen gradients were vertically decoupled in summer upon the formation of a suboxic zone. Surprisingly, this did not affect the vertical distribution or potential methane oxidation of MOB. Moreover, water-air fluxes remained below 0.6 mmol m-2 day-1. Our findings suggest active methane removal by MOB in virtually anoxic water. Weakening of the stratification in September resulted in higher diffusive methane fluxes to the atmosphere (up to 1.6 mmol m-2 day-1). This was likely due to a faster supply of methane, but also a reduction of methane oxidation. Thus, despite the rapid adaptation and versatile genomic potential of the MOB community, seasonal water column dynamics significantly influence methane removal efficiency.

microbiology↗

Versatile methanotrophs form an active methane biofilter in the oxycline of a seasonally stratified coastal basin

The potential and drivers of microbial methane removal in the water column of seasonally stratified coastal ecosystems and the importance of the methanotrophic community composition for ecosystem functioning are not well explored. Here, we combined depth profiles of oxygen and methane with 16S rRNA gene amplicon sequencing, metagenomics, and methane oxidation rates at discrete depths in a stratified coastal marine system (Lake Grevelingen, The Netherlands). Three amplicon sequence variants (ASVs) belonging to different genera of aerobic Methylomonadaceae and the corresponding three methanotrophic metagenome-assembled genomes (MOB-MAGs) were retrieved by 16S rRNA sequencing and metagenomic analysis respectively. The abundances of the different methanotrophic ASVs and MOB-MAGs peaked at different depths along the methane oxygen counter-gradient and the MOB-MAGs show a quite diverse genomic potential regarding oxygen metabolism, partial denitrification, and sulfur metabolism. Moreover, potential aerobic methane oxidation rates indicated high methanotrophic activity throughout the methane oxygen counter-gradient, even at depths with low in situ methane or oxygen concentration. This suggests that niche-partitioning with high genomic versatility of the present Methylomonadaceae might contribute to the functional resilience of the methanotrophic community and ultimately the efficiency of methane removal in the stratified water column of marine Lake Grevelingen.

microbiology↗

Sulfide toxicity as key control on anaerobic oxidation of methane in eutrophic coastal sediments

Coastal zones account for significant global marine methane emissions to the atmosphere. In coastal ecosystems, the tight balance between microbial methane production and oxidation in sediments prevents most methane from escaping to the water column. Anthropogenic activities, causing eutrophication and bottom water deoxygenation, could disrupt this balance in the microbial methane cycle and lead to increased methane release from coastal sediments. Here, we combined microbiological and biogeochemical analyses of sediments from three sites along a bottom water redox gradient (oxic-hypoxic-euxinic) in the eutrophic Stockholm Archipelago to investigate the impact of anthropogenically-induced redox shifts on microbial methane cycling. At both the hypoxic and euxinic site, sediments displayed a stronger depletion of terminal electron acceptors at depth and a shoaling of the sulfate-methane transition zone in comparison to the oxic site. Porewater methane and sulfide concentrations and potential methane production rates were also higher at the hypoxic and euxinic site. Analyses of metagenome-assembled genomes and 16S rRNA gene profiling indicated that methanogens became more abundant at the hypoxic and euxinic site, while anaerobic methane-oxidizing archaea (ANME), present in low coverage at the oxic site, increased at the hypoxic site but virtually disappeared at the euxinic site. A 98% complete genome of an ANME-2b Ca. Methanomarinus archaeon had genes encoding a complete reverse methanogenesis pathway, several multiheme cytochromes, and a sulfite reductase predicted to detoxify sulfite. Based on these results, we infer that sulfide exposure at the euxinic site led to toxicity in ANME, which, despite the abundance of substrates at this site, could no longer thrive. These mechanistic insights imply that the development of euxinia, driven by eutrophication, could disrupt the coastal methane biofilter, leading to increased benthic methane release and potential increased methane emissions from coastal zones to the atmosphere.

microbiology↗

Metagenomic analysis reveals large potential for carbon, nitrogen and sulfur cycling in coastal methanic sediments of the Bothnian Sea

The Bothnian Sea is an oligotrophic brackish basin characterized by low salinity and high concentrations of reactive iron, methane and ammonium in the sediments potentially enabling an intricate microbial network. Therefore, we analyzed and compared biogeochemical and microbial profiles at one offshore and two near coastal sites in the Bothnian Sea. 16S rRNA amplicon sequence analysis revealed stratification of both bacterial and archaeal taxa in accordance with the geochemical gradients of iron, sulfate and methane. The communities at the two near coastal sites were more similar to each other than that at the offshore site located at a greater water depth. To obtain insights into the metabolic networks within the iron-rich methanic sediment layer located below the sulfate-methane transition zone (SMTZ), we performed metagenomic sequencing of sediment-derived DNA. Genome bins retrieved from the most abundant bacterial and archaeal community members revealed a broad potential for respiratory sulfur metabolism via partially reduced sulfur species. Nitrogen cycling was dominated by reductive processes via a truncated denitrification pathway encoded exclusively by bacterial lineages. Gene-centric fermentative metabolism analysis indicated the central role of acetate, formate, alcohols and hydrogen in the analyzed anaerobic sediment. Methanogenic/-trophic pathways were dominated by Methanosaetaceae, Methanosarcinaceae, Methanomassiliicoccaceae, Methanoregulaceae and ANME-2 archaea. Thorarchaeota and Bathyarchaeota encoded pathways for acetogenesis. Our results indicate flexible metabolic capabilities of core community bacterial and archaeal taxa, which can adapt to changing redox conditions, and with a spatial distribution in Bothnian Sea sediments that is likely governed by the quality of available organic substrates.

ecology↗

Exchange catalysis during anaerobic methanotrophy revealed by 12CH2D2 & 13CH3D in methane

The anaerobic oxidation of methane (AOM) is a crucial component of the methane cycle, but its enzymatic versatility under environmental conditions remains poorly understood. We use sediment samples collected during IODP Expedition 347 to the Baltic Sea to show that relative abundances of 12CH2D2 and 13CH3D molecules in methane gas trace the reversibility of methyl-coenzyme M reductase during AOM by driving methane towards internal, thermodynamic isotopic equilibrium. These data suggest that 12CH2D2 and 13CH3D together can identify the influence of methanotrophy in environments where conventional bulk isotope ratios are ambiguous, and these findings may lead to new insights regarding the global significance of enzymatic back-flux in the methane cycle.

biochemistry↗