bioRxiv Science⌕ Search

Biology subjects

Lenstra, W. K.

Publications and source records attributed to Lenstra, W. K..

7 recordsLinked to original sources

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↗

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↗