von Arx, Jan Niccolo

The consequences of global warming are omnipresent, especially with current record heat waves in Europe, North America and Asia. The natural greenhouse gas effect is essential for human life on Earth but anthropogenic activity increases greenhouse gas emissions and amplifies this warming effect. Global warming also has a significant impact on marine environments, making them more thermally stratified, acidic and oxygen-depleted, thereby disrupting the natural cycle of greenhouse gases. Methane and nitrous oxide (N2O) are important greenhouse gases with key functions in marine biogeochemistry and can be both formed and consumed by microbial activity. However, emerging discoveries regarding both methane and N2O highlight the need for further investigations of the underlying microbial transformations, as our understanding remains incomplete. For example, methane formation was thought to be a strictly anaerobic process until it has been shown to also occur in fully oxygenated environments, possibly by a plethora of microbial pathways. N2O formation and consumption is well documented, particularly in oxygen-limited environments but both coastal environments and oxygen-limited environments without significant N2O accumulation remain understudied. Thus understanding the physico-chemical driving factors of these greenhouse gas cycles and the underlying microbial activities and communities is vital for predicting the effects of continuous climate disruptions and the resulting consequences for the fluxes of these greenhouse gases to the atmosphere. To address some of these knowledge gaps, this thesis explored microbial methane and N2O cycling in different oceanic regions by combining extensive field measurements using stable isotope incubation experiments and molecular analyses to determine the underlying microbial pathways and controlling factors. Current research suggests that methylphosphonate (MPn) utilisation can lead to methane formation in oxygenated waters, especially in phosphate-limited environments, where the microbial community can use it as an alternative phosphorus source. In chapter II, we explored the extent of MPn-driven methane formation, using 13C-MPn, in the upper 200 metres of the western Tropical North Atlantic off Barbados and the microbial community and controlling factors behind their activity. We show that MPn was a major methane precursor, with the highest methane formation found in the surface waters above the deep chlorophyll maximum. Interestingly, methane formation was detected even in the presence of phosphate, a more energetic phosphorus source, suggesting that MPn-driven methane formation may extend into more phosphate replete environments. Phylogenetic analysis of the phnJ, the marker gene for MPn-driven methane formation, identified a diverse microbial community. Alphaproteobacteria generally dominated the microbial community possessing the phnJ gene, whereas the cyanobacterium Trichodesmium was most abundant in the surface waters. Our results suggest there is a link between primary productivity and methane formation and we conclude that phosphonates, including MPn, could account for 11% of the phosphorus requirement of primary producers in the surface waters. In chapter III we investigated N2O cycling in the suboxic zone of the Black Sea. Despite harbouring a massive oxygen-limited water column, the Black Sea is only considered to be a minor source of N2O to the atmosphere. It has been suggested previously that there is an active N2O cycle in the suboxic zone but the pathways and microbial community responsible remain poorly constrained. We used 15N-based stable isotope incubation experiments to identify the main pathways of N2O formation (aerobic ammonia oxidation and denitrification) and consumption. We were able to demonstrate that aerobic ammonia oxidation led to small but persistent rates in contrast to nitrite reduction which led to sporadic but explosive rates of N2O formation. The latter were especially amplified in the presence of sulphide, suggesting chemolithotrophic denitrification took place. Despite these high rates, N2O reduction could outpace its formation, suggesting a balance within the suboxic zone being responsible for the lack of N2O accumulation. Phylogenetic analysis of the amoA, the marker gene for ammonia oxidation, revealed that the Nitrososphaerales were dominant. Analysis of denitrification genes revealed a diverse community which included denitrifiers of the Gammaproteobacteria and potential N2O reducing specialists of the Marinisomatales. All of these denitrifiers belonged to groups previously associated with sulphur cycling. Therefore, we could demonstrate that despite the lack of N2O accumulation in the water column, there is an active but well-balanced microbial N2O cycle. Finally, in chapter IV we investigated N2O cycling in the Peruvian oxygen minimum zone (OMZ), the single largest marine source of N2O to the atmosphere. We investigated the shallow (< 100 metres water depth) OMZ using 15N-based stable isotope incubation experiments to identify the main microbial processes of N2O cycling. The water column seemed to be highly dynamic with oxygen measurements suggesting oxygen intrusions into the OMZ. Rate measurements showed that aerobic ammonia oxidation was a minor but persistent source of N2O, with denitrification from both nitrite and nitrate dominating. However, N2O reduction rates exceeded the combined formation rates from all sources. Therefore, these results suggest that there is the capacity for a microbial N2O filter to prevent N2O accumulation. However, this is likely mitigated by the dynamic nature of the environment, thereby making the coastal OMZ an important source of N2O. Combined these chapters give new insights into methane and N2O cycling in understudied marine environments and pose new and exciting questions for future research.

The R/V POSEIDON cruise POS539 took place in the northwestern basin of the Black Sea (42°30’N to 44°N and 29°E to 31°E). The overarching aim of the campaign was to obtain sediment and water samples, including suspended particle material, from the various redox zones of the Black Sea. The campaign lasted between November 6th and November 21st 2019 and the collected samples were taken in order to investigate the activity and physiology of microorganisms involved in the conversion of nitrogen compounds and degradation of organic carbon under various oxygen conditions. The main topics of the cruise were: (a) to quantify the contribution of archaeal nitrifiers to the nitrogen and carbon cycles, b) to measure the production and consumption of the powerful greenhouse gases CH4 and N2O, c) to record palaeoenvironmental changes in high resolution, and d) to describe the complexity and identity of biopolymers. For this, water and sediment samples were retrieved from 10 discrete shelf and slope stations. First, ‘deep water’ transect was conducted, which included three stations with water depths over 2000 m. The second perpendicular transect encompassed stations that gradually transitioned from the deep parts of the slope towards the shelf (ca. 80 m depth). Additionally, two stations were setup north and south of the shelf transect, respectively, for paleoceanographic studies. Throughout the cruise the weather conditions were overwhelmingly good, only towards the end of the campaign gusty winds of 7 Bft were recorded. The recorded oceanographic conditions were in agreement with the expected water properties at all stations. Station activities were completed on November 20th at 14:00 local board time. On November 21st at 10:30 local time, R/V POSEIDON reached the port of Varna, Bulgaria, thus concluding the POS539 expedition. Analyses and results from the samples and experiments will provide a basis for our understanding of the microbial control on the carbon and nitrogen cycle of the Black Sea.

von Arx, Jan Niccolo

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