Kuypers, Marcel

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Kuypers, Marcel

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Kuypers, Marcel

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Kuypers, Marcel M. M.

Kuypers, M. M. M.

Kuypers, M.

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Greenhouse gas cycling in the marine environment - from coast to open ocean
(2023-09-21)
von Arx, Jan Niccolo
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Frey, Claudia
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Kuypers, Marcel
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Milucka, Jana
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Kuypers, Marcel
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.
Dissertation
216 288
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The role of unicellular cyanobacteria in nitrogen fixation and assimilation in subtropical marine waters
(2013-10-02)
Krupke, Andreas
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Fuchs, Bernhard
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Kuypers, Marcel
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Kuypers, Marcel
Biological N2 fixation constitutes the major source of nitrogen in open ocean systems, regulating the marine nitrogen inventory and primary productivity. Symbiotic relationships between phytoplankton and N2 fixing microorganisms (diazotrophs) have been suggested to play a significant role in the ecology and biogeochemistry in these oceanic regions. The widely distributed, uncultured N2 fixing cyanobacterium UCYN A was suggested to live in symbiosis since it has unprecedented genome reduction, including the lack of genes encoding for oxygen evolving photosystem II and the tricarboxylic acid cycle. This thesis aims to study carbon and nitrogen metabolism on field populations of UCYN A using molecular biology, as well as mass spectrometry tools to visualize metabolic activity on a single cell scale. The development of a 16S rRNA oligonucleotide probe specifically targeting UCYN A cells and its successful application on environmental samples (Manuscript I and II) revealed a symbiotic partnership with a unicellular prymnesiophyte. We demonstrated a nutrient transfer in carbon and nitrogen compounds between these two partner cells, providing an explanation how these diazotrophs thrive in open ocean systems. Further, UCYN A can also associate with globally abundant calcifying prymnesiophyte members, e.g. Braarudosphaera bigelowii, indicating that this symbiosis might impact the efficiency of the biological carbon pump. In manuscript III, we provided quantitative information on the cellular abundance and distribution of UCYN A cells in the North Atlantic Ocean and identified the eukaryotic partner cell as Haptophyta (including prymnesiophyte) via double Catalyzed Reporter Deposition Fluorescence In Situ Hybridization (CARD FISH). The UCYN A Haptophyta association was the dominant form (87.0±6.1%) over free living UCYN A cells. Interestingly, we also detected UCYN A cells living in association with unknown eukaryotes and non calcifying Haptophyta cells, raising questions about the host specificity. During a follow up study (Manuscript IV), we conducted various nutrient amendment experiments (including iron, phosphorus, ammonium nitrate and Saharan Dust) in order to examine physiological interactions between individual UCYN A and Haptophyta cells. Single cell measurements using nanometer scale secondary ion mass spectrometry (nanoSIMS) revealed a tight physiological coupling in the transfer of carbon (R2 = 0.6232; n = 44) and nitrogen (R2 = 0.9659; n = 44) between host and symbiont. N2 fixation was mainly stimulated when iron rich Saharan Dust was added, emphasizing on aeolian dust deposition in seawater as a major parameter in constraining N2 fixation of UCYN A. Moreover, when fixed nitrogen species (ammonium and nitrate) were added, a third unknown microbial partner cell was observed within individual UCYN A Haptophyta associations, but their menaing is unclear. Based on this thesis work we revealed how UCYN A cells thrive in the environment and established a culture independent technique to assess the in situ activity in respect to CO2 and N2 fixation of this ecological relevant group of microorganisms. Furthermore, this unusual partnership between a cyanobacterium and a unicellular alga is a model for symbiosis and is analogous to plastid and organismal evolution, and if calcifying, may have important implications for past and present oceanic N2 fixation.
Dissertation
321 82
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Impacts and Importance of Ammonia- and Nitrite Oxidation in the Marine Nitrogen Cycle
(2014-03-27)
Fuessel, Jessika
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Daims, Holger
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Kuypers, Marcel
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Kuypers, Marcel
Nitrification produces the most abundant form of bioavailable nitrogen in the ocean, which is also a major electron acceptor in the oxidation of organic matter. The latter role of nitrate becomes crucial in the absence of oxygen. One major aim of this thesis is to investigate the role of nitrite oxidation in oxygen minimum zone (OMZ) N-cycling. Nitrite oxidation was detected throughout the Namibian OMZ and appears unaffected even by non-detectable oxygen levels. It could recycle up to 100% of reduced nitrate and thereby potentially reduce N-loss. The high abundance of nitrite oxidizing bacteria of the genus Nitrococcus can likely be explained by their versatile metabolism. While Nitrococcus grows chemolithoautotrophically in the presence of oxygen, it gains energy via organoheterotrophic nitrate reduction to nitrite and nitrous oxide in the absence of oxygen. In the oxygenated ocean of the Mauritanian upwelling ammonia- and nitrite oxidizers appeared to be associated with marine aggregates. An alternative source of nitrite was provided by nitrate reduction, which is likely facilitated by oxygen reduced microniches within marine aggregates.
Dissertation
516 213
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Viral regulation of nutrient assimilation by algae and prokaryotes
(2012-12-10)
Sheik, Abdul Rahiman
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Brussaard, Corina
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Kuypers, Marcel
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Kuypers, Marcel
Viruses are the most abundant entities in the ocean and represent a large portion of lifes genetic diversity. As mortality agents, viruses catalyze transformations of particulate matter to dissolved forms. This viral catalytic activity may influence the microbial community structure and affect the flow of critical elements in the sea. However, the extent to which viruses mediate bacterial diversity and biogeochemical processes is poorly studied. The current thesis, using a single cell approach, provides rare and novel insights in to how viral infections of algae influence host carbon assimilation. Furthermore this thesis details how cell lysis by viruses regulates the temporal bacterial community structure and their subsequent uptake of algal viral lysates. Chapter 2 shows how viruses impair the release of the star-like structures of virally infected Phaeocystis globosa cells. The independent application of high resolution single cells techniques using atomic force microscopy (AFM) visualized the unique host morphological feature due to viral infection and nanoSIMS imaging quantified the impact of viral infection on the host carbon assimilation. Prior to cell lysis, substantial amounts of newly produced viruses (~ 68%) were attached to P. globosa cells. The hypothesis that impediment of star-like structures in infected P. globosa cells leads to enhanced grazing was proposed. The scenario of enhanced grazing is in sharp contrast to the current view that viral infections divert the organic carbon transfer from higher trophic levels (e.g., grazers). In chapter 3, during early hours of viral infection, the application of secondary-ion mass spectrometry (nanoSIMS) showed a high transfer of infected P. globosa biomass towards Alteromonas cells well before the latent period, which stimulated its initial doubling in abundance, attachment to algal cell surroundings. Following algal viral lysis, the succession of bacterial populations consisted of Alteromonas and Roseobacter cells and an efficient transfer of P. globosa viral lysates by these specific bacterial members (Day 2). The sharp increase of these two genera, which occurred in aggregate-association, declined in abundance due to plausible phage mediated lysis. The potential phage mediated lysis appeared to result in aggregate dissolution and was responsible for regeneration of dissolved inorganic carbon (55% of the particulate 13C-organic carbon) and generation of plentiful recalcitrant organic carbon. The findings such as algal leakage during infection substantiate a previously undocumented role of viruses, which appears to be responsible for alterations in the marine ecosystem process such as bacterial community structure and carbon availability. In chapter 4, it appears that viral infection of Micromonas pusilla cells led to the hindrance of pyrenoid synthesis (starch and proteins) and much of the newly assimilated material was diverted towards viral production. Viral lysis of M. pusilla led to dominance of Alteromonas cells and Bacteroidetes, where as Alteromonas cells dominated the bacterial communities in non-infected cultures through out the experiment. The ecological implication of viral mediated starch impediment in M. pusilla cells may lead to the release of labile proteins and increased levels of polysaccharides, which potentially directs the marine pelagic system to more regenerative processes.
Dissertation
308 122
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Microscale insights into marine biogeochemical cycling: Linking microbial activity and mass transfer
(2023-11-20)
Jalaluddin, Farooq Moin
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Ploug, Helle
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Kuypers, Marcel
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Ahmerkamp, Soeren
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Kuypers, Marcel
Microbial transformations are fundamental drivers of biogeochemical cycling in marine environments. While larger-scale processes undoubtedly shape marine microbial communities, the life of individual microorganisms is intricately governed by processes occurring at a much smaller scale, ranging from micrometers to millimeters. At these scales, the solute concentration available to the microbial community is influenced by the interplay between transport processes and microbial metabolism. However, our current understanding of microbially mediated biogeochemical processes within such microenvironments is still limited. The aim of this thesis was to study the interplay of mass transfer and microbial reaction rates to determine how they govern biogeochemical cycling in microenvironments. To gain insights into these processes, microfluidic techniques were developed and combined with modeling studies to quantify and explore microscale transport processes. The study in chapter 2 aimed to assess the role of oxic sandy sediments in removing anthropogenic nitrogen inputs to the continental shelves by quantifying the contribution of anoxic microenvironments in nitrogen loss. We used oxygen sensitive sensor particles in a microfluidic device to map oxygen production and consumption rates on the surface of individual sand grains. The results showed significant variability in oxygen production and consumption rates on individual sand grain surfaces, suggesting the formation of distinct microenvironments. Integration of microfluidic data into a two-dimensional single sand grain model revealed that the formation of anoxic microenvironments is controlled by solute supply and microbial oxygen production and consumption rates. Subsequently, a non-dimensional number derived from the model was used to estimate the volumes of anoxic microenvironments and calculate associated nitrogen loss. The findings indicated that nitrogen loss in the North Sea could be underestimated by approximately 40%. To further investigate the impact of flow on microscale transport processes and activity within microenvironments, we utilized oxygen-sensitive sensor particles in conjunction with advanced imaging techniques to simultaneously visualize oxygen concentrations and flow fields (chapter 3). The method proved highly effective in non-invasively visualizing the microscale transport processes in the boundary layer, allowing us to visualize oxygen concentrations within and around a model laboratory aggregate. We further show how this novel approach can be used in other marine microenvironments, examining the exchange processes facilitated by cilia on corals. The results show the importance of flow in determining oxygen concentrations and the potential for different microbial metabolisms in marine microenvironments. The activity of microorganisms residing in distinct microenvironments was investigated in chapter 4 using a newly developed microfluidic device for cultivating cells under well-defined solute concentrations. By cultivating marine bacteria under controlled oxic and anoxic conditions, we observed variable growth rates attributed to different energy yields from aerobic respiration and fermentation. Automated image segmentation revealed delayed morphological adaptations in response to changing oxygen concentrations. This study emphasizes the diversity within the microbial community residing in different microenvironments. The combined findings from this thesis show that microbial activity and behavior within seemingly uniform environments are influenced by microscale gradients of solute resulting from mass transport and microbial reaction rates. The work presented in this thesis, through microfluidics, imaging techniques, and modeling studies, highlights the intricate interplay of solute transport and microbial reaction rates, ultimately determining the solute availability in microenvironments. Microbial activity within these distinct microenvironments likely plays a key role in biogeochemical cycling in the oceans.
Dissertation
244 196
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Microbial Oxidation of Methane in Aquatic Systems Illuminated by Functional Metagenomics
(2018-01-18)
Graf, Jon
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Wagner, Michael
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Kuypers, Marcel
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Kuypers, Marcel
Freshwater and marine environments are hotspots of methane cycling. Vast amounts of methane, a potent greenhouse gas, are produced predominantly in the sediments of these environments but very little eventually escapes to the atmosphere due to the activity of methane-oxidizing microorganisms. These microorganisms are pivotal in regulating methane emissions from the oceans and freshwater systems and their study therefore transcends scientific curiosity and is of global relevance to society as a whole. Despite their importance, the knowledge about these microorganisms is restricted to cultured isolates and little is known about the physiology of environmentally-relevant uncultured species. Using culture-independent functional metagenomics in combination with physiological experiments, this thesis aims to improve our understanding of the individual metabolic potential and activity that underlie the ecophysiology and environmental relevance of several uncultured methane-oxidizing microorganisms.
Dissertation
642 229
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Nitrogen Losses and Nutrient Regeneration in Oxygen Minimum Zones
(2012-07-27)
Kalvelage, Tim
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Bange, Hermann W.
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Kuypers, Marcel M. M.
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Kuypers, Marcel M. M.
In the tropical oceans, coastal upwelling of nutrient-rich deep waters fuels high surface productivity. The decomposition of sinking algal biomass results in the formation of large oxygen-deficient water bodies at mid depths (~100 1,000 m). Although, these oxygen minimum zones (OMZs) amount to <1% of the global ocean volume, they account for ~30-50% of total oceanic nitrogen (N) loss. Anammox, the anaerobic oxidation of NH4 with NO2- to gaseous N2 is the major N-loss pathway in OMZs. The recirculation of N-deficient waters to the surface limits phytoplankton growth and thus carbon sequestration in large parts of the tropical oceans. Continuing ocean de-oxygenation is expected to result in significantly increasing N-losses, thereby reducing the ocean s capacity to attenuate rising atmospheric CO2. This thesis aimed to determine regulatory effects of O2 and organic matter availability on anammox and N-linked processes in OMZs to facilitate model-based assessments of future ocean changes.
Dissertation
609 111
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Transformation processes of nitrogen, phosphorus and iron in sub-euphotic waters and surface sediments
(2013-11-20)
Sokoll, Sarah
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Zabel, Matthias
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Kuypers, Marcel M. M.
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Kuypers, Marcel M. M.
In the ocean, concentrations and ratios of nitrogen (N), phosphorus (P) and iron (Fe) determine primary production. In upwelling regions, nutrient-rich deep waters fuel this primary production. Knowledge of nutrient transformation processes in deep waters is still scarce. Therefore N-removal via denitrification and anaerobic ammonium oxidation (anammox) as well as P and Fe transformation processes were investigated. In the Arabian Sea up to 50% of N-loss was due to benthic N-removal, emphasizing the high potential of sediments to contribute to the N-deficit in the water column. In sandy permeable sediments off Mauritania, denitrification rates correlated with sediment grain size, indicating a strong relationship between benthic denitrification rates and advective porewater transport. On the shelf off Mauritania and Namibia, P-uptake was investigated in sub-euphotic waters and found to be largely biologically driven. In conclusion, transformation processes determine concentration and bioavailability of nutrients in the sub-euphotic water column and sediments and may eventually have an impact on the primary production in the surface ocean.
Dissertation
157 141
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Nitrogen cycling in coastal permeable sediments from eutrophied regions
(2014-03-27)
Marchant, Hannah
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Winter, Christian
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Kuypers, Marcel
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Kuypers, Marcel
Coastal seas buffer the ocean from anthropogenic pollution such as fixed nitrogen. Much of the coastal zones are comprised of sandy sediments, which are permeable. The interaction between sediment topography and bottom water movement causes advective flow of porewater in the sediment. This enhanced porewater supply leads to intense biogeochemical activity, removing nitrate and reducing it to inert N2. Therefore this work focuses on nitrogen cycling in coastal sands. It was possible to follow the fate of nitrate within the sediment, revealing the surprising importance of eukaryotes to N-loss. Furthermore, in subtidal sediments high rates of nitrification were identified, which coupled to high denitrification rates suggests that sandy sediments play an important role in mediating N-turnover in this region. The fluctuating oxygen and nutrient concentrations lead to an environment, which stimulates the occurrence of aerobic denitrification and allows for high nitrous oxide production, much of which is emitted to the atmosphere.
Dissertation
370 178
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Nitrogen loss from intertidal permeable Wadden Sea sediments
(2011-06-01)
Gao, Hang
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Kuypers, Marcel
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Hinrichs, Kai-Uwe
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Kuypers, Marcel
In the oceanic nitrogen (N) cycle, the sedimentary N2 production accounts for 50-70 % of global marine N-loss. Coastal regions or continental shelves, where terrestrial riverine systems and the oceansintersect, play a role as a significant N-sink in the marine N-cycle by regulating the fixed-N flow at the land-sea boundary. Although continental shelf sediments cover only 7.5 % of the global marine seafloor, they contribute> 60 % of benthic N-loss. The majority of the seafloor on continental shelves worldwide is covered by permeable sediments. Advection, instead of diffusion, is the predominant mass transport in these permeable sediments.The particle and solute exchanges between water column and sediments under advective conditions exceed those under diffusive conditionsby several orders of magnitude.Advective pore water flowsallow oxygen penetration to greater depths, expanding the biogeochemical oxic zone in permeable sediments. However,so far little is known about N-loss in these sediments, and the impacts of advection on N- loss and N-cycling processes in general. The aim of this thesis is to investigate the extent and mechanisms of N-loss in the Wadden Sea permeable sediments under simulated in situadvective conditions. Spatial and temporal N-loss rates were determined in order to assess the significance of the Wadden Sea permeable sediments, and furthermore these sediments from this worldwide tidal flat system were used as a case study to elucidate the role of permeable sediments in the global marine N-loss. Potential links between N-loss and other N-cycling processes such as nitrification are further explored, especially under the influence of fluctuating oxic-anoxic conditions. Using amodified core 15N-incubation method with one-pulseperfusion to simulate advections, and with simultaneous multiple-sensor measurements, active N-loss via denitrification was found to occur under oxic conditions. Such occurrence was further corroborated by slurry incubations with 15N-labelled substrates by O2microsensor measurement and on-line measurement using membrane inlet mass spectrometry (MIMS). These combined results show that permeable Wadden Sea sediments are characterized by some of the highest denitrification rates (190µmol Nm-2 h-1) under aerobic conditions (with oxygen concentrations of up to 90µM) in the marine environment.This is the first time that the substantial N-loss inpermeable sedimentshas been attributed to aerobic denitrification under oxic-anoxic oscillations driven by advection. To examine the significance of N-loss in permeable Wadden Sea sediments over an annual cycle, N-loss rates were determined across three seasons. The impacts of advection were also evaluated by comparing three incubation methods: (i) intact core incubations simulating diffusive transport, (ii) intact core incubations simulating advective transport conditions, or (iii) slurry incubations. Nitrogen loss ratesunder simulated advective conditions exceeded those under diffusive conditions by 1-2 orders of magnitude, and were comparable to rates determined in slurries. Intensive N loss rates (mean 207± 30 µmol m-2 h-1) were measured in permeable Wadden Sea sediments with little temporal and spatial variation. Furthermore, NOx- fluxes over a full annual cycle were empirically simulated by 2-dimensional model with in situ monitoring data as input parameters, includingtemperatures, bottom current velocities and NOx- concentrations in water column. Combined with actual rate measurements across seasons and sites, theannual N-loss in permeable Wadden Sea sediments was estimated to be 745 mmol N m-2 y-1. These results in the case study of the Wadden Sea verify that permeable sediments, accounting for up to 68 % of the continental shelves, are an important N-sink in the global marine N-cycle. The expansion of the oxic biogeochemical zone in permeable sediments due to advection may favor aerobic processes such as nitrification. Hence, the occurrence of nitrification and its interaction with N-loss processes in permeable Wadden Sea sediments were evaluated using 15N-isotope paring experiments.Net NOx- production was determined under aerobic conditions in these sediments, verifying the active occurrence of nitrification. In addition, the NOx- produced by nitrification could be immediately channeled to N-loss to produce N2. Instead of anammox(at very low rates of <2 µmol N m-2 h-1, and <1 %of total N-loss), aerobic denitrification predominated in these permeable sediments. Moreover, thecoupled nitrification-denitrificationwas found to represent up to 17 % to total N-loss, particularly apparent in surficial (permeable) sediments where the influence from advection was the strongest. This study provides direct and quantitative evidence that nitrification plays a keyrole in linking N-sourcesand N-sinksin permeableWadden Sea sediments.
Dissertation
516 98

Kuypers, Marcel

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