Droevendaalsesteeg 10
6708 PB Wageningen
The Netherlands
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About
I foresee that a deep understanding of soil microbial communities will allow us to predict and even steer their activity to benefit crops and the environment
Biography
Microorganisms are responsible for decomposing plant material in soil, which makes them central players in greenhouse gas production, soil carbon storage, and recycling of plant nutrients. My research targets the ecological mechanisms of these processes. In particular, I aim to understand how viruses (bacteriophages) shape bacterial communities and redirect the flow of carbon and plant nutrients between plants, soil and atmosphere. This focus fits within the broader goal of understanding soil microbial lifestyles and their interactions with agricultural practice. I study these ecological mechanisms in realistic soil systems using a variety of chemical, stable isotope and molecular tools.
Research groups
Dossier
Carbon storage in natureCV
Employment
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2010–2014The Green House, Cape Town, South Africa, Environmental sustainability consultant
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2015–2018University of Goettingen, Department of Agricultural Soil Science, PhD candidate
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2018–2021Netherlands Institute of Ecology, Department of Terrestrial Ecology, Post-doctoral researcher
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2021–PresentNetherlands Institute of Ecology, Department of Terrestrial Ecology, Junior group leader
Ancillary activities
Publications
Key publications
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Microbial storage and its implications for soil ecology
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T4-like phages reveal the potential role of viruses in soil organic matter mineralization
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Intracellular storage reduces stoichiometric imbalances in soil microbial biomass – A theoretical exploration
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Viruses in soil: Nano-scale undead drivers of microbial life, biogeochemical turnover and ecosystem functions
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Contrasting effects of organic and mineral nitrogen challenge the N-Mining Hypothesis for soil organic matter priming.
Peer-reviewed publications
Meeting report: The first soil viral workshop 2022
Soil viral ecology is a growing research field; however, the state of knowledge still lags behind that of aquatic systems. Therefore, to facilitate progress, the first Soil Viral Workshop was held to encourage international scientific discussion and collaboration, suggest guidelines for future research, and establish soil viral research as a concrete research area. The workshop took place at Søminestationen, Denmark, between 15 and 17th of June 2022. The meeting was primarily held in person, but the sessions were also streamed online. The workshop was attended by 23 researchers from ten different countries and from a wide range of subfields and career stages. Eleven talks were presented, followed by discussions revolving around three major topics: viral genomics, virus-host interactions, and viruses in the soil food web. The main take-home messages and suggestions from the discussions are summarized in this report.https://doi.org/10.1016/j.virusres.2023.199121Intracellular carbon storage by microorganisms is an overlooked pathway of biomass growth
The concept of biomass growth is central to microbial carbon (C) cycling and ecosystem nutrient turnover. Microbial biomass is usually assumed to grow by cellular replication, despite microorganisms’ capacity to increase biomass by synthesizing storage compounds. Resource investment in storage allows microbes to decouple their metabolic activity from immediate resource supply, supporting more diverse microbial responses to environmental changes. Here we show that microbial C storage in the form of triacylglycerides (TAGs) and polyhydroxybutyrate (PHB) contributes significantly to the formation of new biomass, i.e. growth, under contrasting conditions of C availability and complementary nutrient supply in soil. Together these compounds can comprise a C pool 0.19 ± 0.03 to 0.46 ± 0.08 times as large as extractable soil microbial biomass and reveal up to 279 ± 72% more biomass growth than observed by a DNA-based method alone. Even under C limitation, storage represented an additional 16–96% incorporation of added C into microbial biomass. These findings encourage greater recognition of storage synthesis as a key pathway of biomass growth and an underlying mechanism for resistance and resilience of microbial communities facing environmental change.https://doi.org/10.1038/s41467-023-37713-4Environmental refuges from disease in host‐parasite interactions under global change
The physiological performance of organisms depends on their environmental context, resulting in performance–response curves along environmental gradients. Parasite performance–response curves are generally expected to be broader than those of their hosts due to shorter generation times and hence faster adaptation. However, certain environmental conditions may limit parasite performance more than that of the host, thereby providing an environmental refuge from disease. Thermal disease refuges have been extensively studied in response to climate warming, but other environmental factors may also provide environmental disease refuges which, in turn, respond to global change. Here, we (1) showcase laboratory and natural examples of refuges from parasites along various environmental gradients, and (2) provide hypotheses on how global environmental change may affect these refuges. We strive to synthesize knowledge on potential environmental disease refuges along different environmental gradients including salinity and nutrients, in both natural and food-production systems. Although scaling up from single host–parasite relationships along one environmental gradient to their interaction outcome in the full complexity of natural environments remains difficult, integrating host and parasite performance–response can serve to formulate testable hypotheses about the variability in parasitism outcomes and the occurrence of environmental disease refuges under current and future environmental conditions.https://doi.org/10.1002/ecy.4001Formation of necromass-derived soil organic carbon determined by microbial death pathways
Soil organic matter is the dominant carbon pool in terrestrial ecosystems, and its management is of increasing policy relevance. Soil microbes are the main drivers of soil organic carbon sequestration, especially through accumulation of their necromass. However, since the direct characterization of microbial necromass in soil is challenging, its composition and formation remain unresolved. Here we provide evidence that microbial death pathways (the distinct processes of microbial dying) in soil affect necromass composition and its subsequent fate. Importantly, the composition of derived microbial necromass does not equal that of microbial biomass. From biomass to necromass, distinct chemical transformations lead to increases in cell wall/cytoplasm ratios while nutrient contents and easily degradable compounds are depleted. The exact changes depend on environmental conditions and the relevance of different microbial death pathways, for example, predation, starvation or anthropogenic stresses. This has far-reaching consequences for mechanisms underpinning biogeochemical processes: (1) the quantity and persistence of microbial necromass is governed by microbial death pathways, not only the initial biomass composition; (2) efficient recycling of nutrients within microbial biomass presents a possible pathway of organic carbon sequestration that minimizes nitrogen losses; (3) human-induced disturbances affect the causes of microbial death and consequently necromass composition. Thus, new research focusing on microbial death pathways holds great potential to improve management strategies for soil organic carbon storage. Not only microbial growth but also death drive the soil microbial carbon pump.https://doi.org/10.1038/s41561-022-01100-3Experimental evidence for the impact of phages on mineralization of soil-derived dissolved organic matter under different temperature regimes
https://doi.org/10.1016/j.scitotenv.2022.157517Microbial mineralization of dissolved organic matter (DOM) plays an important role in regulating C and nutrient cycling. Viruses are the most abundant biological agents on Earth, but their effect on the density and activity of soil microorganisms and, consequently, on mineralization of DOM under different temperatures remains poorly understood. To assess the impact of viruses on DOM mineralization, we added soil phage concentrate (active vs. inactive phage control) to four DOM extracts containing inoculated microbial communities and incubated them at 18 °C and 23 °C for 32 days. Infection with active phages generally decreased DOM mineralization at day one and showed accelerated DOM mineralization later (especially from day 5 to 15) compared to that with the inactivated phages. Overall, phage infection increased the microbially driven CO2 release. Notably, while higher temperature increased the total CO2 release, the cumulative CO2 release induced by phage infection (difference between active phages and inactivated control) was not affected. However, higher temperatures advanced the response time of the phages but shortening its active period. Our findings suggest that bacterial predation by phages can significantly affect soil DOM mineralization. Therefore, higher temperatures may accelerate host-phage interactions and thus, the duration of C recycling.
Microbial functional changes mark irreversible course of Tibetan grassland degradation
The Tibetan Plateau’s Kobresia pastures store 2.5% of the world’s soil organic carbon (SOC). Climate change and overgrazing render their topsoils vulnerable to degradation, with SOC stocks declining by 42% and nitrogen (N) by 33% at severely degraded sites. We resolved these losses into erosion accounting for two-thirds, and decreased carbon (C) input and increased SOC mineralization accounting for the other third, and confirmed these results by comparison with a meta-analysis of 594 observations. The microbial community responded to the degradation through altered taxonomic composition and enzymatic activities. Hydrolytic enzyme activities were reduced, while degradation of the remaining recalcitrant soil organic matter by oxidative enzymes was accelerated, demonstrating a severe shift in microbial functioning. This may irreversibly alter the world´s largest alpine pastoral ecosystem by diminishing its C sink function and nutrient cycling dynamics, negatively impacting local food security, regional water quality and climate.https://doi.org/10.1038/s41467-022-30047-7Biogels in Soils: Plant Mucilage as a Biofilm Matrix That Shapes the Rhizosphere Microbial Habitat
Mucilage is a gelatinous high-molecular-weight substance produced by almost all plants, serving numerous functions for plant and soil. To date, research has mainly focused on hydraulic and physical functions of mucilage in the rhizosphere. Studies on the relevance of mucilage as a microbial habitat are scarce. Extracellular polymeric substances (EPS) are similarly gelatinous high-molecular-weight substances produced by microorganisms. EPS support the establishment of microbial assemblages in soils, mainly through providing a moist environment, a protective barrier, and serving as carbon and nutrient sources. We propose that mucilage shares physical and chemical properties with EPS, functioning similarly as a biofilm matrix covering a large extent of the rhizosphere. Our analyses found no evidence of consistent differences in viscosity and surface tension between EPS and mucilage, these being important physical properties. With regard to chemical composition, polysaccharide, protein, neutral monosaccharide, and uronic acid composition also showed no consistent differences between these biogels. Our analyses and literature review suggest that all major functions known for EPS and required for biofilm formation are also provided by mucilage, offering a protected habitat optimized for nutrient mobilization. Mucilage enables high rhizo-microbial abundance and activity by functioning as carbon and nutrient source. We suggest that the role of mucilage as a biofilm matrix has been underestimated, and should be considered in conceptual models of the rhizosphere.https://doi.org/10.3389/fpls.2021.798992Soil, climate, and variety impact on quantity and quality of maize root mucilage exudation
https://doi.org/10.1007/s11104-022-05669-xAims: This study investigated the influence of climate and soil on the exudation rate and polysaccharide composition of aerial nodal root mucilage from drought-resistant and drought-susceptible maize varieties.
Methods: Two maize varieties were grown in two different soils (sandy-clay loam Acrisol and loam Luvisol) under simulated climatic conditions of their agroecological zones of origin in Kenya and Germany. The exudation rate of mucilage from the aerial nodal roots was quantified as dry weight per root tip per day and the mucilage was characterized for its polysaccharide composition.
Results: On average, the mucilage exudation rate was 35.8% higher under the Kenyan semi-arid tropical than under the German humid temperate climatic conditions. However, cultivation in the loam Luvisol soil from Germany led to 73.7% higher mucilage exudation rate than cultivation in the sandy-clay loam Acrisol soil from Kenya, plausibly due to its higher microbial biomass and nutrient availability. The drought-resistant Kenyan maize variety exuded 58.2% more mucilage than the drought-susceptible German variety. On average, mucilage polysaccharides were composed of 40.6% galactose, 26.2% fucose, 13.1% mannose, 11% arabinose, 3.5% glucose, 3.2% xylose, 1.3% glucuronic acid, and 1% an unknown uronic acid. Overall, significantly higher proportions of the uronic acids were found in the mucilage of the plants grown in the Kenyan sandy-clay loam soil and under the Kenyan semi-arid tropical climatic conditions.
Conclusions: Maize is able to enhance its mucilage exudation rate under warm climatic conditions and in soils of high microbial activity to mitigate water stress and support the rhizosphere microbiome, respectively.
Microbial storage and its implications for soil ecology
Organisms throughout the tree of life accumulate chemical resources, in particular forms or compartments, to secure their availability for future use. Here we review microbial storage and its ecological significance by assembling several rich but disconnected lines of research in microbiology, biogeochemistry, and the ecology of macroscopic organisms. Evidence is drawn from various systems, but we pay particular attention to soils, where microorganisms play crucial roles in global element cycles. An assembly of genus-level data demonstrates the likely prevalence of storage traits in soil. We provide a theoretical basis for microbial storage ecology by distinguishing a spectrum of storage strategies ranging from surplus storage (storage of abundant resources that are not immediately required) to reserve storage (storage of limited resources at the cost of other metabolic functions). This distinction highlights that microorganisms can invest in storage at times of surplus and under conditions of scarcity. We then align storage with trait-based microbial life-history strategies, leading to the hypothesis that ruderal species, which are adapted to disturbance, rely less on storage than microorganisms adapted to stress or high competition. We explore the implications of storage for soil biogeochemistry, microbial biomass, and element transformations and present a process-based model of intracellular carbon storage. Our model indicates that storage can mitigate against stoichiometric imbalances, thereby enhancing biomass growth and resource-use efficiency in the face of unbalanced resources. Given the central roles of microbes in biogeochemical cycles, we propose that microbial storage may be influential on macroscopic scales, from carbon cycling to ecosystem stability.https://doi.org/10.1038/s41396-021-01110-wT4-like Phages Reveal the Potential Role of Viruses in Soil Organic Matter Mineralization
https://doi.org/10.1021/acs.est.0c06014Viruses are the most abundant biological entities in the world, but their ecological functions in soil are virtually unknown. We hypothesized that greater abundance of T4-like phages will increase bacterial death and thereby suppress soil organic carbon (SOC) mineralization. A range of phage and bacterial abundances were established in sterilized soil by reinoculation with 10-3 and 10-6 dilutions of suspensions of unsterilized soil. The total and viable 16S rRNA gene abundance (a universal marker for bacteria) was measured by qPCR to determine bacterial abundance, with propidium monoazide (PMA) preapplication to eliminate DNA from non-viable cells. Abundance of the g23 marker gene was used to quantify T4-like phages. A close negative correlation between g23 abundance and viable 16S rRNA gene abundance was observed. High abundance of g23 led to lower viable ratios for bacteria, which suggested that phages drove microbial necromass production. The CO2 efflux from soil increased with bacterial abundance but decreased with higher abundance of T4-like phages. Elimination of extracellular DNA by PMA strengthened the relationship between CO2 efflux and bacterial abundance, suggesting that SOC mineralization by bacteria is strongly reduced by the T4-like phages. A random forest model revealed that abundance of T4-like phages and the abundance ratio of T4-like phages to bacteria are better predictors of SOC mineralization (measured as CO2 efflux) than bacterial abundance. Our study provides experimental evidence of phages' role in organic matter turnover in soil: they can retard SOC decomposition but accelerate bacterial turnover.
Intracellular Storage Reduces Stoichiometric Imbalances in Soil Microbial Biomass – A Theoretical Exploration
Microbial intracellular storage is key to defining microbial resource use strategies and could contribute to carbon (C) and nutrient cycling. However, little attention has been devoted to the role of intracellular storage in soil processes, in particular from a theoretical perspective. Here we fill this gap by integrating intracellular storage dynamics into a microbially explicit soil C and nutrient cycling model. Two ecologically relevant modes of storage are considered: reserve storage, in which elements are routed to a storage compartment in proportion to their uptake rate, and surplus storage, in which elements in excess of microbial stoichiometric requirements are stored and limiting elements are remobilized from storage to fuel growth and microbial maintenance. Our aim is to explore with this model how these different storage modes affect the retention of C and nutrients in active microbial biomass under idealized conditions mimicking a substrate pulse experiment. As a case study, we describe C and phosphorus (P) dynamics using literature data to estimate model parameters. Both storage modes enhance the retention of elements in microbial biomass, but the surplus storage mode is more effective to selectively store or remobilize C and nutrients according to microbial needs. Enhancement of microbial growth by both storage modes is largest when the substrate C:nutrient ratio is high (causing nutrient limitation after substrate addition) and the amount of added substrate is large. Moreover, storage increases biomass nutrient retention and growth more effectively when resources are supplied in a few large pulses compared to several smaller pulses (mimicking a nearly constant supply), which suggests storage to be particularly relevant in highly dynamic soil microhabitats. Overall, our results indicate that storage dynamics are most important under conditions of strong stoichiometric imbalance and may be of high ecological relevance in soil environments experiencing large variations in C and nutrient supply.https://doi.org/10.3389/fevo.2021.714134Mucilage Polysaccharide Composition and Exudation in Maize From Contrasting Climatic Regions
Mucilage, a gelatinous substance comprising mostly polysaccharides, is exuded by maize nodal and underground root tips. Although mucilage provides several benefits for rhizosphere functions, studies on the variation in mucilage amounts and its polysaccharide composition between genotypes are still lacking. In this study, eight maize (Zea mays L.) genotypes from different globally distributed agroecological zones were grown under identical abiotic conditions in a randomized field experiment. Mucilage exudation amount, neutral sugars and uronic acids were quantified. Galactose (∼39–42%), fucose (∼22–30%), mannose (∼11–14%), and arabinose (∼8–11%) were the major neutral sugars in nodal root mucilage. Xylose (∼1–4%), and glucose (∼1–4%) occurred only in minor proportions. Glucuronic acid (∼3–5%) was the only uronic acid detected. The polysaccharide composition differed significantly between maize genotypes. Mucilage exudation was 135 and 125% higher in the Indian (900 M Gold) and Kenyan (DH 02) genotypes than in the central European genotypes, respectively. Mucilage exudation was positively associated with the vapor pressure deficit of the genotypes’ agroecological zone. The results indicate that selection for environments with high vapor pressure deficit may favor higher mucilage exudation, possibly because mucilage can delay the onset of hydraulic failure during periods of high vapor pressure deficit. Genotypes from semi-arid climates might offer sources of genetic material for beneficial mucilage traits.https://doi.org/10.3389/fpls.2020.587610Short-term temperature history affects mineralization of fresh litter and extant soil organic matter, irrespective of agricultural management
The influence of temperature on mineralization of plant litter and pre-existing soil organic matter (SOM) involves not only the prevailing temperature, but also how it has changed through time. However, little is known about how temperature variability through time influences mineralization processes. Here, we investigated how short-term temperature history affects the mineralization of SOM and plant litter in soils from different agricultural management systems. We used soils from a long-term experiment with conventional and organic management treatments to set up microcosms. The microcosms were exposed to eight days of contrasting temperature regimes (different mean temperatures and constant versus fluctuating temperatures). Microcosms were then returned to a common temperature of 16 °C, 13C-labelled plant litter was added to half of them, and CO2 efflux was measured over the following week. We found that SOM and litter mineralization were both sensitive to the temperature history, with lower mean temperatures during preliminary treatment associated with higher mineralization during the subsequent common-temperature incubation. This effect persisted through the week after temperature differences were removed. Different patterns of temperature fluctuation and agricultural management did not significantly affect mineralization during common-temperature incubation. The history sensitivity of litter mineralization, despite litter being added after temperature differences had ended, indicates that the temperature history effects may be driven by short-term microbial acclimation. We conclude that organic matter and litter mineralization, which are key processes in the carbon cycle, are sensitive to short-term temperature history. This suggests that future investigations of soil CO2 efflux may need to take recent weather effects into account.https://doi.org/10.1016/j.soilbio.2020.107985Form of nitrogen deposition affects soil organic matter priming by glucose and cellulose
To examine the interplay of C and N availability, glucose (high microbial availability) and cellulose (low microbial availability)https://doi.org/10.1007/s00374-019-01357-8
were added to soils collected from a temperate forest that had received simulated N deposition for 6 years (organic and/or
inorganic N). The priming effect was higher for glucose addition than for cellulose. N deposition decreased the priming effect of
easily available glucose but increased the priming effect of cellulose. This confirmed an interactive effect of fresh organic matter
(FOM) availability and N deposition on priming. Furthermore, the interactive effect was affected by the form of N deposition,
with interaction mainly observed with organic N deposition. Qualitatively different patterns of priming were observed for the two
FOM types and were accompanied by contrasting abundance of fungi and bacteria in the community, as determined by phospholipid
fatty acid (PLFA) analysis. Organic N deposition increased bacterial biomass but decreased the intensity of priming. In
contrast, a competitive advantage of fungi with respect to organic N sources may drive priming by cellulose. The results
highlighted the importance of the availability of FOM in regulating the priming effect and showed that interactions between
the form of N deposition and the availability of the FOM should be considered when predicting soil C cycling in scenarios of
increased N deposition. Organic N deposition had a greater impact on priming effects than inorganic N deposition, and the
influence of microbial availability of FOM largely depended on organic N deposition.
Projects & collaborations
Projects
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Small but deadly: The role of viruses in bacterial death and soil carbon storage
Billions of microorganisms live and die in the soil beneath our feet, affecting soil carbon storage and its release to the atmosphere. This project investigates how viruses drive bacterial death and the fate of bacterial remains, to better understand how soil can contribute to maintaining a healthy climate.
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Vital soils for sustainable intensification of agriculture
A key challenge for sustainable intensification of agriculture is to produce increasing amounts of food for a growing world population, with minimal loss of biodiversity and ecosystem services. In order to facilitate ecological intensification of agriculture, the underlying principles need to be understood and validated in farmers’ fields
Additional Projects
Small but deadly: The role of viruses in bacterial death and soil carbon storage
2021–2024
Billions of microorganisms live and die in the soil beneath our feet, affecting soil carbon storage and its release to the atmosphere. This project investigates how viruses drive bacterial death and the fate of bacterial remains, to better understand how soil can contribute to maintaining a healthy climate.
Collaborations
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Microbial storage compounds: A neglected dimension of soil C cycling
2020–Present -
Nematode-phage-bacterial interactions in spatially structured soil environments
2021–Present
Outreach
Categories
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Featured in
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Beneath your feet, soil microbes are getting fat
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Enhancing Soil Biodiversity
At NIOO, we are on a mission to explore the strange world beneath our feet, to seek out new soil-borne life, uncover new miniature civilisations, and to boldly take humankind where it could not go before.
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Spotlight on living soil at COP15 biodiversity conference
The UN Biodiversity Conference in Montreal (COP15) is discussing global action to reverse biodiversity loss. Healthy, living soil is of key importance.
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Carbon storage in nature
Carbon storage is a hot item. Almost literally, as it is closely linked to climate warming. NIOO researchers discover more and more about the role of the living soil within our planet's carbon cycle. That role is: very influential, invaluable and essential for a sustainable climate policy.