Biology subjects

Meibom, A.

Publications and source records attributed to Meibom, A..

11 recordsLinked to original sources

bioRxiv2024

Single-cell trait diversity explains niche and fitness differences in aquatic microbial communities

Two fundamental questions in ecology are how biodiversity is maintained and how it affects ecosystem functioning. Until now, it has been difficult to study the above mechanisms in natural microbial communities, yet they are important drivers of biogeochemical ecosystem functions. Here, we use a new approach to define and measure biodiversity in complex lake microbial communities (Lake Cadagno, Switzerland) based on the cell-to-cell variation in multiple functionally relevant phenotypic traits. We use stable isotope probing coupled to correlative imaging using confocal laser scanning microscopy (CLSM) and nanometer-scale secondary ion mass spectrometry (NanoSIMS) to obtain morphological (size), physiological (pigments) and metabolic (carbon and nitrogen isotope uptake and sulfur content) traits for a large number of individual cells along the environmental gradient found across lake depth. We show that cell-to-cell trait variation is significantly correlated with cell densities as a proxy for ecosystem functioning, whereas genetic diversity measured at the level of 16S and 18S is not. Our single-cell analysis provides evidence for a simultaneous increase in niche partitioning (measured as increased evenness in pigment composition) and decrease in fitness differences (measured as decreased variability in sulfur content) due to light limitation and competition for nutrients in deep layers of the lake. This leads to a negative relationship between niche and fitness differences. Our results suggest that niche and fitness differences in natural microbial communities can be understood at the level of single-cell traits, providing a mechanistic understanding of the relationship between microbial diversity and ecosystem functioning.

microbiology↗

bioRxiv2023

Symbiotic nutrient exchange enhances the long-term survival of cassiosomes, the autonomous stinging-cell structures of Cassiopea

Medusae of the widely distributed and locally invasive upside-down jellyfish Cassiopea release autonomous, mobile stinging structures. These so-called cassiosomes are a major contributor to contactless stinging incidents in (sub-)tropical shallow waters. While the presence of endosymbiotic dinoflagellates in cassiosomes has previously been observed, their potential contribution to the metabolism and long-term survival of cassiosomes is unknown. Combining stable isotope labeling and correlative SEM and NanoSIMS imaging with a long-term in vitro experiment, this study reveals a mutualistic symbiosis based on nutritional exchanges in dinoflagellate-bearing cassiosomes. We were able to show that organic carbon input from the dinoflagellates fuels the metabolism of the host tissue and enables anabolic nitrogen assimilation. Thanks to this symbiotic nutrient exchange, cassiosomes showed enhanced survival in the light compared to dark conditions for at least one month in vitro. Overall, this study demonstrates that cassiosomes, in analogy with Cassiopea medusae, are photosymbiotic holobionts. Cassiosomes thus promise to be a powerful new miniaturized model system for in-depth ultrastructural and molecular investigation of cnidarian photosymbioses.

ecology↗

bioRxiv2023

Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis

Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was to a large extent concealed by body shrinkage of the starving animals, resulting in what could be referred to as invisible bleaching. Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in our warming oceans.

ecology↗

bioRxiv2023

Foraging on host synthesized metabolites enables the bacterial symbiont Snodgrassella alvi to colonize the honey bee gut

Dietary nutrients and microbial cross-feeding allow diverse bacteria to colonize the animal gut. Less is known about the role of host-derived nutrients in enabling gut bacterial colonization. We examined metabolic interactions within the evolutionary ancient symbiosis between the honey bee (Apis mellifera) and the core gut microbiota member Snodgrassella alvi. This Betaproteobacteria is incapable of metabolizing saccharides, yet colonizes the honey bee gut in the presence of only a sugar diet. Using comparative metabolomics, 13C tracers, and Nanoscale secondary ion mass spectrometry (NanoSIMS), we show in vivo that S. alvi grows on host-derived organic acids, including citrate, glycerate and 3-hydroxy-3-methylglutarate which are actively secreted by the host into the gut lumen. S. alvi additionally modulates tryptophan metabolism in the gut by converting kynurenine to anthranilate. These results suggest that S. alvi is adapted to a specific metabolic niche in the gut that depends on host-derived nutritional resources.

microbiology↗

bioRxiv2023

Non-invasive investigation of the morphology and optical properties of the upside-down jellyfish Cassiopea with optical coherence tomography

The jellyfish Cassiopea largely cover their organic carbon demand via photosynthates produced by their microalgal endosymbionts, but how holobiont morphology and optical properties affect the light microclimate and symbiont photosynthesis in Cassiopea remain unexplored. Here, we use optical coherence tomography (OCT) to study the morphology of live Cassiopea medusae at high spatial resolution. We include detailed 3D reconstructions of external micromorphology, and show the spatial distribution of endosymbionts clustered in amoebocytes and white granules in the bell tissue. Furthermore, we use OCT data to extract inherent optical properties from light scattering white granules in Cassiopea and show that white granules enhance local light availability for symbionts in close proximity. Individual granules had a scattering coefficient of s = 200-300 cm-1, and a scattering anisotropy factor of g = 0.7, while large tissue regions filled with white granules had a lower s = 40-100 cm-1, and g = 0.8-0.9. We combined OCT information with an isotopic labelling experiment to investigate the effect of enhanced light availability in whitish tissue regions. Algal symbionts located in whitish tissue exhibited significantly higher carbon fixation as compared to symbionts in anastomosing tissue (i.e., tissue without light scattering white granules). Our findings support previous suggestions that white granules in Cassiopea play an important role in the host modulation of the light-microenvironment.

biophysics↗

bioRxiv2022

Symbiotic nutrient cycling enables the long-term survival of Aiptasia in the absence of heterotrophic food sources

Phototrophic Cnidaria are mixotrophic organisms that can complement their heterotrophic diet with nutrients assimilated by their algal endosymbionts. Metabolic models suggest that the translocation of photosynthates and their derivatives from the algae may be sufficient to cover the metabolic energy demands of the host. However, the importance of heterotrophy to the nutritional budget of these holobionts remains unclear. Here, we report on the long-term survival of the photosymbiotic anemone Aiptasia in the absence of heterotrophic food sources. Following one year of heterotrophic starvation, these anemones remained fully viable but showed an 85 % reduction in biomass compared to their regularly fed counterparts. This shrinking was accompanied by a reduction in host protein content and algal density, indicative of severe nitrogen limitation. Nonetheless, isotopic labeling experiments combined with NanoSIMS imaging revealed that the contribution of algal-derived nutrients to the host metabolism remained unaffected due to an increase in algal photosynthesis and more efficient carbon translocation. Taken together, our results suggest that, on a one- year timescale, heterotrophic feeding is not essential to fulfilling the energy requirements of the holobiont. But, while symbiotic nutrient cycling effectively retains carbon in the holobiont over long time scales, our data suggest that heterotrophic feeding is a critical source of nitrogen required for holobiont growth under oligotrophic conditions.

ecology↗

bioRxiv2022

Coupled carbon and nitrogen cycling regulates the cnidarian-algal symbiosis

Efficient nutrient recycling underpins the ecological success of the cnidarian-algal symbiosis in oligotrophic waters. In a stable symbiosis, nitrogen limitation restricts the growth of algal endosymbionts and stimulates their release of photosynthates to the cnidarian animal host. However, the detailed mechanisms controlling nitrogen availability in hospite and their role in symbiosis regulation remain poorly understood. Here, we studied the metabolic regulation of symbiotic nitrogen cycling in the sea anemone Aiptasia by experimentally altering labile carbon availability in a series of experiments. Combining 13C and 15N stable isotope labeling experiments with physiological analyses and NanoSIMS imaging, we show that the competition for environmental ammonium between the host and its algal symbionts is regulated by labile carbon availability. Light regimes optimal for algal photosynthesis increased carbon availability in the holobiont and stimulated nitrogen assimilation in the host metabolism. Consequently, algal symbiont densities were lowest under optimal environmental conditions and increased toward the symbiosiss lower and upper light tolerance limits. This metabolic regulation promotes efficient carbon recycling in a stable symbiosis across a wide range of environmental conditions. At the same time, the dependence on resource competition may favor parasitic interactions explaining the instability of the symbiosis as the environmental conditions in the Anthropocene shift towards its tolerance limits.

ecology↗

bioRxiv2022

The mesoglea buffers the physico-chemical microenvironment of photosymbionts in the upside-down jellyfish Cassiopea sp.

The jellyfish Cassiopea has a conspicuous lifestyle, positioning itself upside-down on sediments in shallow waters thereby exposing its photosynthetic endosymbionts (Symbiodiniaceae) to light. Several studies have shown how the photosymbionts benefit the jellyfish host in terms of nutrition and O2 availability, but little is known about the internal physico-chemical microenvironment of Cassiopea during light-dark periods. Here, we used fiber-optic sensors to investigate how light is modulated at the water-tissue interface of Cassiopea sp. and how light is scattered inside host tissue. We additionally used electrochemical and fiber-optic microsensors to investigate the dynamics of O2 and pH in response to changes in the light availability in intact living specimens of Cassiopea sp. Mapping of photon scalar irradiance revealed a distinct spatial heterogeneity over different anatomical structures of the host, where oral arms and the manubrium had overall higher light availability, while shaded parts underneath the oral arms and the bell had less light available. White host pigmentation, especially in the bell tissue, showed higher light availability relative to similar bell tissue without white pigmentation. Microprofiles of scalar irradiance into white pigmented bell tissue showed intense light scattering and enhanced light penetration, while light was rapidly attenuated over the upper 0.5 mm in tissue with symbionts only. Depth profiles of O2 concentration into bell tissue of intact, healthy/living jellyfish showed increasing concentration with depth into the mesoglea, with no apparent saturation point during light periods. O2 was slowly depleted in the mesoglea in darkness, and O2 concentration remained higher than ambient water in large (> 6 cm diameter) individuals, even after 50 min in darkness. Light-dark shifts in large medusae showed that the mesoglea slowly turns from a net sink during photoperiods into a net source of O2 during darkness. In contrast, small medusae showed a more dramatic change in O2 concentration, with rapid O2 buildup/consumption in response to light-dark shifts; in a manner similar to corals. These effects on O2 production/consumption were also reflected in moderate pH fluctuations within the mesoglea. The mesoglea thus buffers O2 and pH dynamics during dark-periods.

ecology↗

bioRxiv2021

Photosynthesis from stolen chloroplasts increases sea slug reproductive fitness

Some sea slugs are able to steal functional chloroplasts (kleptoplasts) from their algal food sources, but the role and relevance of photosynthesis to the animal host remain controversial. While some researchers claim that kleptoplasts are slowly digestible snacks, others advocate that they enhance the overall fitness of sea slugs much more profoundly. Our analysis show light-dependent incorporation of 13C and 15N in the albumen gland and gonadal follicles of the sea slug Elysia timida, representing translocation of photosynthates to kleptoplast-free reproductive organs. Long-chain polyunsaturated fatty acids with reported roles in reproduction were produced in the sea slug cells using labelled precursors translocated from the kleptoplasts. Finally, we report reduced fecundity of E. timida by suppressing kleptoplast photosynthesis. The present study provides the first thorough experimental evidence that photosynthesis enhances the reproductive fitness of kleptoplast-bearing sea slugs, confirming the biological relevance of this remarkable association between a metazoan and an algal-derived organelle. TeaserSea slugs incorporate functional chloroplasts from algae and use products of photosynthesis to maximize reproductive output.

ecology↗

bioRxiv2020

Imaging stable isotope labelling kinetics (iSILK) for following spatial Aβ plaque aggregation dynamics in evolving Alzheimers disease pathology

For our understanding of Alzheimers disease (AD) pathophysiology, it is of critical importance to determine how key pathological factors, specifically amyloid {beta} (A{beta}) plaque formation, are interconnected and implicated in neurodegeneration, disease progression and the development of clinical symptoms. Exactly how A{beta} plaque formation is initiated and how the ongoing plaque deposition proceeds is not well understood. This is partly because we can only examine details of the molecular pathology after death in humans, and in mice, we can only examine a particular point in time without any longitudinal information on the fate of individually formed deposits. Herein, we used metabolic labelling of proteins with stable isotopes, together with multimodal imaging mass spectrometry (IMS) for imaging stable isotope labelling kinetics (iSILK) in the APPNL-G-F knock-in mouse model of AD. The aim was to monitor the earliest seeds of A{beta} deposition through ongoing plaque development and track the deposition of A{beta} that is produced later in relation to already deposited plaques. This allowed us to visualize A{beta} peptide aggregation dynamics within individual deposits across different brain regions. We identified the cortex as a primary site of deposition in precipitating plaque pathology. Further, our data show that structural plaque heterogeneity is associated with differential peptide deposition. Specifically, A{beta}1-42 is forming an initial core seed followed by radial outgrowth and late secretion and deposition of A{beta}1-38. Together these data prove the potential of iSILK for probing amyloid protein secretion, processing and aggregation dynamics in AD pathology.

neuroscience↗

bioRxiv2018

Tissue- and cellular-level allocation of autotrophic and heterotrophic nutrients in the coral symbiosis -- A NanoSIMS study

Corals access inorganic seawater nutrients through their autotrophic endosymbiotic dinoflagellates, but also capture planktonic prey through heterotrophic feeding. Correlating NanoSIMS and TEM imaging, we visualize and quantify the subcellular fate of autotrophic and heterotrophic C and N in the coral Stylophora pistillata using stable isotopes. Six scenarios were compared after 6h: autotrophic pulse (13C-bicarbonate, 15N-nitrate) in either unfed or regularly fed corals, and heterotrophic pulse (13C-, 15N-labelled brine shrimps) in regularly fed corals; each at ambient and elevated temperature. Host assimilation of photosynthates was similar under fed and unfed conditions, but symbionts assimilated 10% more C in fed corals. Photoautotrophic C was primarily channelled into host lipid bodies, whereas heterotrophic C and N were generally co-allocated to the tissue. Food-derived label was detected in some subcellular structures associated with the remobilisation of host lipid stores. While heterotrophic input generally exceeded autotrophic input, it was more negatively affected by elevated temperature. The reduced input from both feeding modes at elevated temperature was accompanied by a shift in the partitioning of C and N, benefiting epidermis and symbiont. This study provides a unique view on the nutrient partitioning in corals and highlights the tight connection of nutrient fluxes in symbiotic partners.

physiology↗