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Kühl, M.

Publications and source records attributed to Kühl, M..

12 recordsLinked to original sources

Colony geometric complexity predicts the co-occurrence of coral photosymbiont genera

The endosymbiosis between tropical reef-building corals and dinoflagellate algae (family Symbiodiniaceae) underpins the healthy functioning of coral reef ecosystems. Although dominant host-symbiont pairings differ across spatial scales (e.g., bioregion, reef zone, and depth), corals often associate with multiple symbionts. Where diverse symbionts occur together, their local-scale ecology is poorly understood. Moreover, whilst coral morphological plasticity generates a structurally complex spatial habitat for endosymbiosis, the role of host geometry in facilitating symbiont co-occurrence is completely unexplored. Here, we integrated high-throughput sequencing of the ITS2 gene region with digital 3D photogrammetry to evaluate symbiont distribution within coral structural habitat and determine the influence of host morphology on symbiont community composition. Symbiont composition was characterised along a vertical gradient (coral apex to base) across 50 Hydnophora microconos colonies from Rarotonga, Cook Islands. We identified dominance by the genera Durusdinium and Cladocopium, with inter-genus co-occurrence recognised in 60% of coral colonies. The co-occurrence of two Cladocopium lineages (C3f and C3k) was validated based on congruence with the plastid minicircle psbA non-coding region (psbAncr). Geometric quantification from digital 3D reconstructions of coral colonies revealed that single symbiont taxon colonies were morphologically distinct, whilst multi-symbiont colonies exhibited a broader morphological range. Where Cladocopium-Durusdinium co-occurrence was identified, surface orientation indicated increased Durusdinium prevalence toward the base of coral colonies, corresponding to regions with the highest occlusion of modelled downwelling light. Collectively, these findings suggest that coral structural heterogeneity supports Symbiodiniaceae diversity and highlights the value of resolving microhabitat-level variation to understand symbiont co-occurrence.

ecology↗

Carbon substrate type shapes spatial self-organization in a multi-species biofilm community

Spatial organization is a defining feature of multispecies biofilms and critically influences microbial interactions and emergent community properties. However, understanding and manipulating how microbes assemble into spatially structured biofilms remains challenging because most experimental frameworks emphasize species composition and pairwise interactions, while often overlooking the spatial constraints on biofilms imposed by the environment. In this study, we focus on how carbon substrate type, distinguishing between diffusible sugars and polymeric substrates, affects biofilm self-organization in a four-member synthetic bacterial community (SynCom). Across all tested conditions, the SynCom consistently formed more biofilm biomass than any of its subsets, indicating a robust synergistic phenotype. Using chemically defined, 3D-printed hydrogel substrates with consistent physical properties, we varied carbon source composition to identify its impact on biofilm assembly. Microscopic imaging showed that carbon substrate type strongly influenced biofilm self-organization with diffusible simple carbon substrates yielding relatively intermixed communities, whereas polymer-rich carbon substrates promoted a highly structured biofilm organization characterized by the dominance and peripheral localization of polymer-degrading species. Bioinformatic analyses of carbohydrate-active enzymes (CAZymes) annotation and genome-scale metabolic modeling suggested that metabolite exchange networks in the SynCom may drive more complex metabolic interactions beyond the commonly observed degrader-exploiter-scavenger relationship within planktonic microbial communities. Together, our findings demonstrate carbon substrate type as an important ecological determinant of biofilm self-organization, highlighting the need to integrate environmental factors alongside species composition and metabolic potential to fully understand and manipulate natural and engineered multispecies biofilms.

microbiology↗

Microscale sampling of the coral gastric cavity reveals a gut-like microbial community

Animal guts contain numerous microbes, which are critical for nutrient assimilation and pathogen defence. While corals and other Cnidaria lack a true differentiated gut, they possess gastrovascular cavities (GVCs), semi-enclosed compartments where vital processes such as digestion, reproduction and symbiotic exchanges take place. The microbiome harboured in GVCs is therefore likely key to holobiont fitness, but remains severely understudied due to challenges of working in these small compartments. Here, we developed minimally invasive methodologies to sample the GVC of coral polyps and characterise the microbial communities harboured within. We used glass capillaries, low dead volume microneedles, or nylon microswabs to sample the gastric microbiome of individual polyps from six species of corals, then applied low-input DNA extraction to characterise the microbial communities from these microliter volume samples. Microsensor measurements of GVCs revealed anoxic or hypoxic micro-niches, which persist even under prolonged illumination with saturating irradiance. These niches harboured microbial communities enriched in putatively microaerophilic or facultatively anaerobic taxa, such as Epsilonproteobacteria. Some core taxa found in the GVC of Lobophyllia hemprichii from the Great Barrier Reef were also detected in conspecific colonies held in aquaria, indicating that these associations are unlikely to be transient. Our findings suggest that the coral GVC is chemically and microbiologically similar to the gut of higher Metazoa. Given the importance of gut microbiomes in mediating animal health, harnessing the coral "gut microbiome" may foster novel active interventions aimed at increasing the resilience of coral reefs to the climate crisis.

microbiology↗

Near infrared radiation-driven oxygenic photosynthesis contributes substantially to primary production in biofilms harboring chlorophyll f-containing cyanobacteria

Cyanobacteria with far-red light photoacclimation (FaRLiP) can modify their photopigmentation by synthesizing red-shifted phycobiliproteins and chlorophylls, i.e., chlorophyll (Chl) d and f. This enables use of near-infrared radiation (NIR) for oxygenic photosynthesis in habitats depleted of visible light (VIS). Cyanobacteria with FaRLiP are widespread but their quantitative importance for primary production in natural habitats remains unknown. Previously we showed that intertidal beachrock formations can harbor endolithic populations of Chl f-containing cyanobacteria capable of using NIR for oxygenic photosynthesis (Kuhl et al., 2020). Here we use a combination of gas exchange measurements and luminescence lifetime-based O2 imaging to quantify how endolithic cyanobacteria with far-red chlorophylls contribute to the primary production of an intertidal beachrock habitat when exposed to a natural gradient of visible and near-infrared radiation. While VIS-driven photosynthesis predominantly took place in the dense cyanobacterial surface biofilm of beachrock, NIR-driven photosynthesis was mainly confined to a subsurface layer in the beachrock containing endolithic cyanobacteria with Chl f and d. Yet such subsurface, NIR-driven photosynthesis provided a substantial O2 production reaching >20% of the gross photosynthesis rates under comparable photon irradiance of visible light. This points to a hitherto overlooked role of far-red light acclimated cyanobacteria for primary production in natural habitats characterized by steep attenuation of visible light and relative enrichment in near-infrared radiation.

ecology↗

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↗

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↗

Green fluorescent protein-like pigments optimize the internal light environment in symbiotic reef building corals

Pigments homologous to the Green Fluorescent Protein (GFP) have been proposed to fine-tune the internal light microclimate of corals, facilitating photoacclimation of photosynthetic coral symbionts (Symbiodiniaceae) to life in different reef habitats and environmental conditions. However, direct measurements of the in vivo light conditions inside the coral tissue supporting this conclusion are lacking. Here, we quantified the intra-tissue spectral light environment of corals expressing GFP-like proteins from widely different light regimes. We focus on (1) photoconvertible red fluorescent proteins (pcRFPs), thought to enhance photosynthesis in mesophotic habitats via wavelength conversion, and (2) chromoproteins (CPs), which provide photoprotection to the symbionts in shallow water via light absorption. Optical microsensor measurements indicated that both pigment groups strongly alter the coral tissue light environment. Estimates derived from light spectra measured in pcRFP-containing corals showed that fluorescence emission can contribute to >50% of orange-red light available to the photosynthetic symbionts at mesophotic depths. We further show that upregulation of pink CPs in shallow-water corals during bleaching leads to a reduction of orange light by 10-20% compared to low-CP tissue. Thus, screening by CPs has an important role in mitigating the light-enhancing effect of coral tissue scattering during bleaching. Our results provide the first experimental quantification of the importance of GFP-like proteins in fine-tuning the light microclimate of corals during photoacclimation.

ecology↗

Dynamic characteristics rather than static hubs are important in biological networks

Biological processes are rarely a consequence of single protein interactions but rather of complex regulatory networks. However, interaction graphs cannot adequately capture temporal changes. Among models that investigate dynamics, Boolean network models can approximate simple features of interaction graphs integrating also dynamics. Nevertheless, dynamic analyses are time-consuming and with growing number of nodes may become infeasible. Therefore, we set up a method to identify minimal sets of nodes able to determine network dynamics. This approach is able to depict dynamics without calculating exhaustively the complete network dynamics. Applying it to a variety of biological networks, we identified small sets of nodes sufficient to determine the dynamic behavior of the whole system. Further characterization of these sets showed that the majority of dynamic decision-makers were not static hubs. Our work suggests a paradigm shift unraveling a new class of nodes different from static hubs and able to determine network dynamics.

bioinformatics↗

Substantial near-infrared radiation-driven photosynthesis of chlorophyll f-containing cyanobacteria in a natural habitat

Far-red absorbing chlorophylls are constitutively present as Chl d in the cyanobacterium Acaryochloris marina, or dynamically expressed by synthesis of Chl f and red-shifted phycobilins via far-red light photoacclimation in a range of cyanobacteria, which enables them to use near-infrared-radiation (NIR) for oxygenic photosynthesis. While the biochemistry and molecular physiology of Chl f-containing cyanobacteria has been unraveled in culture studies, their ecological significance remains unexplored and no data on their in situ activity exist. With a novel combination of hyperspectral imaging, confocal laser scanning microscopy, and nanoparticle-based O2 imaging, we demonstrate substantial NIR-driven oxygenic photosynthesis by endolithic, Chl f-containing cyanobacteria within natural beachrock biofilms that are widespread on (sub)tropical coastlines. This indicates an important role of NIR-driven oxygenic photosynthesis in primary production of endolithic and other shaded habitats.\n\nImpact statementCyanobacteria with chlorophyll f show substantial near-infrared radiation-driven photosynthesis in intertidal habitats.

ecology↗

Bio-optical properties and radiative energy budgets in fed and starved scleractinian corals (Pocillopora damicornis) during thermal bleaching

Corals achieve outstanding photosynthetic quantum efficiencies approaching theoretical limits (i.e. 0.125 O2 photon-1) and it is unknown how such photosynthetic efficiency varies with environmental stress. In this study, we investigated the combined effects of thermal stress and active feeding on the radiative energy budget and photosynthetic efficiency of the symbiont-bearing coral Pocillopora damicornis by using fiber-optic and electrochemical microsensors in combination with variable chlorophyll fluorescence imaging. At normal temperature (25{degrees}C), the percentage of absorbed light energy used for photosynthesis was higher for fed (~5-6% under low light exposure) compared to unfed corals (4%). Corals from both feeding treatments responded equally to stress from high light exposure (2400 mol photons m-2 s-1), exhibiting a decrease in photosynthetic energy efficiency down to 0.5-0.6%. Fed corals showed increased resilience against thermal bleaching compared to unfed corals, as fed corals were able to uphold their high photosynthetic energy efficiency for 5 days longer during thermal stress, as compared to unfed corals, which decreased their photosynthetic energy efficiency almost immediately when exposed to thermal stress. We conclude that active feeding is beneficial to corals by prolonging coral health and resilience during thermal stress as a result of an overall healthier symbiont population.

biophysics↗

Effect of feeding and thermal stress on photosynthesis, respiration and the carbon budget of the scleractinian coral Pocillopora damicornis

Studying carbon dynamics in the coral holobiont provides essential knowledge of nutritional strategies and is thus central to understanding coral ecophysiology. In this study, the first aim was to investigate the effect of daily feeding and thermal stress on oxygen (O2) rates measured at polyp-scale with microsensors and at whole fragment scale using incubation methods. The second aim was to assess the carbon budget of the symbiotic association using H13CO3, under the different conditions. Micro- and macro-scale measurements revealed enhanced O2 evolution rates for fed compared to unfed corals. However, gross O2 production in fed corals was increased at high temperature on a macroscale but not on a microscale basis, likely due to a heterogeneous distribution of photosynthesis over the coral surface. Starved corals always exhibited reduced photosynthetic activity at high temperature, which suggests that the nutritional status of the coral host is a key limiting factor for coral productivity under thermal stress. Quantification of photosynthate translocation and carbon budgets showed very low incorporation rates, for both symbionts and host (0.03 - 0.6 g C cm-2 h-1) equivalent to only 0.008 - 0.6 %, of the photosynthetically fixed carbon for P. damicornis, in all treatments. Carbon loss (via respiration and/or mucus release) was about 41 - 47 % and 52 - 76% of the fixed carbon for starved and fed corals, respectively. Such high loss of translocated carbon suggests that P. damicornis is nitrogen and/or phosphorus limited. Heterotrophy might thus cover a larger portion of the nutritional demand for P. damicornis than previously assumed. Our results suggest that active feeding plays a fundamental role in metabolic dynamics and bleaching susceptibility of corals.

ecology↗

In vitro community synergy between bacterial soil isolates can be facilitated by pH stabilisation of the environment

Composition and development of naturally occurring microbial communities is defined by a complex interplay between the community and the surrounding environment and by interactions between community members. Intriguingly, these interactions can in some cases cause community synergies where the community is able to outperform it single species constituents. However, the underlying mechanisms driving community interactions are often unknown and difficult to identify due to high community complexity. Here we show how pH stabilisation of the environment through the metabolic activity of specific community members acts as a positive inter-species interaction driving in vitro community synergy in a model consortium of four co-isolated soil bacteria: Microbacterium oxydans, Xanthomonas retroflexus, Stenotrophomonas rhizophila and Paenibacillus amylolyticus. Using micro-sensor pH measurements to show how individual species change the local pH micro-environment, and how co-cultivation leads to a stabilised pH regime over time. Specifically, in vitro acid production from Paenibacillus amylolyticus and alkali production primarily from Xanthomonas retroflexus lead to an overall pH stabilisation of the local environment over time, which in turn resulted in enhanced community growth. This specific type of interspecies interaction was found to be highly dependent on media type and media concentration, however similar pH drift from the individual species could be observed across media variants.\n\nImportanceWe show that in vitro metabolic activity of individual members of a synthetic, co- isolated model community presenting community synergistic growth arises through the inter-species interaction of pH stabilization of the community micro-environment. The observed inter-species interaction is highly media specific and most pronounced under high nutrient availability. This adds to the growing diversity of identified community interactions leading to enhanced community growth.

microbiology↗