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Pogoreutz, C.

Publications and source records attributed to Pogoreutz, C..

5 recordsLinked to original sources

Chilling injury to algal symbionts induces host starvation and metabolic reorganization in a temperate cnidarian

Global temperature anomalies increasingly disrupt the cnidarian-algal symbiosis through a phenomenon termed bleaching. In contrast to heat stress, the mechanisms underlying symbiotic breakdown under cold stress remain largely unknown. Combining physiological and metabolomic measurements, we investigated the response of the photosymbiotic sea anemone holobiont Aiptasia couchii to an experiment mimicking a cold spell in the Mediterranean Sea. Within four weeks, we observed the onset of symbiotic breakdown reflected in reduced algal endosymbiont density and chlorophyll a content. While photosynthetic efficiency remained largely unaffected, no gross photosynthesis was detectable in cold-stressed anemones and decreases in glycosyldiacylglycerols and fatty acyl glycosides indicated chloroplast lipid remobilization. This breakdown of symbiotic carbon cycling was reflected in increased dipeptide and ceramide levels suggesting anemones catabolized protein reserves and induced pre-apoptotic pathways. Taken together, these responses suggest a decoupling of light and dark reactions of photosynthesis in cold-stressed endosymbionts, resembling chilling injury in higher plants and free-living microalgae. This chilling-induced collapse of symbiotic nutrient cycling eventually leads to host starvation in cold-stressed Cnidaria. Hence, while cold and heat stress may invoke contrasting physiological effects on endosymbionts, our results suggest that both stressors destabilize the symbiosis through similar mechanisms culminating in host starvation.

ecology↗

From genomic decay to functional advantage: Trait-based evidence for long-term host residency of a next-generation coral probiotic

A key bottleneck in microbiome engineering is ensuring the long-term host association of introduced microbes. Selecting probiotic candidates based on evolutionary genomic decay signatures of emerging host dependency offers a potential solution. The Ruegeria strain B4 of the population MC10, identified by such signatures, has shown persistent colonization in corals in a companion study. Whether this persistence translates into a measurable host benefit compared to other coral-associated Ruegeria strains, and which mechanisms underlie such benefit, remained unknown. Here we directly compare the probiotic efficacy of MC10-B4 against two sympatric Ruegeria strains isolated from the same coral colony and mucus compartment, controlling for host genotype and microenvironment. MC10-B4 inoculation significantly increased heat stress tolerance in the coral model cnidarian Aiptasia (Exaiptasia diaphana strain H2), outperforming both sympatric control strains. To understand the mechanistic basis of this probiotic efficacy, we characterized the functional profile of MC10 using an integrated multi-omics approach. The genome of MC10 is enriched in genes associated with host-interaction, including siderophore-mediated iron acquisition and exopolysaccharide biosynthesis, which were phenotypically confirmed by detectable iron scavenging and enhanced biofilm formation. Following exposure to coral tissue extract, MC10-B4 underwent a coordinated motility-to-sessility proteomic reprogramming, downregulating flagellar motor components while upregulating flagellin and biofilm regulators. This response was distinct from its sympatric relatives, which instead mounted broad upregulation of nutrient acquisition systems. MC10-B4s functional profile, particularly its sensitivity to oxidative stress, contrasts with the traits typically favored in conventional probiotic screens. Our results move beyond the descriptive identification of a coral probiotic by providing initial mechanistic insight into traits associated with long-term host association and improved thermal performance. These findings validate an evolution-guided approach that prioritizes innate colonization potential over pre-defined laboratory functionalities, informing the rational design of durable probiotics.

microbiology↗

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↗

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↗

Coral reef carbonate budgets and ecological drivers in the naturally high temperature and high alkalinity environment of the Red Sea

The coral structural framework is crucial for maintaining reef ecosystem function and services. In the central Red Sea, a naturally high alkalinity is beneficial to reef growth, but rising water temperatures impair the calcification capacity of reef-building organisms. However, it is currently unknown how beneficial and detrimental factors affect the balance between calcification and erosion, and thereby the overall growth of the reef framework. To provide insight into present-day carbonate budgets and reef growth dynamics in the central Red Sea, we measured in situ net-accretion and net-erosion rates (Gnet) by deployment of limestone blocks and estimated census-based carbonate budgets (Gbudget) in four reef sites along a cross-shelf gradient (25 km). We assessed abiotic variables (i.e., temperature, inorganic nutrients, and carbonate system variables) and biotic drivers (i.e., calcifier and bioeroder abundances). On average, total alkalinity AT (2346 - 2431 mol kg-1), aragonite saturation state (4.5 - 5.2 {Omega}a), and pCO2 (283 -315 atm) were close to estimates of pre-industrial global ocean surface waters. Despite these calcification-favorable carbonate system conditions, Gnet and Gbudget encompassed positive (offshore) and negative net-production (midshore-lagoon and exposed nearshore site) estimates. Notably, Gbudget maxima were lower compared to reef growth from pristine Indian Ocean sites. Yet, a comparison with historical data from the northern Red Sea suggests that overall reef growth in the Red Sea has likely remained similar since 1995. When assessing sites across the shelf gradient, AT correlated well with reef growth rates ({rho} = 0.89), while temperature was a weaker, negative correlate ({rho} = -0.71). Further, AT explained about 65 % of Gbudget in a best fitting distance-based linear model. Interestingly, parrotfish abundances added up to 82% of explained variation, further substantiating recent studies highlighting the importance of parrotfish to reef ecosystem function. Our study provides a baseline that will be particularly useful in assessing future trajectories of reef growth capacities in the Red Sea under continuous ocean warming and acidification.

ecology↗