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Weis, V. M.

Publications and source records attributed to Weis, V. M..

8 recordsLinked to original sources

Thermal pre-treatment of algal symbiont species differentially affects coral development

The foundation of coral reef ecosystems centered around the nutritional relationship between corals and intracellular algal symbionts. Although these symbioses are highly obligate for coral hosts, many partnerships are re-established anew with each coral generation. Furthermore, climate change destabilizes the symbiosis, and the cellular mechanisms underlying successful symbiont colonization of hosts and host development, and how they are affected by thermal stress are poorly understood. Here, we explored the effect of algal species and thermal treatments on symbiont and host cell proliferation by offering Acropora tenuis larvae one of four algal species pre-exposed to elevated or ambient temperature. In addition, we characterized the cell-surface glycome of each species-temperature combination to understand its role in symbiont recognition and proliferation. We found that thermal pre-treatment negatively affected algal photosynthetic efficiency and initial symbiont density in hosts, but did not affect symbiont colonization rate or cell proliferation. In contrast, host cell proliferation was affected in a species-specific manner. Thermal pre-treatment of B. minutum and D. trenchii negatively affected host cell proliferation compared to control symbionts, whereas thermal treatment of S. microadriaticum did not affect developmental outcomes. Further, uptake of thermally pre-treated D. trenchii decreased host cell proliferation below that of larvae not offered any symbionts, indicating that this relationship is costly to host development despite the high thermal tolerance of this species. Algal surface glycan composition varied across species but not by thermal pre-treatment, suggesting reductions in density of thermally pre-treated algae may be due to changes in physiology rather than altered surface chemistry. Further, variation in glycan abundance across species did not track differences in colonization rate or symbiont density, hinting towards a smaller role of glycans in host-symbiont specificity.

cell biology↗

Aiptasia oral regeneration is host-controlled but supported by symbiont-derived photosynthates

The study of oral regeneration in the sea anemone Exaiptasia diaphana (commonly called Aiptasia) - a prominent model for the study of coral-algal symbiosis - offers the unique opportunity to investigate the role of symbionts in regeneration. Algal symbionts have the potential to affect healing and regeneration by supplementing host nutrition and/or modulating host immune responses. Here we revisited the descriptions of Aiptasia oral regeneration from the 1970s with modern imaging techniques. Upon oral amputation, the anemones progressed through six distinct and repeatable stages of wound healing and regeneration, a process that was completed within a week. We followed regeneration in symbiotic anemones (i.e., associated with native dinoflagellate symbionts) in comparison to aposymbiotic anemones (i.e., lacking algae), and symbiotic anemones kept in the dark (i.e., blocking photosynthesis). In most symbiotic anemones under normal light, tentacle buds appeared within 32 hours post-amputation, whereas in aposymbiotic anemones and symbiotic anemones kept in the dark buds appeared 12 hours later. This pattern suggests that the contribution of symbiont-derived photosynthates to host nutrition shortened regeneration time. Our study provides the basis for further research on the underlying molecular processes in Aiptasia oral regeneration, for comparative studies of different symbiotic cnidarians and for investigating the relative role of host and symbionts in different developmental processes such as whole-body morphogenesis during asexual reproduction.

zoology↗

Octadecanoids as emerging lipid mediators in cnidarian-dinoflagellate symbiosis

Oxylipin signaling has been suggested as a potential mechanism for the inter-partner recognition and homeostasis regulation of cnidarian-dinoflagellate symbiosis, which maintains the ecological viability of coral reefs. Here we assessed the effects of symbiosis and symbiont identity on a model cnidarian, the sea anemone Exaiptasia diaphana, using mass spectrometry to quantify octadecanoid oxylipins (i.e., 18-carbon-derived oxygenated fatty acids). A total of 84 octadecanoids were reported, and distinct stereospecificity was observed for the synthesis of R- and S-enantiomers for symbiont-free anemones and free-living cultured dinoflagellate symbionts, respectively. Symbiont-derived 13(S)-hydroxy-octadecatetraenoic acid (13(S)- HOTE) linked to a 13S-lipoxygnase was translocated to the host anemone with a 32-fold increase, suggesting it as a biomarker of symbiosis and as a potential agonist of host receptors that regulate inflammatory transcription. Only symbiosis with the native symbiont Breviolum minutum decreased the abundance of pro-inflammatory 9(R)-hydroxy-octadecadienoic acid (9(R)-HODE) in the host. In contrast, symbiosis with the non-native symbiont Durusdinium trenchii was marked by higher abundance of autoxidation-derived octadecanoids, corroborating previous evidence for cellular stress in this association. The putative octadecanoid signaling pathways reported here suggest foundational knowledge gaps that can support the bioengineering and selective breeding of more optimal host-symbiont pairings to enhance resilience and survival of coral reefs.

biochemistry↗

Symbiosis collapses during development of asexual offspring in the absence of heterotrophic feeding in a model cnidarian-algal symbiosis

A stable symbiosis between corals and dinoflagellate algae is crucial for coral reef health, and it is driven by nutrient exchange and environmental interactions. Our understanding of the homeostasis between host cnidarian and algal symbiont during the host adult stage is a longtime area of focus, but little is known about the balance of partners during development and regeneration. We investigated the role of symbiotic algae and heterotrophic feeding on development in the sea anemone model organism commonly called Aiptasia. We focused on asexually-produced offspring (G1), examining the effects of autotrophic and heterotrophic nutrition on developmental rates. We found that the presence of symbionts enhanced growth in fed conditions but impeded development and survival under starvation. The effect of symbiont presence on starved offspring was dose-dependent where those offspring with more symbionts at an earlier stage lost tentacles and mass faster than those with fewer symbionts. Our data demonstrate the importance of heterotrophic nutrition during early development and establishment of symbiosis. We propose that suppression of immunity during development may account for the observed patterns, although further research is required to validate this hypothesis. Our results provide insight into the metabolic costs and benefits of symbiosis under different nutritional conditions during development and regeneration of symbiotic cnidarians.

developmental biology↗

Molecular insights into the Darwin paradox of coral reefs from the sea anemone Aiptasia

Symbiotic cnidarians such as corals and anemones form highly productive and biodiverse coral-reef ecosystems in nutrient-poor ocean environments, a phenomenon known as Darwins Paradox. Resolving this paradox requires elucidating the molecular bases of efficient nutrient distribution and recycling in the cnidarian-dinoflagellate symbiosis. Using the sea anemone Aiptasia, we show that during symbiosis, the increased availability of glucose and the presence of the algae jointly induce the coordinated upregulation and re-localization of glucose and ammonium transporters. These molecular responses are critical to support symbiont functioning and organism-wide nitrogen assimilation through GS/GOGAT-mediated amino-acid biosynthesis. Our results reveal crucial aspects of the molecular mechanisms underlying nitrogen conservation and recycling in these organisms that allow them to thrive in the nitrogen-poor ocean environments. One-sentence summaryWhole-organism nitrogen assimilation fueled by glucose from symbiotic algae enables corals to flourish in oligotrophic waters.

molecular biology↗

Coral larvae suppress the heat stress response during the onset of symbiosis thereby decreasing their odds of survival

The endosymbiosis between most corals and their photosynthetic dinoflagellate partners begins early in the host life history, when corals are larvae or juvenile polyps. The capacity of coral larvae to buffer climate-induced stress while in the process of symbiont acquisition could come with physiological trade-offs that alter larval behavior, development, settlement and survivorship. Here we examined the joint effects of thermal stress and symbiosis onset on colonization dynamics, survival, metamorphosis and host gene expression of Acropora digitifera larvae. We found that thermal stress decreased symbiont colonization of hosts by 50% and symbiont density by 98.5% over two weeks. Temperature and colonization also influenced larval survival and metamorphosis in an additive manner, where colonized larvae fared worse or prematurely metamorphosed more often than non-colonized larvae under thermal stress. Transcriptomic responses to colonization and thermal stress treatments were largely independent, while the interaction of these treatments revealed contrasting expression profiles of genes that function in the stress response, immunity, inflammation and cell cycle regulation. The combined treatment either canceled or lowered the magnitude of expression of heat-stress responsive genes in the presence of symbionts, revealing a physiological cost to acquiring symbionts at the larval stage with elevated temperatures. In addition, host immune suppression, a hallmark of symbiosis onset under ambient temperature, turned to immune activation under heat stress. Thus, by integrating the physical environment and biotic pressures that mediate pre-settlement event in corals, our results suggest that colonization may hinder larval survival and recruitment creating isolated, genetically similar populations under projected climate scenarios.

ecology↗

Cryopreservation of Hydractinia symbiolongicarpus sperm to support community-based repository development for preservation of genetic resources

Hydractinia symbiolongicarpus is an emerging model organism in which cutting-edge genomic tools and resources are being developed for use in a growing number of research fields. However, one limitation of this model system is the lack of long-term storage for genetic resources. Our goal in this study was to establish a generalizable approach to sperm cryopreservation that would support future repository development and could be applied to many species according to available resources. Our approach was to: 1) Assess sperm characteristics and standardize collection and processing; 2) Assess acute toxicity to cryoprotectants, and 3) Evaluate and refine freezing conditions to permit post-thaw fertilization and produce viable offspring. By following this approach, we found that Hydractinia sperm incubated in 5% DMSO, equilibrated at 4{degrees}C for 20 min, and cooled at a rate of 20{degrees}C/min to - 80{degrees}C at a cell concentration of 108-109/mL in 0.25-mL aliquots were able to fertilize 150-300 eggs which yielded offspring that could metamorphose into juvenile polyps. In addition, improvements were made for processing sperm using a customized 3-D printed collection system. Other opportunities for improvement include optimizing the volumetric sperm-to-egg ratio for fertilization. Establishing repository capabilities for the Hydractinia research community will be essential for future development, maintenance, protection, and distribution of genetic resources. More broadly, this application-based approach highlights the long-term value of establishing repository-level resources that can be expanded to fit community needs.

zoology↗

N-linked surface glycan biosynthesis, composition, inhibition, and function in cnidarian-dinoflagellate symbiosis

The success of symbioses between cnidarian hosts (e.g. corals and sea anemones) and micro-algal symbionts hinges on the molecular interactions that govern the establishment and maintenance of intracellular mutualisms. As a fundamental component of innate immunity, glycan-lectin interactions impact the onset of marine endosymbioses, but our understanding of the effects of cell surface glycome composition on symbiosis establishment remains limited. In this study, we examined the canonical N-glycan biosynthesis pathway in the genome of the dinoflagellate symbiont Breviolum minutum (family Symbiodiniaceae) and found it to be conserved with the exception of the transferase GlcNAc-TII (MGAT2). Using coupled liquid chromatography-mass spectrometry (LC-MS/MS), we characterized the cell surface N-glycan content of B. minutum, providing the first insight into the molecular composition of surface glycans in dinoflagellates. We then used the biosynthesis inhibitors kifunensine and swainsonine to alter the glycan composition of B. minutum. Successful high-mannose enrichment via kifunensine treatment resulted in a significant decrease in colonization of the model sea anemone Aiptasia (Exaiptasia pallida) by B. minutum. Hybrid glycan enrichment via swainsonine treatment, however, could not be confirmed and did not impact colonization. We conclude that functional Golgi processing of N-glycans is critical for maintaining appropriate cell surface glycan composition and for ensuring colonization success by B. minutum.

molecular biology↗