Biology subjects

Cleves, P. A.

Publications and source records attributed to Cleves, P. A..

9 recordsLinked to original sources

bioRxiv2026

Aiptasia larvae are phenotypically validated as a model of coral bleaching using high-throughput machine-learning image analysis

The sea anemone Aiptasia is a model system for understanding cnidarian loss of symbiotic algae under heat stress (bleaching). While Aiptasia polyps have been widely used to study this process, accurate symbiosis phenotyping grapples with discordant length scales: fine spatial resolution (~100 um) is needed across a whole organism (~5 mm). To address this, we consider small (~100 um), optically transparent Aiptasia larvae as a bleaching model suitable for whole-organism phenotyping by fluorescence microscopy with larvae classified as symbiotic when algae are localized within gastrodermal cells. To expedite phenotyping, we introduce a machine-learning (ML) image-analysis pipeline (SYMPHONY) designed for single-larva resolution analysis of intact larvae. SYMPHONY efficiently identifies the cellular location of internalized algae (accuracy: 79%, precision: 82%, recall: 79%, F1 score: 79%; training dataset composed of 1611 total objects). Additionally, SYMPHONY reports statistically significant larval bleaching under heat stress and corroborates manual phenotyping results, while significantly reducing operator labor from hours to minutes. The combination of the Aiptasia larvae model and the SYMPHONY pipeline aims to accelerate our understanding of symbiosis breakdown.

bioengineering↗

bioRxiv2026

CRISPR/Cas9-mutagenesis reveals that varying dependence on HSF1 is associated with differences in coral heat tolerance

Coral reefs face declines due to increasing water temperatures associated with climate change. Major research efforts have focused on determining the mechanisms corals can use to adapt to heat stress and identifying molecular indicators for this adaptation. CRISPR/Cas9-based genomic editing promises a new avenue to study gene function in corals; however, these methods are limited by the annual spawning of corals in the wild. Here, we shifted spawning of the reef-building coral Galaxea fascicularis to access gametes multiple times a year in the lab. We discovered the remarkable plasticity and programmability in coral spawning, which enabled the development of a genetically tractable model coral. To investigate the molecular responses of corals to heat stress, we profiled transcriptional changes in heat-tolerant G. fascicularis and heat-sensitive Acropora millepora during acute heat stress. Comparison of the transcriptional responses to heat stress in larvae of the two species revealed that A. millepora has a stronger magnitude of the early heat stress response than G. fascicularis. This increased response in A. millepora included the upregulation of the conserved transcriptional regulator of heat stress response, Heat Shock Transcription Factor 1 (HSF1), and its predicted targets. CRISPR/Cas9 mutagenesis of HSF1 in both species showed that the heat-tolerant G. fascicularis is less dependent on HSF1 than A. millepora for survival during acute heat stress. These results suggest that differences in HSF1 expression after heat exposure contribute to variation in coral heat tolerance and may be used as biomarkers to predict heat tolerance in wild corals.

genetics↗

bioRxiv2025

Co-option of lysosomal machinery shapes the symbiosis supporting coral reefs

Intracellular photosymbiosis has evolved across life and forms the foundation of coral reef ecosystems. Using the sea anemone Aiptasia as a model, we generated a high-quality proteome of the symbiosome, the organelle that houses algal symbionts. This proteome revealed protein trafficking mechanisms and the types of biomolecules exchanged during symbiosis. Symbiosomal enrichment of lysosomal proteins, visualization of lysosomal fusion, along with reduced symbiosis following knockdown of lysosomal genes, supports its phagolysosomal identity and that extensive co-option of lysosomal proteins shapes the symbiosome. CRISPR/Cas9-induced mutations in the symbiosomal and lysosomal bicarbonate/sulfate transporter, SLC26A11, disrupted symbiosis in both Aiptasia and a reef-building coral. These findings support that anemones and corals independently evolved a carbon-concentrating and sulfate transport mechanism to fuel photosymbiosis by co-opting an orthologous lysosomal transporter.

cell biology↗

bioRxiv2025

Lipid nanoparticle supplementation enhances host metabolism in a model symbiotic cnidarian

Stable cnidarian-dinoflagellate symbiosis provides the trophic foundation of coral reef ecosystems. Understanding nutrient exchange underpinning this symbiosis grows increasingly urgent as reefs face accelerating threats from climate change, and the need for time-critical interventions to improve coral health via aquaculture. Lipid nanoparticles (LNPs), widely used as delivery vehicles in biomedical science, are emerging as a promising tool to supplement coral nutrition. However, physiological impacts of LNPs on cnidarians, including uptake, nutritional value, and holobiont response, remain largely unexplored. Here, we delivered empty, phosphatidylcholine LNPs to both symbiotic and aposymbiotic Exaiptasia diaphana, an anemone model for corals, and analyzed the host proteomic response via mass spectrometry. LNP supplementation elicited broad proteome shifts, with notable overlap between symbiosis- and LNP-induced protein expression. Proteins involved in lipid catabolism, lipid transport, {beta}-oxidation, lysosomal function, and protein translation were significantly more abundant, consistent with enhanced lipid processing and metabolic activity. LNP supplementation, like symbiosis, suppressed both asexual reproduction and the expression of a suite of predation- and digestion-associated venom proteins and proteases, suggesting a conserved "sated" phenotype in response to lipid supply. Variations in feeding frequency with Artemia had minimal impact, indicating that LNPs can be a robust supplement irrespective of primary feeding regime. These data demonstrate that adult Exaiptasia are capable of direct uptake of LNPs, offering a tool for probing lipid metabolism, signaling and symbiotic function in cnidarians. Moreover, the ability to manipulate host physiology using defined lipid formulations holds significant potential for advancing coral aquaculture stress resilience, including reef restoration strategies.

zoology↗

bioRxiv2024

Global coral genomic vulnerability explains recent reef losses

The dramatic decline of reef-building corals calls for a better understanding of coral adaptation to ocean warming. Here, we characterized genetic diversity of the widespread genus Acropora by building a genomic database of 595 coral samples from different oceanic regions--from the Great Barrier Reef to the Persian Gulf. Through genome-environment associations, we found that different Acropora species showed parallel evolutionary signals of heat-adaptation in the same genomic regions, pointing to genes associated with molecular heat shock responses and symbiosis. We then projected the present and the predicted future distribution of heat-adapted genotypes across reefs worldwide. Reefs projected with low frequency of heat-adapted genotypes display higher rates of Acropora decline, indicating a potential genomic vulnerability to heat exposure. Our projections also suggest a transition where heat-adapted genotypes will spread at least until 2040. However, this transition will likely involve mass mortality of entire non-adapted populations and a consequent erosion of Acropora genetic diversity. This genetic diversity loss could hinder the capacity of Acropora to adapt to the more extreme heatwaves projected beyond 2040. Genomic vulnerability and genetic diversity loss estimates can be used to reassess which coral reefs are at risk and their conservation.

evolutionary biology↗

bioRxiv2022

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↗

bioRxiv2020

Metabolome shift associated with thermal stress in coral holobionts

Coral reef systems are under global threat due to warming and acidifying oceans1. Understanding the response of the coral holobiont to environmental change is crucial to aid conservation efforts. The most pressing problem is "coral bleaching", usually precipitated by prolonged thermal stress that disrupts the algal symbiosis sustaining the holobiont2,3. We used metabolomics to understand how the coral holobiont metabolome responds to heat stress with the goal of identifying diagnostic markers prior to bleaching onset. We studied the heat tolerant Montipora capitata and heat sensitive Pocillopora acuta coral species from the Hawaiian reef system in K[a]neohe Bay, Oahu. Untargeted LC-MS analysis uncovered both known and novel metabolites that accumulate during heat stress. Among those showing the highest differential accumulation were a variety of co-regulated dipeptides present in both species. The structures of four of these compounds were determined (Arginine-Glutamine, Lysine-Glutamine, Arginine-Valine, and Arginine-Alanine). These dipeptides also showed differential accumulation in symbiotic and aposymbiotic (alga free) individuals of the sea anemone model Aiptasia4, suggesting their animal provenance and algal symbiont related function. Our results identify a suite of metabolites associated with thermal stress that can be used to diagnose coral health in wild samples.

evolutionary biology↗

bioRxiv2019

Varied effects of algal symbionts on transcription factor NF-κB in a sea anemone and a coral: possible roles in symbiosis and thermotolerance

Many cnidarians, including the reef-building corals, undergo symbiotic mutualisms with photosynthetic dinoflagellate algae of the family Symbiodiniaceae. These partnerships are sensitive to temperature extremes, which cause symbiont loss and increased coral mortality. Previous studies have implicated host immunity and specifically immunity transcription factor NF-{kappa}B as having a role in the maintenance of the cnidarian-algal symbiosis. Here we have further investigated a possible role for NF-{kappa}B in establishment and loss of symbiosis in various strains of the anemone Exaiptasia (Aiptasia) and in the coral Pocillopora damicornis. Our results show that NF-{kappa}B expression is reduced in Aiptasia larvae and adults that host certain algae strains. Treatment of Aiptasia larvae with a known symbiosis-promoting cytokine, transforming growth factor {beta}, also led to decreased NF-{kappa}B expression. We also show that aposymbiotic Aiptasia (with high NF-{kappa}B expression) have increased survival following infection with the pathogenic bacterium Serratia marcescens as compared to symbiotic Aiptasia (low NF-{kappa}B expression). Furthermore, a P. damicornis coral colony hosting Durusdinium spp. (formerly clade D) symbionts had higher basal NF-{kappa}B expression and decreased heat-induced bleaching as compared to two individuals hosting Cladocopium spp. (formerly clade C) symbionts. Lastly, genome-wide gene expression profiling and genomic promoter analysis identified putative NF-{kappa}B target genes that may be involved in thermal bleaching, symbiont maintenance, and/or immune protection in P. damicornis. Our results provide further support for the hypothesis that modulation of NF-{kappa}B and immunity plays a role in some, but perhaps not all, cnidarian-Symbiodiniaceae partnerships as well as in resistance to pathogens and bleaching.

molecular biology↗

bioRxiv2018

Strength in numbers: collaborative science for new experimental model systems

Our current understanding of biology is heavily based on the contributions from a small number of genetically tractable model organisms. Most eukaryotic phyla lack such experimental models, and this limits our ability to explore the molecular mechanisms that ultimately define their biology, ecology, and diversity. In particular, marine protists suffer from a paucity of model organisms despite playing critical roles in global nutrient cycles, food webs, and climate. To address this deficit, an initiative was launched in 2015 to foster development of ecologically and taxonomically diverse marine protist genetic models. This multifaceted, complex but important challenge required a highly collaborative community-based approach. Herein we describe this approach, the advances achieved, and the lessons learned by participants in this novel community-based model for research.

microbiology↗