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Barott, K. L.

Publications and source records attributed to Barott, K. L..

13 recordsLinked to original sources

Comparative profiling of sperm small RNAs in cnidarians highlights potential for paternal inheritance

Small RNAs in mature sperm are crucial regulators of gene expression following fertilization during early development in bilaterians. However, the presence and functions of sperm-derived small RNAs remain poorly understood in early-diverging (i.e., non-bilaterian) metazoans. In this study, we characterize three classes of small RNAs-microRNAs (miRNAs), piwi-interacting RNAs (piRNAs), and tRNA-derived RNAs (tDRs)-in sperm from three phylogenetically and ecologically distinct species from the early-diverging phylum Cnidaria: the sea anemone Nematostella vectensis, the temperate stony coral Astrangia poculata, and the reef-building tropical coral Acropora hyacinthus. All three classes of small RNAs examined were present in sperm from these cnidarians. Most miRNAs were species-specific; however, target prediction analysis revealed enriched putative targets involved in conserved developmental and signaling pathways. piRNAs overlapped with transposable elements and genic regions, indicating a potential dual role in genomic maintenance and gene expression regulation. Characterization of tDRs demonstrated that 5 prime-terminal fragments constituted the primary structural type across the three species, driven by high accumulation of specific isoacceptors including 5 prime-tDR-GlyGCC. Together, these findings provide the first evidence that cnidarian sperm carry a rich repertoire of small RNAs, including both conserved and species-specific types. Their presence suggests that paternal small RNAs contribute important regulatory information to the zygote in cnidarians, implicating paternal small RNAs as possible mediators of epigenetic inheritance in this early-branching metazoan phylum.

molecular biology↗

Decadal tracking reveals species-specific limits to coral thermal acclimatization

Mass coral bleaching events driven by marine heatwaves are increasing in frequency and severity, yet the long-term recovery trajectories of surviving corals remain poorly understood. Here, leveraging a cohort of individual coral colonies with a decade of tracked environmental and bleaching history, we captured structural shifts in the coral thermal performance landscape. Specifically, we quantified thermal performance curves (TPCs) for photosynthesis and calcification in bleaching-resistant and bleaching-susceptible colonies of two ecologically dominant reef-building corals (Montipora capitata and Porites compressa) at four and six years following the 2019 marine heatwave in K[a]neohe Bay, Hawaii (2023 and 2025, respectively). Coral thermal performance shifted substantially between 2023 and 2025, and these shifts differed between species, bleaching phenotypes, and traits. In P. compressa, photosynthetic thermal optimum (Topt) shifted downward over time by 1.6{degrees}C across both phenotypes, suggesting recalibration toward prevailing conditions at the potential cost of future heat tolerance. In M. capitata, photosynthetic performance was lower in bleaching-susceptible corals in 2023 but converged by 2025, suggesting susceptible colonies recovered. In contrast, Topt of photosynthesis remained persistently higher in bleaching-resistant colonies, likely reflecting established symbiont communities. Critically, photosynthesis and calcification did not recover in parallel. Calcification TPCs for both phenotypes of M. capitata were stable across both timepoints, whereas calcification TPCs in P. compressa continued to change through 2025. These findings demonstrate that coral thermal performance is not static following heatwaves but continues to be reshaped over multi-year recovery periods, and that species-specific traits and strategies can fundamentally constrain the pace and coupling of physiological recovery. Furthermore, elevated thermal tolerance acquired through a heatwave can erode during prolonged periods of ambient temperatures. As recurrent bleaching events shorten recovery windows, understanding these dynamic physiological trajectories are essential for understanding and forecasting reef futures.

physiology↗

The temperate coral Astrangia poculata maintains acid-base homeostasis through heat stress

Heat stress can disrupt acid-base homeostasis in reef-building corals and other tropical cnidarians, often leading to cellular acidosis that can undermine organismal function. Temperate cnidarians experience a high degree of seasonal temperature variability, leading us to hypothesize that temperate taxa have more thermally robust pH homeostasis than their tropical relatives. To test this, we investigated how elevated temperature affects intracellular pH and calcification in the temperate coral Astrangia poculata. Clonal pairs were exposed to elevated (30{degrees}C) or control (22{degrees}C) temperatures for 17 days. Despite causing damage to host tissues and symbiont cells, elevated temperature did not affect intracellular pH or inhibit calcification in A. poculata. These responses contrast with those of tropical cnidarians, which experience cellular acidification and decreased growth during heat stress. A. poculata therefore appears to have thermally resilient cellular acid-base homeostasis mechanisms, possibly due to adaptation to large seasonal temperature variations. However, we also observed tissue damage and lower egg densities in heat-treated individuals, suggesting that increasingly severe marine heatwaves can still threaten temperate coral fitness. These results provide insight into corals nuanced adaptive capacity across latitudes and biological scales.

ecology↗

Hypoxia threatens coral and sea anemone early life stages

Seawater hypoxia is increasing globally and can drive declines in organismal performance across a wide range of marine taxa. However, the effects of hypoxia on early life stages (e.g., larvae and juveniles) are largely unknown, and it is unclear how evolutionary and life histories may influence these outcomes. Here, we addressed this question by comparing hypoxia responses across early life stages of three cnidarian species representing a range of life histories: the reef-building coral Galaxea fascicularis, a broadcast spawner with horizontal transmission of endosymbiotic algae (family Symbiodiniaceae); the reef-building coral Porites astreoides, a brooder with vertical endosymbiont transmission; and the estuarine sea anemone Nematostella vectensis, a non-symbiotic broadcast spawner. Transient exposure of larvae to hypoxia (dissolved oxygen < 2 mg L-1 for 6 h) led to decreased larval swimming and growth for all three species, which resulted in impaired settlement for the corals. Coral-specific responses also included larval swelling, depressed respiration rates, and decreases in symbiont densities and function. These results indicate both immediate and latent negative effects of hypoxia on cnidarian physiology and coral-algal mutualisms specifically. In addition, G. fascicularis and P. astreoides were sensitized to heat stress following hypoxia exposure, suggesting that the combinatorial nature of climate stressors will lead to declining performance for corals. However, sensitization to heat stress was not observed in N. vectensis exposed to hypoxia, suggesting that this species may be more resilient to combined stressors. Overall, these results emphasize the importance of reducing anthropogenic carbon emissions to limit further ocean deoxygenation and warming.

ecology↗

Genomic comparison of the temperate coral Astrangia poculata with tropical corals yields insights into winter quiescence, innate immunity, and sexual reproduction

Facultatively symbiotic corals provide important experimental models to explore the establishment, maintenance, and breakdown of the mutualism between corals and members of the algal family Symbiodiniaceae. The temperate coral Astrangia poculata is one such model as it is not only facultatively symbiotic, but also occurs across a broad temperature and latitudinal gradient. Here, we report the de novo chromosome-scale assembly and annotation of the A. poculata genome. Though widespread segmental/tandem duplications of genomic regions were detected, we did not find strong evidence of a whole genome duplication (WGD) event. Comparison of the gene arrangement between A. poculata and the tropical coral Acropora millepora revealed 56.38% of the orthologous genes were conserved in syntenic blocks despite [~]415 million years of divergence. Gene families related to sperm hyperactivation and innate immunity, including lectins, were found to contain more genes in A. millepora relative to A. poculata. Sperm hyperactivation in A. millepora is expected given the extreme requirements of gamete competition during mass spawning events in tropical corals, while lectins are important in the establishment of coral-algal symbiosis. By contrast, gene families involved in sleep promotion, feeding suppression, and circadian sleep/wake cycle processes were expanded in A. poculata. These expanded gene families may play a role in A. poculatas ability to enter a dormancy-like state ("winter quiescence") to survive freezing temperatures at the northern edges of the species range.

genomics↗

Divergent recovery trajectories in reef-building corals following a decade of successive marine heatwaves

Increasingly frequent marine heatwaves are devastating coral reefs. Corals that survive these extreme heat stress events must rapidly recover if they are to withstand subsequent events, and long-term survival in the face of rising ocean temperatures may hinge on recovery capacity and acclimatory gains in heat tolerance over an individuals lifespan. To better understand coral recovery trajectories in the face of successive marine heatwaves, we monitored the responses of bleaching-susceptible and bleaching-resistant individuals of two dominant coral species in Hawaii, Montipora capitata and Porites compressa, over a decade that included three marine heatwaves. Bleaching-susceptible colonies of P. compressa exhibited beneficial acclimatization to heat stress (i.e., less bleaching) following repeat heatwaves, becoming indistinguishable from bleaching-resistant conspecifics during and after the third heatwave. In contrast, bleaching-susceptible M. capitata repeatedly bleached during all successive heatwaves and exhibited seasonal bleaching for up to three years following the third heatwave. Encouragingly, bleaching-resistant individuals of both species remained pigmented across the entire time series; however, pigmentation did not necessarily indicate physiological resilience. Specifically, M. capitata displayed incremental yet only partial recovery of symbiont density and tissue biomass across both bleaching phenotypes up to 35 months following the third heatwave. Conversely, P. compressa appeared to recover across most physiological metrics within two years, reverting to predictable seasonal variability. Ultimately, these results indicate that even some visually robust, bleaching-resistant corals can carry the cost of recurring heatwaves over multiple years, leading to divergent recovery trajectories that may erode coral reef resilience in the Anthropocene. Significance StatementCoral reefs are in jeopardy as climate change has led to increasingly frequent marine heatwaves. Some corals can survive these extreme heat stress events, thus acquiring environmental memory that may prime them for increased resistance and resilience in subsequent heatwaves via beneficial acclimatization. Yet, as the time between heatwaves decreases, the accumulation of stress experienced by some individuals may preclude opportunities for beneficial acclimatization. This nearly decade-long study revealed divergent recovery trajectories within and between species in response to successive marine heatwaves, ranging from costly to beneficial. As the climate continues to change, surviving corals must not only gain heat tolerance, but also rapidly recover to maintain the critically important ecosystem services that humanity relies on.

ecology↗

Heat stress disrupts acid-base homeostasis independent of symbiosis in the model cnidarian Exaiptasia diaphana

Heat stress threatens the survival of symbiotic cnidarians by causing their photosymbiosis to break down in a process known as bleaching. The direct effects of temperature on cnidarian host physiology remain difficult to describe because heat stress depresses symbiont performance, leading to host stress and starvation. The symbiotic sea anemone Exaiptasia diaphana provides an opportune system in which to disentangle direct vs. indirect effects of heat stress on the host, since it can survive indefinitely without symbionts. Here, we tested the hypothesis that heat stress directly influences cnidarian physiology by comparing symbiotic and aposymbiotic individuals of a clonal strain of E. diaphana. We exposed anemones to a range of temperatures (ambient, +2{degrees}C, +4{degrees}C, +6{degrees}C) for 15-18 days, then measured their symbiont population densities, autotrophic carbon assimilation and translocation, photosynthesis, respiration, and host intracellular pH (pHi). Anemones with initially high symbiont densities experienced dose-dependent symbiont loss with increasing temperature, resulting in a corresponding decline in host photosynthate accumulation. In contrast, anemones with low initial symbiont densities did not lose symbionts or assimilate less photosynthate as temperature increased, similar to the response of aposymbiotic anemones. Interestingly, pHi decreased in anemones at higher temperatures regardless of symbiont presence, cell density, or photosynthate translocation, indicating that heat stress disrupts cnidarian acid-base homeostasis independent of symbiosis dysfunction, and that acid-base regulation may be a critical point of vulnerability for hosts of this vital mutualism. Summary StatementWarming oceans threaten marine invertebrates. We found that heat disrupts acid-base homeostasis in a model symbiotic sea anemone regardless of symbiont presence or function, highlighting bleaching-independent effects of climate change.

physiology↗

Maximal coral thermal tolerance is found at intermediate diel temperature variability

O_LIIt has become critically important to identify environmental drivers of enhanced thermal tolerance in coral populations as ocean warming threatens the persistence of coral reef ecosystems globally. Variable temperature regimes that expose corals to sub-lethal heat stress have been recognized as a mechanism to increase coral thermotolerance and lessen coral bleaching; however, there is a need to better understand which thermal regimes are best for promoting coral stress hardening, and if thermal priming results in consistent benefits across species with distinct life-history strategies. C_LIO_LIStandardized thermal stress assays were used to determine the relative thermal tolerance of three divergent genera of corals (Acropora, Pocillopora and Porites) originating from six reef sites fluctuating in temperature by up to 7.7{degrees}C day-1, with an annual mean diel variability of 1-3{degrees}C day-1. Bleaching severity and dark-acclimated photochemical yield (Fv/Fm) were quantified following exposure to five temperature treatments ranging from 23.0 to 36.3{degrees}C -- up to 9{degrees}C above the regional maximum monthly mean. C_LIO_LIThe greatest thermal tolerance across all species was found at the site with intermediate mean diel temperature variability (2.2{degrees}C day-1), suggesting there is an optimal priming exposure that leads to maximal thermotolerance. Interestingly, Acropora and Pocillopora originating from the least thermally variable regimes (i.e., <1.3{degrees}C day-1) had lower thermal tolerance than corals from the most variable sites (i.e., > 2.8{degrees}C day-1), whereas the opposite was true for Porites, suggesting divergent responses to priming across taxa. C_LIO_LIWe highlight that fine-scale heterogeneity in temperature dynamics across habitats can increase coral thermal tolerance in diverse coral lineages, although in a non-linear manner. Remarkably, comparisons across global studies revealed that the range in coral thermotolerance uncovered in this study across a single reef system (<5 km) were as large as differences observed across vast latitudinal gradients (>300 km). This important finding indicates that local gene flow could improve thermal tolerance between habitats. However, as climate change continues, exposure to intensifying marine heatwaves is already compromising thermal priming as a mechanism to enhance coral thermal tolerance and bleaching resistance. C_LI

ecology↗

Endosymbiont strategic shifts inhibit cooperation during coral bleaching recovery

The future of coral reefs in a warming world depends on corals ability to resist or recover from losing their photosynthetic algal endosymbionts (coral bleaching) during marine heatwaves. Heat-tolerant algal species can confer bleaching resistance by remaining in symbiosis during heat stress but tend to provide less photosynthate to the host than heat-sensitive species. Understanding this potential nutritional tradeoff is crucial for predicting coral success under climate change, but the energetic dynamics of corals hosting different algal species during bleaching recovery are poorly understood. To test how algal energetics affects coral recovery, we heat-stressed corals (Montipora capitata) hosting either heat-sensitive Cladocopium sp. or heat-tolerant Durusdinium glynni algae for two weeks, followed by a one-month recovery period. We found that while thermotolerant D. glynni regained density and photochemical efficiency faster after bleaching than Cladocopium, this algal recovery did not correspond with host physiological recovery, and D. glynni populations still contributed less photosynthate to the host relative to Cladocopium. Further, high-density algal populations of both species translocated a smaller proportion of their photosynthate than low-density populations, and corals receiving less photosynthate suffered reduced calcification rates and lower intracellular pH. This is the first evidence of a direct negative relationship between symbiont population size and selfishness, and the first to establish a connection between Symbiodiniaceae carbon translocation and coral cellular homeostasis. Together, these results suggest that algal energy reallocation towards regrowth after bleaching can harm coral physiology, and that reestablishing a beneficial endosymbiosis can pose a secondary challenge for holobionts surviving stress.

ecology↗

Molecular mechanisms of sperm motility are conserved in a basal metazoan

Efficient and targeted sperm motility is essential for animal reproductive success. Studies in mammals and echinoderms have uncovered a highly conserved signaling mechanism in which sperm motility is stimulated by pH-dependent activation of the cAMP-producing enzyme soluble adenylyl cyclase (sAC). However, the presence of this pathway in basal metazoans has, until now, been unexplored. Here we found that cytoplasmic alkalinization induced a rapid burst of cAMP signaling and the full activation of motility in sperm from the reef-building coral Montipora capitata. Coral sperm expressed sAC in the flagellum, midpiece, and acrosomal regions, indicating that this molecular pH sensor may play a role in regulating mitochondrial respiration and flagellar beating. In bilaterians, sAC is a central node of a broader pH-dependent signaling pathway that alters cellular behavior in response to changes to the extracellular environment. We present transcript-level evidence that a homologous pathway is present in coral sperm, including the Na+/H+ exchanger SLC9C1, protein kinase A, and the CatSper Ca2+ channel conserved even in mammalian sperm. Our discovery of this pathway in a basal metazoan species highlights the ancient origin of the pH-sAC-cAMP signaling node in sperm physiology and suggests that it may be present in many other marine invertebrate taxa for which sperm motility mechanisms remain unexplored. These results emphasize our need to better understand the role of pH-dependent signaling in marine reproductive success, particularly as worsening ocean acidification and warming due to climate change continue to impair the physiology of corals and other marine invertebrates. Statement of significanceReef-building corals are the keystone species of the worlds most biodiverse yet threatened marine ecosystems. Corals reproduce by broadcast spawning, making the ability of their sperm to swim through the water column essential for fertilization. However, little is known about the mechanisms that regulate coral sperm motility. Here we found that elevated intracellular pH promotes the production of the second messenger cAMP in coral sperm and triggers the onset of motility. This study reveals the deep conservation of a sperm activation pathway from humans to corals, presenting the first comprehensive examination of the molecular mechanisms regulating sperm motility in an ancestral animal. These results are critical for understanding the resilience of this sensitive life stage to a changing marine environment.

ecology↗

Marine heatwaves depress metabolic activity and impair cellular acid-base homeostasis in reef-building corals regardless of bleaching susceptibility

Ocean warming is causing global coral bleaching events to increase in frequency, resulting in widespread coral mortality and disrupting the function of coral reef ecosystems. However, even during mass bleaching events, many corals resist bleaching despite exposure to abnormally high temperatures. While the physiological effects of bleaching have been well documented, the consequences of heat stress for bleaching resistant individuals are not well understood. In addition, much remains to be learned about how heat stress affects cellular level processes that may be overlooked at the organismal level, yet are crucial for coral performance in the short term and ecological success over the long term. Here we compared the physiological and cellular responses of bleaching resistant and bleaching susceptible corals throughout the 2019 marine heatwave in Hawai i, a repeat bleaching event that occurred four years after the previous regional event. Relative bleaching susceptibility within species was consistent between the two bleaching events, yet corals of both resistant and susceptible phenotypes exhibited pronounced metabolic depression during the heatwave. At the cellular level, bleaching susceptible corals had lower intracellular pH than bleaching resistant corals at the peak of bleaching for both symbiont-hosting and symbiont-free cells, indicating greater disruption of acid-base homeostasis in bleaching susceptible individuals. Notably, cells from both phenotypes were unable to compensate for experimentally induced cellular acidosis, indicating that acid-base regulation was significantly impaired at the cellular level even in bleaching resistant corals and in cells containing symbionts. Thermal disturbances may thus have substantial ecological consequences, as even small reallocations in energy budgets to maintain homeostasis during stress can negatively affect fitness. These results suggest concern is warranted for corals coping with ocean acidification alongside ocean warming, as the feedback between temperature stress and acid-base regulation may further exacerbate the physiological effects of climate change.

ecology↗

Bleaching resistant corals retain heat tolerance following acclimatization to environmentally distinct reefs

Urgent action is needed to prevent the demise of coral reefs as the climate crisis leads to an increasingly warmer and more acidic ocean. Propagating climate change resistant corals to restore degraded reefs is one promising strategy; however, empirical evidence is needed to determine if resistance is retained following transplantation within or beyond a corals natal reef. Here we assessed the performance of bleaching-resistant individuals of two coral species following reciprocal transplantation between environmentally distinct reefs (low vs high diel variability) to determine if stress resistance is retained following transplantation. Critically, transplantation to either environment had no influence on coral bleaching resistance, indicating that this trait was relatively fixed and is thus a useful metric for selecting corals for reef restoration within their native range. In contrast, growth was highly plastic, and native performance was not predictive of performance in the novel environment. Coral metabolism was also plastic, with cross transplants of both species matching the performance of native corals at both reefs within three months. Coral physiology (autotrophy, heterotrophy, and metabolism) and overall fitness (survival, growth, and reproduction) were higher at the reef with higher flow and fluctuations in diel pH and dissolved oxygen, and did not differ between native corals and cross-transplants. Conversely, cross-transplants at the low-variability reef had higher fitness than native corals, thus increasing overall fitness of the recipient population. This experiment was conducted during a non-bleaching year, which suggests that introduction of these bleaching-resistant individuals will provide even greater fitness benefits to recipient populations during bleaching years. In summary, this study demonstrates that propagating and transplanting bleaching-resistant corals can elevate the resistance of coral populations to ocean warming while simultaneously maintaining reef function as the climate crisis worsens.

ecology↗

Coral bleaching susceptibility is predictive of subsequent mortality within but not between coral species

Marine heat waves instigated by anthropogenic climate change are causing increasingly frequent and severe coral bleaching events that often lead to widespread coral mortality. While community-wide increases in coral mortality following bleaching events have been documented on reefs around the world, the ecological consequences for conspecific individual colonies exhibiting contrasting phenotypes during thermal stress (e.g. bleached vs. not bleached) are not well understood. Here we describe the ecological outcomes of colonies of the two dominant reef-building coral species in K[a]ne{square}ohe Bay, Hawai{square}i, Montipora capitata and Porites compressa, that exhibited either a bleaching susceptible phenotype (bleached) or resistant phenotype (non-bleached) following the second of two consecutive coral bleaching events in Hawai{square}i in 2015. Conspecific pairs of adjacent bleaching susceptible vs. resistant corals were tagged on patch reefs in two regions of K[a]ne{square}ohe Bay with different seawater residence times and terrestrial influence. The ecological consequences (symbiont recovery and mortality) were monitored for two years following the peak of the bleaching event. Bleaching susceptible corals suffered higher partial mortality than bleaching resistant corals of the same species in the first 6 months following thermal stress. Surprisingly, P. compressa had greater resilience following bleaching (faster pigment recovery and lower post-bleaching mortality) than M. capitata, despite having less resistance to bleaching (higher bleaching prevalence and severity). These differences indicate that bleaching susceptibility of a species is not always a good predictor of mortality following a bleaching event. By tracking the fate of individual colonies of resistant and susceptible phenotypes, contrasting ecological consequences of thermal stress were revealed that were undetectable at the population level. Furthermore, this approach revealed individuals that underwent particularly rapid recovery from mortality, including some colonies over a meter in diameter that recovered all live tissue cover from >60% partial mortality within just one year. These coral pairs continue to be maintained and monitored in the field, serving as a "living library" for future investigations on the ecology and physiology of coral bleaching.

ecology↗