bioRxiv Science⌕ Search

Biology subjects

Putnam, H.

Publications and source records attributed to Putnam, H..

5 recordsLinked to original sources

A miRNA-mediated gene regulatory network supports seasonal plasticity in the temperate coral Astrangia poculata

Phenotypic plasticity is a critical strategy for sessile marine invertebrates that cannot escape changing environmental conditions. For corals facing intensifying climate change, the molecular mechanisms that generate and regulate acclimatory responses are central to understanding performance and persistence. MicroRNAs (miRNAs), small non-coding RNAs that regulate gene expression via translational repression and transcript degradation, are compelling candidates for mediating such plasticity, but their role in coral biology remains poorly characterized. Here, we use Astrangia poculata, a temperate coral that endures annual temperature ranges exceeding 25{degrees}C, to investigate the potential for miRNA-mediated plasticity across seasonal and thermal contexts. We exposed adult aposymbiotic colonies to ambient seasonal temperatures ([~]5-22{degrees}C) and a chronic +3{degrees}C warming treatment from February to August 2021, sampling monthly for physiological analyses and at three time points (February, June, August) for molecular analyses. Seasonal change drove significant shifts in photosynthesis, respiration, and soluble protein, whereas the +3{degrees}C treatment had minimal physiological effect. RNA-seq analysis identified the strongest response across seasons, with transcriptional functional enrichment shifting from protein homeostasis, and cellular integrity in the winter, to immunity, metabolism, and reproduction in the summer. We identified 51 miRNAs in A. poculata, 46 of which are novel to this species, providing the first characterization of the miRNA repertoire in this species. Target prediction and co-expression analyses revealed that while mRNA-miRNA networks maintain a stable infrastructure across seasons and treatments, specific interactions are rewired to drive seasonal biology. This dynamic regulation suppresses energy-intensive cell division and morphogenesis during winter quiescence, while shifting to regulate tissue remodeling and reproduction genes during the summer. These results establish miRNAs as seasonal gene regulators in a temperate coral and suggest that the molecular infrastructure underlying its plasticity may also confer resilience to moderate thermal stress.

Molecular Biology↗

Parental effects provide an opportunity for coral resilience following major bleaching events

Identifying processes that promote coral reef recovery and resilience is crucial as ocean warming becomes more frequent and severe. Sexual reproduction is essential for the replenishment of coral populations and maintenance of genetic diversity; however, the ability for corals to reproduce may be impaired by marine heatwaves that cause coral bleaching. In 2014 and 2015, the Hawaiian Islands experienced coral bleaching with differential bleaching susceptibility in the species Montipora capitata, a dominant reef-building coral in the region. We tested the hypothesis that coral bleaching resistance enhances reproductive capacity and offspring performance by examining the reproductive biology of colonies that bleached and recovered (B) and colonies that did not bleach (NB) in 2015 in the subsequent spawning seasons. The proportion of colonies that spawned was higher in 2016 than in 2017. Regardless of parental bleaching history, we found eggs with higher abnormality and bundles with fewer eggs in 2016 than 2017. While reproductive output was similar between B and NB colonies in 2016, survivorship of offspring that year were significantly influenced by the parental bleaching history (egg donor x sperm donor: B x B, B x NB, NB x B, and NB x NB). Offspring produced by NB egg donors had the highest survivorship, while offspring from previously bleached colonies had the lowest survivorship, highlighting the negative effects of bleaching on parental investment and offspring performance. While sexual reproduction continues in M. capitata post-bleaching, gametes are differentially impacted by recovery time following a bleaching event and by parental bleaching resistance. Our results demonstrate the importance of identifying bleaching resistant individuals during and after heating events. This study further highlights the significance of maternal effects through potential egg provisioning for offspring survivorship and provides a baseline for human-assisted intervention (i.e., selective breeding) to mitigate the effects of climate change on coral reefs.

zoology↗

Characterization of a sperm motility signaling pathway in a gonochoric coral suggests conservation across sexual systems

Many marine invertebrates liberate their gametes into the water column broadcast spawning, where fertilization hinges upon the successful activation of sperm motility. Here, we investigated the molecular mechanisms underpinning sperm motility in the broadcast spawning coral Astrangia poculata. We found that cytosolic alkalinization activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), followed by motility, in A. poculata sperm. In addition, we show for the first time in any cnidarian that sAC activity is required to activate protein kinase A (PKA) in sperm, and that PKA activity is required for the initiation of sperm motility. Ultrastructures of A. poculata sperm displayed morphological homology to other gonochoric cnidarians, and investigation of cnidarian proteomes revealed that sAC, the central signaling node in the sperm motility pathway, demonstrates broad structural and functional conservation across a diversity of cnidarian species. Ultimately, these results suggest that the role of sAC signaling in sperm motility is conserved between sperm from gonochoric and hermaphroditic corals, which is surprising given their morphological dissimilarities. This study also offers insight into the evolution of the mechanisms controlling metazoan sperm motility. Summary statementFor broadcast spawning marine invertebrates, the initiation of sperm motility is essential for fertilization. Here, we provide evidence for conservation of a sperm motility pathway across sexual systems in corals.

physiology↗

Transfer of Knowledge from Model Organisms to Evolutionarily Distant Non-Model Organisms: The Coral Pocillopora damicornis Membrane Signaling Receptome

With the ease of gene sequencing and the technology available to study and manipulate non-model organisms, the need to translate our understanding of model organisms to non-model organisms has become an urgent problem. For example, mining of large coral and their symbiont sequence data is a challenge, but also provides an opportunity for understanding functionality and evolution of these and other non-model organisms. Much more information than for any other eukaryotic species is available for humans, especially related to signal transduction and diseases. However, the coral cnidarian host and human have diverged over 700 million years ago and homologies between proteins are therefore often in the gray zone or undetectable with traditional BLAST searches. We introduce a two-stage approach to identifying putative coral homologues of human proteins. First, through remote homology detection using Hidden Markov Models, we identify candidate human homologues in the cnidarian genome. However, for many proteins, the human genome alone contains multiple family members with similar or even more divergence in sequence. In the second stage, therefore, we filter the remote homology results based on the functional and structural plausibility of each coral candidate, shortlisting the coral proteins likely to be true human homologues. We demonstrate our approach with a pipeline for mapping membrane receptors in humans to membrane receptors in corals, with specific focus on the stony coral, P. damicornis. More than 1000 human membrane receptors mapped to 335 coral receptors, including 151 G protein coupled receptors (GPCRs). To validate specific sub-families, we chose opsin proteins, representative GPCRs that confer light sensitivity, and Toll-like receptors, representative non-GPCRs, which function in the immune response, and their ability to communicate with microorganisms. Through detailed structure-function analysis of their ligand-binding pockets and downstream signaling cascades, we selected those candidate remote homologues likely to carry out related functions in the corals. This pipeline may prove generally useful for other non-model organisms, such as to support the growing field of synthetic biology.

bioinformatics↗

Shifting Baselines: Repeat bleaching drives coral physiotypes through environmental legacy and cellular memory

O_LIGlobal climate change is altering coral reef ecosystems. Notably, marine heat waves are producing widespread coral bleaching events that are increasing in frequency, with projections for annual bleaching events on reefs worldwide by mid-century. C_LIO_LIThe response of corals to elevated seawater temperatures can be modulated by abiotic factors at site of origin and dominant endosymbiont type, which can result in a shift in multiple coral traits and drive physiological legacy effects that influence the trajectory of reef corals under subsequent thermal stress events. It is critical, therefore, to evaluate the potential for shifting physiological and cellular baselines driven by these factors in in situ bleaching (and recovery) events. Here, we use the back-to-back regional bleaching events of 2014 and 2015 in the Hawaiian Islands and subsequent recovery periods to test the hypothesis that coral multivariate trait space (here termed physiotype, sensu (Van Straalen, 2003) shift in multiple bleaching events, modulated by both environmental histories and symbiotic partnerships (Symbiodiniaceae). C_LIO_LIDespite fewer degree heating weeks in the first-bleaching event relative to the second (7 vs. 10), bleaching severity in a dominant reef building coral on Hawaiian reefs, Montipora capitata, was greater (~70% vs. 50% bleached cover) and differences due to environmental history (reef site) were more pronounced. Melanin, an immune cytotoxic response, provided an initial defense during the first event, potentially priming antioxidant activity, which peaked in the second-bleaching event (i.e., a legacy effect). While magnitude of bleaching differed, immune response patterns were shared among corals harboring heat-sensitive and heat-tolerant Symbiodiniaceae. This supports a pattern of increased constitutive immunity in corals resulting from repeat bleaching events, with greater specialized enzymes (catalase, peroxidase, superoxide dismutase) and attenuated melanin synthesis. C_LIO_LIThis study demonstrates bleaching events have implications for reef corals beyond shaping their ecological assemblages. These events can change the magnitude and/or identity of response variables contributing to physiotype, thus generating physiological legacies carried over into the future. Quantifying baseline coral physiotypes and tracking their shifts will be critical to understanding and forecasting the effects of increased bleaching frequency on coral biology and ecology in the Anthropocene. C_LI

ecology↗