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Eirin-Lopez, J. M.

Publications and source records attributed to Eirin-Lopez, J. M..

5 recordsLinked to original sources

Cross-talk among miRNAs, lncRNAs, and DNA methylation in three coral species reveal conserved epigenetic regulatory architecture

Epigenetic mechanisms support phenotypic plasticity across metazoans, enabling dynamic response to environmental change. DNA methylation and non-coding RNAs, including microRNAs (miRNAs) and long non-coding RNAs (lncRNAs), regulate gene expression through distinct but interconnected mechanisms. In vertebrate systems, these layers form integrated networks in which specific miRNAs directly target the protein machinery of other epigenetic processes ("epi-miRNAs") and specialized lncRNAs act as competing endogenous RNAs (ceRNAs), sequestering miRNAs from their mRNA targets. Whether equivalent cross-layer regulatory architectures exist in cnidarians, whose methylomes are invertebrate-characteristic and whose miRNAs function mechanistically like those of plants, is unknown. Here we integrate matched RNA-seq, small RNA-seq, and whole-genome bisulfite sequencing across three species of reef-building coral (Acropora pulchra, Porites evermanni, and Pocillopora tuahiniensis) to characterize the landscape and regulatory interactions of microRNAs (miRNAs), long non-coding RNAs (lncRNAs) and DNA methylation, including the first description of epi-miRNAs and ceRNA networks in cnidarian taxa. Across the study species, miRNAs putatively targeted transcripts encoding a suite of epigenetic processes, including DNA methylation regulators (TET3, MBD, PRDM14), ubiquitin-signaling and histone-modifying machinery, and components of the miRNA pathway itself (e.g., AGO, TNRC6). The conserved miRNA miR-100 also exhibited species-divergent target coexpression, suggesting lineage-specific regulatory roles for deeply conserved miRNAs. Candidate ceRNA networks were also recovered, including predicted derepression of epimachinery transcripts, indicating that lncRNA-mediated buffering operates alongside direct miRNA control. Recovery of these regulatory interactions across three evolutionarily divergent species, despite few orthologous miRNA or lncRNA, suggests that multi-layered epigenetic regulation is a conserved feature of cnidarian biology. These results establish direct miRNA and lncRNA control of epigenetic machinery as an active component of coral gene regulation, and provide foundational resources for studying how multilayered epigenetic interactions contribute to coral resilience to environmental change. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=140 SRC="FIGDIR/small/739451v1_ufig1.gif" ALT="Figure 1"> View larger version (29K): org.highwire.dtl.DTLVardef@7e07dforg.highwire.dtl.DTLVardef@36cf0forg.highwire.dtl.DTLVardef@5406d3org.highwire.dtl.DTLVardef@8c09e3_HPS_FORMAT_FIGEXP M_FIG C_FIG

molecular biology↗

Seasonal plasticity of symbiotic strategies clarifies coral holobiont resistance and resilience

As coral reefs face unprecedented declines driven by thermal stress and the breakdown of coral symbiosis (i.e., coral bleaching), restoration efforts increasingly rely on coral health and resilience rankings. However, seasonal plasticity in symbiosis and holobiont metabolism, along with the presence of cryptic species, can complicate data interpretation. Therefore, quantifying seasonal plasticity in coral physiology and incorporating genetic identification are essential for accurately interpreting and drawing conclusions from trait-based and fitness-based analyses. To test the effect of seasonal and site variation on physiological plasticity we sampled three ecologically dominant genera, Acropora, Pocillopora, and Porites across three lagoon sites (n=15 tagged colonies genus-1 site-1) on the north shore of Moorea French Polynesia in January, March, September, and December of 2020. We identified coral host and intracellular symbiotic Symbiodiniaceae to the highest taxonomic resolution possible and quantified 13 physiological variables within the holobiont. Genetic analyses identified A. pulchra along with cryptic lineages in Pocillopora (P. meandrina, P. tuahiniensis) and Porites (P. evermanni, P. lobata/lutea). A. pulchra was dominated by Durusdinium trenchii and also contained Symbiodinium microadriaticum. Symbiont communities differed between cryptic congeners, with P. meandrina hosting Cladocopium latusorum and P. tuahiniensis hosting Cladocopium pacificum, whereas P. evermanni and P. lobata/lutea both hosted Cladocopium (C15), but each with unique C15 profiles. Weedy taxa such as Acropora and Pocillopora displayed a cycle of symbiont boom and bust in response to seasonally variable light and temperature, likely contributing to the high stress sensitivity of these taxa. In contrast, despite seasonal environmental variability, Porites displayed greater symbiont stability, with temperature--rather than light--serving as the stronger explanatory variable of seasonal variation in host physiology. Increased host biomass under cooler conditions, which provides energy reserves, may serve as an important stabilizing factor in massive Porites well-documented stress resilience. Collectively, our data provide essential evidence of the need for integrative analyses considering baseline physiological states across seasons along with host and symbiont genetics, particularly in light of the plethora of climate change related stress test assays taking place throughout the year across coral taxa with cryptic lineages.

physiology↗

Non-coding RNA Repertoire in Reef-Building Corals

Non-coding RNAs (ncRNAs) play critical regulatory roles in gene expression regulation that influences diverse biological processes in response to environmental change. Yet their characterization in non-model organisms, particularly sessile, benthic ecosystem engineers such as reef-building corals that are sensitive to climate change, remains limited. This study provides the first comprehensive analysis of the ncRNA repertoire of species from three ecologically important coral genera from Moorea, French Polynesia: Acropora pulchra, Pocillopora tuahiniensis, and Porites evermanni. These species demonstrate differing symbiotic partners, life history strategies, and physiological traits, offering a broad framework for documenting ncRNA variation in corals. We identified homologs for ncRNA biogenesis and functional machinery, characterized long ncRNAs (lncRNAs), microRNAs (miRNAs), and piwiRNAs (piRNAs), and assessed their genomic context and potential targets. Our findings reveal the presence of conserved ncRNA machinery across these coral species, indicating their capability to generate and utilize ncRNAs for the regulation of gene expression. We identified only a single miRNA conserved with corals and Eumetazoans (miR-100), four miRNAs shared across all three species, previously identified in other cnidarian taxa (miR-100, miR-2023, miR-2025, miR-2036), as well as several species-specific miRNAs. Predicted gene targets of the characterized miRNAs included immune response regulation in A. pulchra and P. tuahiniensis and signal transduction pathways in P. evermanni and P. tuahiniensis. Proximity analysis indicated >71-99% of piRNAs overlapped with genes, with genomic maintenance and stability identified as the primary functional enrichment of those genes. Our characterization of lncRNAs found little sequence overlap across each species (<2%), although lncRNAs in all three species were often in proximity to immune-related genes. This study lays the groundwork for the repertoire and regulatory roles of ncRNAs in reef-building corals, thereby expanding our understanding of epigenetic regulation in environmentally sensitive marine invertebrates and its potential implications in acclimatization and adaptation to environmental change.

molecular biology↗

The protamines of the noble false widow spider Steatoda nobilis provide an example of liquid-liquid phase separation chromatin transitions during spermiogenesis

While there is extensive information about sperm nuclear basic proteins (SNBP) in vertebrates, there is very little information about Arthropoda by comparison. This paper aims to contribute to filling this gap by analyzing these proteins in the sperm of the noble false widow spider Steatoda nobilis (Order Araneae, Family Theridiidae). To this end, we have developed a protein extraction method that allows the extraction of cysteine-containing protamines suitable for the preparation and analysis of SNBPs from samples where the amount of starting tissue material is limited. We carried out top-down mass spectrometry sequencing and molecular phylogenetic analyses to characterize the protamines of S. nobilis and other spiders. We also used electron microscopy to analyze the chromatin organization of the sperm, and we found it to exhibit liquid-liquid phase spinodal decomposition during the late stages of spermiogenesis. These studies further our knowledge of the distribution of SNBPs within the animal kingdom and provide additional support for a proposed evolutionary origin of many protamines from a histone H1 (H5) replication-independent precursor.

biochemistry↗

Invertebrate methylomes provide insight into mechanisms of environmental tolerance and reveal methodological biases

There is a growing focus on the role of DNA methylation in the ability of marine invertebrates to rapidly respond to changing environmental factors and anthropogenic impacts. However, genome-wide DNA methylation studies in non-model organisms are currently hampered by limited understanding of methodological biases. Here we compare three methods for quantifying DNA methylation at single base-pair resolution -- Whole Genome Bisulfite Sequencing (WGBS), Reduced Representation Bisulfite Sequencing (RRBS), and Methyl-CpG Binding Domain Bisulfite Sequencing (MBDBS) -- using multiple individuals from two reef-building coral species with contrasting environmental sensitivity. All methods reveal substantially greater methylation in Montipora capitata (11.4%) than the more sensitive Pocillopora acuta (2.9%). The majority of CpG methylation in both species occurs in gene bodies and flanking regions. In both species, MBDBS has the greatest capacity for detecting CpGs in coding regions at our sequencing depth, however MBDBS may be influenced by intra-sample methylation heterogeneity. RRBS yields robust information for specific loci albeit without enrichment of any particular genome feature and with significantly reduced genome coverage. Relative genome size strongly influences the number and location of CpGs detected by each method when sequencing depth is limited, illuminating nuances in cross-species comparisons. As genome-wide methylation differences, supported by data across bisulfite sequencing methods, may contribute to environmental sensitivity phenotypes in critical marine invertebrate taxa, these data provide a genomic resource for investigating the functional role of DNA methylation in environmental tolerance.

genomics↗