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Matz, M. V.

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

At least 19 recordsLinked to original sources

Environmental drivers of metabolomic profiles within and between cryptic lineages of Montastraea cavernosa, the great star coral

Reef restoration practitioners aim to preserve coral genetic diversity by protecting reefs and cultivating diverse genotypes in coral nurseries. However, cryptic genetic lineages in most corals complicate restoration strategies, as the role of between-lineage genetic divergence remains unclear regarding adaptation. In Montastraea cavernosa, researchers have identified cryptic lineages, some strongly segregated by depth. We conducted a ten-week reciprocal transplantation experiment using two cryptic lineages restricted to shallow water (<10m depth), with one lineage more common on nearshore reefs and the other on offshore reefs. We aimed to quantify lineage-specific responses to the environment that explain the genetic and ecological divergence between the two lineages. Surprisingly, the strongest response was not lineage-specific. Instead, both lineages exhibited strong and similar changes in growth and metabolomic profiles, depending on the transplantation habitat. These results suggest that cryptic lineages employ similar mechanisms of adaptation and acclimatization to environmental challenges, despite their genetic distinction.

ecology↗

MAT-classifier: A memory-efficient pipeline for accurate genus level profiling from ancient metagenomic data

Background: Advances in sequencing technology have expanded opportunities to recover microbial DNA from ancient samples and reconstruct past environments and host-microbe interactions. However, the field remains constrained by computational challenges and accuracy problems, as rare ancient microbial DNA must be distinguished from abundant modern contaminants. Moreover, existing pipelines demand substantial computational resources, particularly memory, limiting their accessibility. Results: Here, we present MAT-classifier, a genus-level profiling workflow for detecting ancient microbial taxa from metagenomic projects, designed to reduce computational requirements while increasing accuracy. Unlike its counterparts, MAT-classifier first consolidates candidate references at the genus level and then performs independent alignments using conventional short-read aligners instead of metagenomic aligners. Using simulated datasets, we showed that this approach achieves more accurate classification of ancient taxa while requiring substantially less memory and shorter runtime than a modern counterpart, the aMeta pipeline. Benchmarking on multiple empirical ancient datasets further confirmed its low memory footprint and practical utility. Conclusions: MAT-classifier provides a reliable, computationally efficient, and accessible framework for ancient microbiome profiling. It lowers computational barriers while maintaining robust classification performance, facilitating broader application of ancient microbial DNA analysis.

genomics↗

The Acropora millepora microbiome is predicted by algal symbionts, host genetics, and environment

The coral microbiome is a critical component of coral health and resilience, yet it is unclear what factors drive coral microbiome composition, especially within the context of coral bleaching. Here, we use whole genome sequencing data combined with a machine learning approach (RDAforest) to assess predictors of the microbiome in 208 colonies of Acropora millepora from 12 reef sites in the Central Great Barrier Reef during a 2016 bleaching event. We characterized microbiome variation using k-mers. While some environmental variables, such as chlorophyll seasonal range and maximum degree heating weeks, were associated with microbiome composition, we find that host genetics and dominant photosymbionts were more powerful predictors. In contrast, bleaching score had negligible predictive power. The corals microbiome therefore correlates with dominant photosymbiont identity even during a bleaching event. The association of the microbiome with the environment suggests that the coral microbiome can serve as a proxy for environmental variation when environment cannot be measured directly, which may be especially useful in ancient DNA studies.

evolutionary biology↗

The microbial fingerprint: fine-scale environmental, genetic, and temporal factors drive the reef metagenome during coral spawning

Understanding the stability of microbial community assembly on coral reefs is crucial for determining their response to changing environments. Here, we evaluate how the marine sediment, water column, and mountainous star coral (Orbicella faveolata) metagenomic communities shift over temporal, spatial, and genetic gradients, centered on the annual coral spawning event on St. Croix, USVI. Using low-coverage shotgun sequencing and a reference-free approach, we characterized metagenomic communities and additionally report 15 metagenome-assembled genomes from environmental samples. We show that diel time can be as important as kilometer-scale distance in structuring the coral-associated and marine sediment community structure, albeit with other highly local factors (genotype, within-reef location) driving most variation. Through multivariate machine learning methods, we find several taxa and metabolic pathways enriched over time, where broad metagenomic community shifts may be linked with concurrent temperature increase or the annual coral spawning event. As understanding the coral microbiome in the context of its environment becomes increasingly important, our research underscores the importance of small-scale variation, both spatially and temporally, in structuring coral reef metagenomic communities.

ecology↗

Environmental drivers of genetic adaptation in two corals from the Florida Keys

Increasingly frequent marine heatwaves devastate coral reefs around the world, so there is great interest in finding warm-adapted coral populations that could be used as sources for assisted gene flow and restoration. Here, we evaluated the relative power of various environmental factors to explain coral genetic variation, suggestive of differential local adaptation to these factors, across the Florida Keys Reef Tract. We applied a machine learning population genomic method (RDAforest) to two coral species - the mustard hill coral Porites astreoides and the lettuce coral Agaricia agaricites - sampled from 65 sites covering the whole reef tract. Both species comprised three genetically distinct lineages distributed across depths in a remarkably similar way. Within these lineages, there was additional genetic variation explained by depth, but even more within-lineage variation was cumulatively explained by water chemistry parameters related to nitrogen, phosphorus, silicate, and salinity. Visualizing the predicted environment-associated genetic variation on a geographic map suggests that these associations reflect adaptation to certain aspects of the inshore-offshore environmental gradient, and, to a lesser extent, to difference of Middle and Lower Keys from the rest of the reef tract. Thermal parameters, most notably maximal monthly thermal anomaly, were also consistently identified as putative drivers of genetic divergence, but had a relatively low explanatory power compared to depth and water chemistry. Overall, our results indicate that temperature is not the most important driver of differential coral adaptation in the Florida Keys, and underscore depth and water chemistry as more important environmental factors from the corals perspective. These findings are relevant for planning assisted gene flow and restoration efforts: not just any warmer reef would be an optimal source of transplants to promote thermal adaptation within the local coral population.

evolutionary biology↗

RDAforest: identifying environmental drivers of polygenic adaptation.

Identifying environmental gradients driving genetic adaptation is one of the major goals of ecological genomics. We present RDAforest, a methodology that leverages the predominantly polygenic nature of adaptation and harnesses the versatility of random forest regression to solve this problem. Instead of computing individual SNP-environment associations, RDAforest seeks to explain the overall genetic covariance structure based on multiple environmental predictors. By relying on random forest instead of linear regression, this method can detect non-linear and non-monotonous dependencies as well as all possible interactions between predictors. It also incorporates a novel procedure to select the best predictor out of several correlated ones, and uses jackknifing to model uncertainty of genetic structure determination. Lastly, our methodology incorporates delineation and plotting of "adaptive neighborhoods" - areas on the landscape that are predicted to harbor differentially adapted individuals. Such maps can be used as a guide for planning conservation and ecological restoration efforts. We demonstrate the use of RDAforest in two simulated scenarios and one real dataset (North American gray wolves).

ecology↗

From juveniles to giants: Drivers of holobiont assembly in massive Porites

The fate of coral reefs in response to climate change depends on their ability to adapt to new environments. The coral animal is buffered from environmental stress by its algal endosymbionts and microbial partners (together, the "holobiont"). However, the flexibility of holobiont community assembly is not well understood, making it difficult to estimate its contribution to coral adaptation. To clarify these processes, we genetically profiled holobiont components (coral, algal symbiont, and microbiome) of massive Porites sampled across two size classes (>2m and <30cm) and ecologically distinct reef sites near Orpheus and Pelorus Islands, Australia. We recovered five major genetic clusters in the coral host, with additional splits within them potentially defining up to ten distinct subclusters. We estimated the relative contributions of the host genetic structure, site, and size class to holobiont community composition. Host genetic structure was the primary driver of both Symbiodiniaceae and microbial communities, indicating strong holobiont specificity in cryptic lineages. In addition, the microbial community was associated with reef site and size class, unlike Symbiodiniaceae that were not significantly affected by either factor. As environmentally segregated, cryptic genetic lineages emerge as a common feature of scleractinian corals, these results emphasize that failure to assess cryptic genetic structure of the coral host may lead to dramatic overestimation of holobiont flexibility.

ecology↗

Decrypting corals: Does regulatory evolution underlie environmental specialization of coral cryptic lineages?

A recent study has shown that two common Caribbean corals, Montastrea cavernosa and Siderastrea siderea, in the Florida Keys each consist of four genetically distinct lineages. These lineages are strongly specialized to a certain depth and, to a lesser extent, to nearshore or offshore habitat. We hypothesized that the lineages environmental specialization is at least in part due to regulatory evolution, which would be manifested as the emergence of groups of coregulated genes ("modules") demonstrating lineage-specific responses to different reef environments. Our hypothesis also predicted that genes belonging to such modules would show greater genetic divergence between lineages than other genes. Contrary to these expectations, responses of cryptic lineages to natural environmental variation were essentially the same at the genome-wide gene coexpression network level. Moreover, none of the identified coregulated gene modules exhibit elevated between-lineage divergence. The environmental specialization of cryptic lineages must, therefore, come from relatively subtle adjustments to gene function or regulation that are not detectable at the gene network level and/or involve other constituents of the coral holobiont rather than the coral host.

evolutionary biology↗

Invertebrate DNA methylation and gene regulation

As human activity alters the planet, there is a pressing need to understand how organisms adapt to environmental change. Of growing interest in this area is the role of epigenetic modifications, such as DNA methylation, in tailoring gene expression to fit novel conditions. Here, we reanalyzed nine invertebrate (Anthozoa and Hexapoda) datasets to validate a key prediction of this hypothesis: changes in DNA methylation in response to some condition correlate with changes in gene expression. While we detected both differential methylation and differential expression, there was no simple relationship between these differences. Hence, if changes in DNA methylation regulate invertebrate transcription, the mechanism does not follow a simple linear relationship.

genomics↗

Codominance of two symbiont genera within the same coral host is associated with elevated symbiont productivity and lower host susceptibility to thermal stress

In recent years, as sea surface temperature increases, many coral species that used to harbor symbionts of the genus Cladocopium have become colonized with the thermally tolerant genus, Durusdinium. Here, we asked how the symbionts of one genus react to the presence of another symbiont genus within the same coral host, and what effect this interaction has on the host. We used previously published transcriptomic data from Acropora hyacinthus corals hosting Cladocopium and/or Durusdinium symbionts and looked at gene expression in all three symbiotic partners depending on the relative proportion of the two symbiont genera within the same host. We find that both Cladocopium and Durusdinium change their expression the most when their proportions within the host are nearly equal (the state that we call "codominance"): both genera elevate expression of photosynthesis and ribosomal genes, suggesting increase in photosynthesis and growth (i.e. higher productivity). At the same time, the coral host also elevates production of ribosomes suggesting faster cellular growth, and, when heated, shows less pronounced stress response. These results can be explained in two alternative ways. One explanation is that increased competition between codominant symbionts switches them to the higher productivity mode, which benefits the host, making it more resilient to stress. Alternatively, the symbionts elevated productivity might be not the cause but the consequence of the host being particularly healthy. Under this explanation, rapid growth of the healthy host creates new space, lowering the symbioints competition and thus promoting their growth, which allows for codominance to happen where one genus would otherwise outcompete another. The latter explanation is supported by the fact that codominance is associated with lower symbiont densities, assessed as relative proportions of symbiont reads in the data. Irrespective of the causation direction, the presence of mixed symbiont communities could potentially be used as an instant indicator of coral well-being, which would be a useful tool for coral conservation and restoration.

evolutionary biology↗

Comparative neurotranscriptomics reveal widespread species differences associated with bonding

BackgroundPair bonding with a reproductive partner is rare among mammals but is an important feature of human social behavior. Decades of research on monogamous prairie voles (Microtus ochrogaster), along with comparative studies using the related non-bonding meadow vole (M. pennsylvanicus), have revealed many of the neural and molecular mechanisms necessary for pair-bond formation in that species. However, these studies have largely focused on just a few neuromodulatory systems. To test the hypothesis that neural gene expression differences underlie differential capacities to bond, we performed RNA-sequencing on tissue from three brain regions important for bonding and other social behaviors across bond-forming prairie voles and non-bonding meadow voles. We examined gene expression in the amygdala, hypothalamus, and combined ventral pallidum/nucleus accumbens in virgins and at three time points after mating to understand species differences in gene expression at baseline, in response to mating, and during bond formation. ResultsWe first identified species and brain region as the factors most strongly associated with gene expression in our samples. Next, we found gene categories related to cell structure, translation and metabolism that differed in expression across species in virgins, as well as categories associated with cell structure, synaptic and neuroendocrine signaling, and transcription and translation that varied among the focal regions in our study. Additionally, we identified genes that were differentially expressed across species after mating in each of our regions of interest. These include genes involved in regulating transcription, neuron structure, and synaptic plasticity. Finally, we identified modules of co-regulated genes that were strongly correlated with brain region in both species, and modules that were correlated with post-mating time points in prairie voles but not meadow voles. ConclusionsThese results reinforce the importance of pre-mating differences that confer the ability to form pair bonds in prairie voles but not promiscuous species such as meadow voles. Gene ontology analysis supports the hypothesis that pair-bond formation involves transcriptional regulation, and changes in neuronal structure. Together, our results expand knowledge of the genes involved in the pair bonding process and open new avenues of research in the molecular mechanisms of bond formation.

neuroscience↗

Environmental specialization and cryptic genetic divergence in two massive coral species from the Florida Keys Reef Tract

Broadcast-spawning coral species have wide geographic ranges, spanning strong environmental gradients, but it is unclear how much spatially varying selection these gradients actually impose. Strong divergent selection might present a considerable barrier for demographic exchange between disparate reef habitats. We investigated whether the cross-shelf gradient (nearshore - offshore - deep) is associated with spatially varying selection in two common coral species, Montastraea cavernosa and Siderastrea siderea, in the Florida Keys. Toward this end, we generated a de novo genome assembly for M. cavernosa and used 2bRAD to genotype 20 juveniles and 20 adults of both species from each of the three reef zones to identify signatures of selection occurring within a single generation. Unexpectedly, each species was found to be composed of four genetically distinct lineages, with gene flow between them still ongoing but highly reduced in 13.0-54.7% of the genome. Each species includes two sympatric lineages that are only found in the deep (20 m) habitat, while the other lineages are found almost exclusively on the shallower reefs (3-10 m). The two "shallow" lineages of M. cavernosa are also specialized for either nearshore or offshore: comparison between adult and juvenile cohorts indicates that cross-shelf migrants are more than twice as likely to die before reaching adulthood than local recruits. Siderastrea siderea and M. cavernosa are among the most ecologically successful species on the degraded Florida Keys Reef Tract, and this work offers important insight on the genomic background of divergent selection and environmental specialization that may in part explain their resilience and broad environmental range.

evolutionary biology↗

Gene expression associated with disease resistance and long-term growth in a reef-building coral

Rampant coral disease, exacerbated by climate change and other anthropogenic stressors, threatens reefs worldwide, especially in the Caribbean. Physically isolated yet genetically connected reefs such as Flower Garden Banks National Marine Sanctuary (FGBNMS) may serve as potential refugia for degraded Caribbean reefs. However, little is known about the mechanisms and trade-offs of pathogen resistance in reef-building corals. Here we measure pathogen resistance in Montastraea cavernosa from FGBNMS. We identified individual colonies that demonstrated resistance or susceptibility to Vibrio spp. in a controlled laboratory environment. Long-term growth patterns suggest no trade-off between disease resistance and calcification. Predictive (pre-exposure) gene expression highlights subtle differences between resistant and susceptible genets, encouraging future coral disease studies to investigate associations between resistance and replicative age and immune cell populations. Predictive gene expression associated with long-term growth underscores the role of cation transporters and extracellular matrix remodelers, contributing to the growing body of knowledge surrounding genes that influence calcification in reef-building corals. Together these results demonstrate that coral genets from isolated sanctuaries such as FGBNMS can withstand pathogen challenges and potentially aid restoration efforts in degraded reefs. Furthermore, gene expression signatures associated with resistance and long-term growth help inform strategic assessment of coral health parameters.

genomics↗

Multilevel community assembly of the tadpole gut microbiome

The assembly of local communities is likely to reflect the effects of local environmental factors associated with filters that act at larger spatial scales. Dissecting these multiscale effects remains a timely challenge that is particularly important for host-associated microbiomes. We investigated the relative roles of local selection (due to host species identity) and regional effects (due to water body identity) on the community structure of bacteria in the gut of tadpoles from three biogeographic areas and used graph theory and metanetwork approaches to explore and illustrate the distribution of bacteria across different ponds. The pond of origin, which represents a regional species pool of bacteria, was in general more important in shaping the gut microbiome of tadpoles than host species identity. The resulting metanetworks are modular and indicate relatively few species of bacteria occurring in more than one pond. Thus, each pond represents a relatively distinct species pool of bacteria available for community assembly of the tadpole microbiomes. Our findings indicate that microbiome community assembly in amphibian larvae, as in many other communities, is a multiscale process with important regional effects that constrain how local (i.e. host-dependent) filters act to influence microbiome community composition.Competing Interest StatementThe authors have declared no competing interest.View Full Text

ecology↗

Co-recruitment of relatives in a broadcast-spawning coral (Acropora hyacinthus) facilitates emergence of an inbred, genetically distinct group within a panmictic population

Many broadly-dispersing marine taxa are species-rich, show genetic heterogeneity on small spatial scales, and are locally adapted to their environmental conditions. How such genetic subdivisions can emerge despite the potential for high gene flow continues to be the major paradox of evolution in the sea. One understudied process potentially contributing to genetic structuring in marine populations is variation in larval recruitment. Here, we report an unusual recruitment pattern in the broadcast-spawning coral species Acropora hyacinthus on Yap Island, Micronesia. Reduced representation genotyping of 275 individuals of varying size classes on this isolated reef system demonstrated general island-wide panmixia but also identified a genetically divergent group of juvenile corals at one out of the four sites sampled, showing elevated inbreeding and relatedness, including two pairs of siblings. Notably, adult corals as well as the majority of juveniles at the same site belong to the panmictic gene pool, suggesting that representatives of the inbred lineage of juveniles co-recruited and may be partially reproductively isolated from the rest of the island population. Reproductive isolation is suggested by the discovery of distinct genomic regions of greatly reduced genetic diversity in the inbred lineage, encompassing genes involved in sperm-egg recognition and fertilization that may serve as reproductive barrier loci. We propose that co-recruitment of genetic relatives via cohesive dispersal, a process that was previously unrecognized in broadcast-spawning corals, can generate familial genetic structure and might be important for the emergence of genetically distinct, locally adapted ecomorphs and cryptic species.

evolutionary biology↗

Benchmarking DNA Methylation Assays for Marine Invertebrates

Interrogation of chromatin modifications, such as DNA methylation, has potential to improve forecasting and conservation of marine ecosystems. The standard method for assaying DNA methylation (Whole Genome Bisulfite Sequencing), however, is too costly to apply at the scales required for ecological research. Here we evaluate different methods for measuring DNA methylation for ecological epigenetics. We compare Whole Genome Bisulfite Sequencing (WGBS) with Methylated CpG Binding Domain Sequencing (MBD-seq), and a modified version of MethylRAD we term methylation-dependent Restriction site-Associated DNA sequencing (mdRAD). We evaluate these three assays in measuring variation in methylation across the genome, between genotypes, and between polyp types in the reef-building coral Acropora millepora. We find that all three assays measure absolute methylation levels similarly, with tight correlations for methylation of gene bodies (gbM), as well as exons and 1Kb windows. Correlations for differential gbM between genotypes were weaker, but still concurrent across assays. We detected little to no reproducible differences in gbM between polyp types. We conclude that MBD-seq and mdRAD are reliable cost-effective alternatives to WGBS. Moreover, the considerably lower sequencing effort required for mdRAD to produce comparable methylation estimates makes it particularly useful for ecological epigenetics.

ecology↗

Population genetics of the coral Acropora millepora: Towards a genomic predictor of bleaching

Although reef-building corals are rapidly declining worldwide, responses to bleaching vary both within and among species. Because these inter-individual differences are partly heritable, they should in principle be predictable from genomic data. Towards that goal, we generated a chromosome-scale genome assembly for the coral Acropora millepora. We then obtained whole genome sequences for 237 phenotyped samples collected at 12 reefs distributed along the Great Barrier Reef, among which we inferred very little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin. We further used 213 of the samples to conduct a genome-wide association study of visual bleaching score, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for the use of genomics-based approaches in conservation strategies.

evolutionary biology↗

Meta-analysis of the General Coral Stress Response: Acropora corals show opposing responses depending on stress intensity

As climate change progresses, reef-building corals must contend more often with suboptimal conditions, motivating a need to understand coral stress response. Here we test the hypothesis that there is a stereotyped transcriptional response that corals enact under any stressful conditions, functionally characterized by downregulation of growth and activation of cell death, response to reactive oxygen species, immunity, and protein homeostasis. We analyze RNA-seq and Tag-Seq data from 14 previously published studies and supplement them with four new experiments involving different stressors, totaling over 600 gene expression profiles from the genus Acropora. Contrary to expectations, we found not one, but two distinct types of response. The type A response was observed under all kinds of high-intensity stress, showed strong correlations between independent projects, and was functionally consistent with the hypothesized stereotyped response. Higher similarity of type A responses irrespective of stress type supports its role as the General Coral Stress Response providing a blanket solution to severely stressful conditions. The distinct type B response was observed under lower intensity stress and was weaker and more variable among studies than type A. Unexpectedly, the type B response was broadly opposite the type A response: biological processes up-regulated under type A response tended to be down-regulated under type B response, and vice versa. Gene network analysis indicated that type B response does not involve specific co-regulated gene groups and is simply the opposite of type A response. We speculate that these paradoxically opposing responses may result from an inherent negative association between stress response and cell proliferation.

genomics↗