bioRxiv Science⌕ Search

Biology subjects

Vermeij, M. J. A.

Publications and source records attributed to Vermeij, M. J. A..

11 recordsLinked to original sources

Baseline microbiomes of the pillar coral Dendrogyra cylindrus reveal novel taxa and regional differences

The pillar coral Dendrogyra cylindrus is a rare but iconic member of Caribbean reefs that has suffered range-wide losses. D. cylindrus is highly susceptible to stony coral tissue loss disease (SCTLD), and the outbreak has contributed to the functional extinction of Floridas population of pillar corals. The coral microbiome can impact the health and disease resistance of coral colonies, yet little is known about what constitutes the core microbiome of D. cylindrus. This information is crucial for comparisons of healthy and diseased tissue in pathogen identification studies and can be applied to restoration efforts as a coral health metric. Therefore, we characterized the microbiomes of D. cylindrus colonies ahead of the SCTLD disease front in Belize and Curacao. The most prevalent members of the D. cylindrus microbial community were bacteria for which taxonomy could not be assigned confidently beyond the level of domain as well as the putatively endosymbiotic genera Endozoicomonas, Ca. Amoebophilus, and Spiroplasma. The coral reefs of Belize and Curacao represent distinct Caribbean marine ecoregions, and we documented regional differences in strains among predominant bacterial taxa. The understudied microbiome of D. cylindrus harbors unique bacterial lineages that are in danger of extinction along with its critically endangered coral host, and these bacterial lineages may be important bioindicators during restoration efforts. IMPORTANCETropical corals face global extinction if average temperatures rise by 2{degrees}C (3.6{degrees}F), which may occur as soon as 2050. Included in the loss of charismatic macrofauna like the majestic pillar coral is the loss of the biological and genetic diversity of its symbionts. Here we examined the bacterial and archaeal communities associated with Caribbean pillar corals and found that the microbiome was dominated by taxonomically unclassified and putatively endosymbiotic taxa. Endosymbiotic bacteria, which live inside the coral tissue, are likely to have evolved unique adaptations to become symbionts and may be important to the health and success of pillar corals in ecosystem restoration efforts.

microbiology↗

Global diversity and distribution of coral-associated protists

Coral reefs are critical ecosystems and biodiversity hotspots that provide ecological stability and essential services to coastal communities. The coral holobiont, a complex symbiotic system composed of the coral animal and a diverse array of associated microbes, plays a central role in coral health and resilience. While Symbiodiniaceae and bacterial symbionts have been extensively studied, much less is known about the diversity and function of microbial eukaryotes such as protists and fungi. These organisms are increasingly recognized as important, yet remain vastly underexplored. Here, we present the first global survey of the coral-associated eukaryome using an anti-metazoan 18S rRNA primer set to bypass host DNA amplification. Our dataset includes corals and related anthozoans from the Caribbean Sea, the Red Sea, and several locations in the Pacific Ocean, spanning a broad taxonomic and geographic range, and includes both healthy and diseased specimens. They reveal a eukaryome that is not only more diverse than that of global coastal waters but also surpasses the diversity of the well-studied coral bacterial microbiome. We recover diverse microbial eukaryotic communities, including Symbiodiniaceae, other known symbionts, potential pathogens, and previously uncharacterized lineages. These results reveal consistent patterns across coral groups and geographic regions. This study provides the most comprehensive taxonomic overview of coral-associated microbial eukaryotes to date, offering new insights into their roles within the holobiont. Our findings highlight the ecological significance of microbial eukaryotes and underscore the importance of incorporating them into broader coral reef research and conservation strategies.

microbiology↗

From SCUBA to spectra: Broadly applicable methods for coral metabolomics research

Corals represent a complex assemblage consisting of a host cnidarian, symbiotic dinoflagellate microalgae, and associated microbiomes and viromes, collectively called the coral holobiont. Corals are foundational to tropical reefs, yet their global decline due to climate change and other stressors creates an uncertain future for this valuable ecosystem. Metabolomics is a powerful means to unravel biochemical interactions within the holobiont that underpin coral resilience and adaptation. However, the remote nature of reefs and the analytical demands of this technique often limit its application. Untargeted metabolomics presents analytical challenges that are amplified in complex samples like corals, such as identifying the biological source of metabolites. Here, we evaluate how different sample fixation methods and time delays before storage--unavoidable in field contexts--affect coral metabolome profiles. We further present a framework for mapping metabolites in holobiont samples to their coral host and algal symbiont origins and introduce a spectral library to improve and automate annotation of coral lipids. Additionally, we demonstrate how single samples can be used concurrently for metabolomics, DNA amplification, and proteomics. Together, our study provides a streamlined, field-adaptable workflow for coral metabolomics that enables larger-scale studies and broader adoption of metabolomics in coral reef research and conservation.

biochemistry↗

Temporal transcriptional rhythms govern coral-symbiont function and microbiome dynamics

Diel rhythms align physiological processes with light/dark cycles, driving predictable oscillations in gene expression and protein activity through tightly controlled transcriptional-translational feedback loops. Transcriptomic analyses in the stony coral Pseudodiploria strigosa revealed tightly regulated transcriptional control: dawn triggers a molecular reset marked by RNA metabolism and protein turnover; midday emphasizes anabolic and phosphate-regulated pathways; dusk reflects transitional lipid and amino acid metabolism; and midnight reveals stress-responses, mRNA catabolism, and mitochondrial organization. The photosymbiont Breviolum sp. exhibits subtler but distinct diel regulation, with photoprotective activation at dawn, metabolite transport and nitrogen cycling through midday and dusk, and cell cycle and ion homeostasis at night. Microbial communities show time-dependent restructuring of co-occurrence networks. Carbohydrate-catabolizing taxa associated with Symbiodiniaceae during daylight, while nighttime assemblages feature methylotrophs likely facilitating dimethylsulfoniopropionate (DMSP) metabolism. Together, these findings present the first system-level molecular framework of diel regulation across the coral-photosymbiont-microbe holobiont, revealing strong time-specific transcriptional control as a key driver of coordinated function and homeostasis. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=190 SRC="FIGDIR/small/668741v1_ufig1.gif" ALT="Figure 1"> View larger version (61K): org.highwire.dtl.DTLVardef@1cb5740org.highwire.dtl.DTLVardef@cd58ceorg.highwire.dtl.DTLVardef@1815777org.highwire.dtl.DTLVardef@9550a8_HPS_FORMAT_FIGEXP M_FIG C_FIG

molecular biology↗

Viral and bacterial traits associated with the success of the yellow pencil coral, Madracis mirabilis, in Curacaos coral reefs

Coral reefs have experienced extensive coral loss and shifts in community composition worldwide. Despite this, some coral species appear naturally more resistant, such as Madracis mirabilis (herein Madracis). Madracis has emerged as the dominant hard coral in Curacao, comprising 26% of coral cover in reefs that declined by 78% between 1973 and 2015. Although life history traits and competitive mechanisms contribute to Madracis success, these factors alone may not fully explain it, as other species with similar traits have not shown comparable success. Here, we investigated the potential role of microbial communities in the success of Madracis on Curacao reefs by leveraging a low-bias bacterial and viral enrichment method for metagenomic sequencing of coral samples, resulting in 77 unique bacterial metagenome-assembled genomes and 2,820 viral genomic sequences. Our analyses showed that Madracis-associated bacterial and viral communities are 1.24-fold and 1.61-fold richer than the communities of five sympatric coral species combined. The Madracis-associated bacterial community was dominated by Ruegeria and Sphingomonas, genera that have previously been associated with coral health, defense against pathogens, and bioremediation. The viral community exhibited a 50% enrichment of proviruses relative to the viral communities of other corals. These proviruses have the genomic capacity to laterally transfer genes involved in antibiotic resistance, central metabolism, and oxidative stress responses, potentially enhancing the adaptive capacity of the Madracis microbiome and contributing to Madracis success on Curacaos reefs. IMPORTANCEUnderstanding why some coral species persist and thrive while most are in fast decline is critical. Madracis mirabilis is increasingly dominant on degraded reefs in Curacao, yet the role of microbial communities in its success remains underexplored. This study highlights the potential role of Madracis-associated bacterial and viral communities in supporting coral resilience and competitive success. By identifying key microbial partners and viral genes that may enhance host stress tolerance and defense against pathogens, we broaden the understanding of how the coral holobiont contributes to species persistence under environmental stress. These insights are valuable for predicting reef community shifts in a changing climate and open avenues for microbiome-informed strategies to support coral conservation and restoration.

microbiology↗

Fireworms (Hermodice carunculata) are a reservoir and potential vector for coral-infecting apicomplexans

Corals (Cnidaria; Anthozoa) play critical roles as habitat-forming species with a wide range, from warm shallow-water tropical coral reefs to cold-water ecosystems [1-3]. They also represent a complex ecosystem as intricate holobionts made up of microbes from all domains of the Tree of Life, that can play significant roles in host health and fitness [4]. The corallicolids are a clade of apicomplexans that infect a wide variety of anthozoans across the world, and can influence the thermal tolerance of habitat-forming corals [1, 5]. Despite their potentially important impacts on reef ecosystems, much of the basic biology and ecology of corallicolids remains unclear. Apicomplexans often have a closed life cycle, with minimal environmental exposure, and sometimes multiple hosts. Corallicolids have only been documented in anthozoan hosts, with no known secondary/reservoir hosts or vectors [6]. Here, we show that abundant corallicolid sequences are recovered from bearded fireworms (Hermodice carunculata) in tropical reef habitats off Curacao, and that they are distinct from corallicolids infecting the corals on which the fireworms were feeding at the time of their collection. The data are consistent with an active infection of fireworms, as opposed to corallicolids being a byproduct of feeding on infected corals, and we suggest that H. carunculata is potentially a vector moving corallicolids among coral hosts through its faeces. These findings not only expand our understanding of the ecological interactions within coral reef ecosystems but also highlight the potential role of host-associated parasites in shaping the resilience of reef habitats.

microbiology↗

Mixed clonal-aggregative multicellularity entrained by extreme salinity fluctuations in a close relative of animals

Multicellularity evolved multiple times independently during eukaryotic diversification1-4. Two distinct mechanisms underpin multicellularity5: clonality (serial cell division without sister-cell separation) and aggregation (whereby independent cells assemble into a multicellular entity). Clonal and aggregative multicellularity are traditionally considered mutually exclusive1,6-9, with rare exceptions10, and evolutionary hypotheses have addressed why multicellularity might diverge toward one or the other extreme3,4. Both animals and their sister group, the choanoflagellates, are currently only known to acquire multicellularity clonally4,11-13. Here, we show that the choanoflagellate Choanoeca flexa14 forms motile and contractile cell monolayers (or "sheets") through multiple mechanisms: C. flexa sheets can form purely clonally, purely aggregatively, or by a combination of both processes. We characterise the life history of C. flexa in its natural environment - ephemeral splash pools on the island of Curacao - and show that C. flexa undergoes reversible transitions between unicellularity and multicellularity during cycles of evaporation and refilling. Different splash pools house genetically distinct strains of C. flexa, between which aggregation is constrained by kin recognition15-18. We show that clonal-aggregative multicellularity serves as a versatile strategy for the robust re-establishment of multicellularity in this variable and fast-fluctuating environment. Our findings challenge former generalisations about choanoflagellates and expand the option space of choanozoan multicellularity.

evolutionary biology↗

Evidence for a biological source of widespread, reproducible nighttime oxygen spikes in tropical reef ecosystems has implications for coral health

Primary producers release oxygen as the by-product of photosynthetic light reactions during the day. However, a prevalent, globally-occurring nighttime spike in dissolved oxygen in the absence of light challenges the traditional assumption that biological oxygen production is limited to daylight hours, particularly in tropical coral reefs. Here we show: 1) the widespread nature of this phenomenon, 2) its reproducibility across tropical marine ecosystems, 3) the influence of biotic and abiotic factors on this phenomenon across numerous datasets, and 4) the observation of nighttime oxygen spikes in vitro from incubations of coral reef benthic organisms. The data from this study demonstrate that in addition to physical forcing, biological processes are likely responsible for increasing dissolved oxygen at night. Additionally, we demonstrate an association between these nighttime oxygen spikes and measures of both net community calcification and net community production. These results suggest that nighttime oxygen spikes are likely a biological response associated with increased respiration and are most prominent in communities dominated by calcifying organisms.

ecology↗

SUCCESSFUL DEMONSTRATION OF ASSISTED GENE FLOW IN THE THREATENED CORAL ACROPORA PALMATA ACROSS GENETICALLY-ISOLATED CARIBBEAN POPULATIONS USING CRYOPRESERVED SPERM

Global change will compromise the population sizes, species ranges, and survival of economically-important plants and animals, including crops, aquaculture species, and foundational ecosystem builders. Scleractinian reef-building corals are a particular concern because they are slow-growing, long-lived, environmentally-sensitive, and concentrated in the warmest regions of the ocean. Assisted Gene Flow (AGF) is considered a viable tool to help natural plant and animal populations, including corals, adapt to changing environments. Our goal was to test for the first time whether cryopreserved coral sperm could be used to facilitate assisted gene flow between genetically-isolated populations of a Caribbean coral. We collected, pooled, and cryopreserved coral sperm from the threatened Caribbean coral Acropora palmata in the western Caribbean (Key Largo, FL), central Caribbean (Rincon, Puerto Rico), and eastern Caribbean (Curacao). Alongside freshly-collected sperm from Curacao, the cryopreserved sperm from each of these populations was used for in vitro fertilization experiments with freshly-collected eggs from Curacao. Across five egg donors, average fertilization success was 91 to 99% for CUR x CUR (fresh sperm) crosses, 37 to 82% for CUR x CUR (frozen sperm) crosses, 3 to 19% for CUR x FL (frozen sperm) crosses and 0 to 24% for CUR x PR (frozen sperm) crosses. Notably, fertilization was achieved in all four categories of crosses, showing for the first time through direct evidence that populations of A. palmata are reproductively compatible, and that genetic diversity can be transferred from one population to another for the purposes of assisted gene flow. The resulting larvae were reared in Curacao for up to 7 days, then the swimming larvae were transported to Florida for settlement and grow-out at two separate facilities, which achieved larval settlement rates of 37 to 60% across all cohorts. Larvae were reared and settled in Florida to acclimate them to the ambient water quality, microbial environment, and temperature regimes of the western genetic A. palmata population as early in their life cycle as possible. At one month, over 54% all settlers had survived, including over 3500 settlers from CUR x CUR (frozen sperm), 1200 settlers from CUR x FL (frozen sperm), and 230 settlers from CUR x PR (frozen sperm). These experiments represent the first-ever pan-Caribbean coral crosses produced in captivity and the first direct evidence that geographically-separated and genetically-isolated populations of any Caribbean coral are reproductively compatible. Moreover, with over 4700 A. palmata settlers produced using cryopreserved sperm, this represents the largest living wildlife population ever created from cryopreserved material. Together, these findings demonstrate that cryopreservation of coral sperm can enable efficient, large-scale assisted gene flow in corals. This form of assisted migration can not only help to preserve the population-level genetic diversity of extant coral populations but also help to increase population resilience to global change.

zoology↗

A widespread coral-infecting apicomplexan contains a plastid encoding chlorophyll biosynthesis

The Apicomplexa are an important group of obligate intracellular parasites that include the causative agents of human diseases like malaria and toxoplasmosis. They evolved from free-living, phototrophic ancestors, and how this transition to parasitism occurred remains an outstanding question. One potential clue lies in coral reefs, where environmental DNA surveys have uncovered several lineages of uncharacterized, basally-branching apicomplexans. Reef-building corals form a well-studied symbiotic relationship with the photosynthetic dinoflagellate Symbiodinium, but identification of other key microbial symbionts of corals has proven elusive. Here, we used community surveys, genomics, and microscopy to identify an apicomplexan lineage, which we name corallicola, that was found in high prevalence (>80%) across all major groups of corals. In-situ fluorescence and electron microscopy confirmed that corallicola lives intracellularly within the tissues of the coral gastric cavity, and possesses clear apicomplexan ultrastructural features. We sequenced the plastid genome, which lacked all genes for photosystem proteins, indicating that corallicola harbours a non-photosynthetic plastid (an apicoplast). However, the corallicola plastid differed from all other known apicoplasts because it retains all four genes involved in chlorophyll biosynthesis. Hence, corallicola shares characteristics with both its parasitic and free-living relatives, implicating it as an evolutionary intermediate, and suggesting that a unique ancestral biochemistry likely operated during the transition from phototrophy to parasitism.

microbiology↗

Relevance of coral geometry in the outcomes of the coral-algal benthic war

Corals have built reefs on the benthos for millennia, becoming an essential element in marine ecosystems. Climate change and human impact, however, are favoring the invasion of non-calcifying benthic algae and reducing coral coverage. Corals rely on energy derived from photosynthesis and heterotrophic feeding, which depends on their surface area, to defend their outer perimeter. But the relation between geometric properties of corals and the outcome of competitive coral-algal interactions is not well known. To address this, 50 coral colonies interacting with algae were sampled in the Caribbean island of Curacao. 3D and 2D digital models of corals were reconstructed to measure their surface area, perimeter, and polyp sizes. A box counting algorithm was applied to calculate their fractal dimension. The perimeter and surface dimensions were statistically non-fractal, but differences in the mean surface fractal dimension captured relevant features in the structure of corals. The mean fractal dimension and surface area were negatively correlated with the percentage of losing perimeter and positively correlated with the percentage of winning perimeter. The combination of coral perimeter, mean surface fractal dimension, and coral species explained 19% of the variability of losing regions, while the surface area, perimeter, and perimeter-to-surface area ratio explained 27% of the variability of winning regions. Corals with surface fractal dimensions smaller than two and small perimeters displayed the highest percentage of losing perimeter, while corals with large surface areas and low perimeter-to-surface ratios displayed the largest percentage of winning perimeter. This study confirms the importance of fractal surface dimension, surface area, and perimeter of corals in coral-algal interactions. In combination with non-geometrical measurements such as microbial composition, this approach could facilitate environmental conservation and restoration efforts on coral reefs.

ecology↗