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Bonacolta, A. M.

Publications and source records attributed to Bonacolta, A. M..

10 recordsLinked to original sources

Experimental Thermal Stress Increases Corallicolid Relative Abundance in the Stony Coral Pocillopora damicornis

Rising ocean temperatures disrupt previously stable coral-microbe interactions, leading to widespread coral mortality and threatening reef ecosystems worldwide. Growing evidence demonstrates the coral microbiome, including protists, plays a critical role in the host response to thermal stress. Specifically, corallicolids (Phylum: Apicomplexa) are positively correlated with thermal stress mortality in soft corals. This study investigates changes in the eukaryotic microbiome of the stony coral, Pocillopora damicornis, across an experimental thermal stress event. Using anti-metazoan 18S rRNA gene metabarcoding, protist communities were assessed at four time-points during experimental thermal stress. Outside of the Symbiodiniaceae, a prominent shift in microbiome composition during thermal stress was observed, most notably a significant increase and dominance in Corallicolida abundance in heat-stressed corals, while other protists declined substantially. Increased corallicolid abundance concurrent with bleaching suggests an overlooked compounding stressor beyond the loss of algal symbionts during heat stress. These results contrast with previous research on Pocillopora microbiomes showing prokaryotic community stability throughout stress, and support the hypothesis that thermal stress may alter the coral-corallicolid relationship, potentially shifting corallicolids from a commensal to a parasitic role, and synergistically contributing to coral mortality during and after heat stress. This work provides critical insight into the role of protists in marine holobionts, supports their inclusion in future microbiome studies, and informs strategies to improve coral resilience under climate change.

ecology↗

HIDDEN APICOMPLEXAN PARASITE DIVERSITY LINKS CORAL AND PLANKTON MICROBIOMES ACROSS REEF SEASCAPES

Parasitism is one of the most widespread trophic strategies in nature, though its diversity and ecological distribution in marine ecosystems remain poorly characterized. Apicomplexa are a major clade of obligate parasites best known for medically important taxa, yet their diversity and distribution in the ocean is still largely unresolved. Here, we used metabarcoding data from the Tara expeditions to investigate the diversity, distribution, and environmental drivers of Apicomplexa across coral reef ecosystems and adjacent oceanic habitats. By integrating samples spanning planktonic communities, coral tissues, and marine sediments across multiple oceanic regions, we substantially expand the known phylogenetic breadth of marine apicomplexans. Although apicomplexans were generally low in relative abundance, they were widely distributed across marine environments. Community composition differed markedly among habitats. Corallicolid lineages were consistently associated with coral hosts, whereas planktonic samples harbored a greater diversity of apicomplexans, dominated by crustacean-associated gregarines. Sediments contained particularly high apicomplexan richness, including several poorly characterized groups. Capitalizing on the pan-Pacific transect of the expedition, we resolved biogeographic patterns in apicomplexan diversity across ocean basins: tropical regions showed the highest overall diversity, while polar environments contained distinct apicomplexan assemblages not detected in other ocean biomes. Together, these results highlight the extensive and previously underappreciated diversity of marine Apicomplexa and demonstrate that integrating multiple marine biomes is essential for resolving the phylogenetic and ecological breadth of parasitism in the ocean.

genomics↗

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↗

Symbiotic bacteria support calcium carbonate precipitation in the Gulf toadfish (Opsanus beta)

Marine fish play a significant yet understudied role in the oceanic carbon cycle through the production of magnesium rich calcium carbonate (CaCO3) precipitates known as ichthyocarbonates. These deposits form in the gut of marine teleost fish in response to salinity, serving as part of their osmoregulation strategy. Through this, marine fish may contribute as much as 9.04 Pg of CaCO3 per year in global new carbonate production, being equivalent to or potentially higher than the production by coccolithophores and pelagic foraminifera. Despite their ecological relevance, the biological mechanisms driving ichthyocarbonate precipitation remain to be fully resolved. Intriguingly, bacteria are consistently found in intimate association with ichthyocarbonate precipitates. Given the widespread capacity of prokaryotes to mediate CaCO precipitation, this association points to a previously unexplored microbial contribution to the process. To investigate the potential role of bacteria in ichthyocarbonate production, we subjected Gulf toadfish (Opsanus beta) to a salinity challenge common to their native range and known to elicit elevated CaCO3 precipitation. To assess the respective contributions of the host and its microbiota to ichthyocarbonate formation in the gut, we characterized the microbiome across the toadfish gut and performed meta-transcriptomic analysis. Across the toadfish gut, we identify a high abundance of vibrios associated with ichthyocarbonates with the metabolic potential for CaCO3 precipitation. Specifically, we observe the expression of the transcriptional activator of urease (ureR) by Photobacterium damselae subsp. damselae, which can induce the precipitation of CaCO3 via the production of bicarbonate. We demonstrate that CaCO precipitation in marine fish may not solely be a host-driven process, but potentially the result of a functional symbiosis with gut-associated Vibrio bacteria. We hypothesize that just as photosymbionts enable corals to build reefs, fish hosts along with their microbial partners may synergistically contribute to oceanic carbonate production. This discovery, if confirmed, expands the role of symbiosis in marine biomineralization and underscores its broader influence on global biogeochemical cycles.

microbiology↗

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↗

Modern microbialites harbor an undescribed diversity of chromerid algae

Chromerid algae and the heterotrophic colpodellids together make up the chrompodellids, which are the closest known relatives to apicomplexan parasites [1]. As apicomplexans are prolific parasites of animals, including humans, their adaptation to parasitism from algal ancestors has garnered significant interest, and chromerids were instrumental in elucidating that evolution [2-5]. But the chromerids were also the first new algal group discovered in 100 years [2], and because so much attention has focused on comparisons with apicomplexans, the ecology of chromerid algae has remained surprisingly mysterious. They have predominately been considered to live only in association with corals, initially as intracellular coral symbionts. To test for a wider distribution of chromerids in nature, we have used plastid metagenomic binning combined with re-analysis of 18S rRNA metabarcoding data, which both support an expanded biogeographic range and ecological niche of chromerid algae by showing they are consistent associates of modern microbialites across the globe. Specifically, a broad and undescribed diversity of chromerid lineages is found in marine and also freshwater microbialites. This includes the recovery of a near-complete V. brassicaformis plastid genome and a second incomplete plastid genome from a new chromerid lineage from Highborne Cay thrombolites. This is the first concrete evidence that this under-sampled algal lineage lives outside some association with coral, including freshwater habitats, and sheds new light on the diversity and ecological range of the most recently discovered algal lineage.

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↗

A new and widespread group of fish apicomplexan parasites

Apicomplexans are obligate intracellular parasites which have evolved from a free-living, phototrophic ancestor. Well-known representatives include Plasmodium, the causative agent of malaria, and the gregarines which infect a vast number of marine invertebrates. Apicomplexans have been reported from marine environmental samples in high numbers1, with several clades of Apicomplexan-Related Lineages (ARLs) having been described from environmental sequencing data (SSU rRNA metabarcoding)2. The most notable of these being the corallicolids (previously known as ARL-V) which possess chlorophyll-biosynthesis genes in their relic chloroplast (apicoplast) and are geographically wide-spread and abundant symbionts of anthozoans3. Ophioblennius macclurei, the redlip blenny, along with other tropical reef fishes, is known to be infected by Haemogregarina-like and Haemohormidium-like parasites4; however previous phylogenetic work using the 18S rRNA genes shows these parasites to be distinct from where they are classified morphologically5,6 and instead related to the Coccidia. Hybrid genomic sequencing incorporating Oxford Nanopore Technologies long reads and Illumina short reads of apicomplexan-infected O. macclurei blood was carried out to retrieve more genetic information on these parasites. Using this approach, we were able to recover the entire rRNA operon of this apicomplexan parasite along with the complete mitochondrion and apicoplast genomes. Phylogenetic analyses using this new genomic information consistently place these fish-infecting apicomplexans, hereby informally named ichthyocolids, sister to the corallicolids within Coccidia. The apicoplast genome did not contain chlorophyll biosynthesis genes, providing evidence for another independent loss of this pathway within Apicomplexa. Based on the 16S rRNA gene found in the apicoplast, this group corresponds to the previously described ARL-VI. Screening of fish microbiome studies using the plastid 16S rRNA gene shows these parasites to be geographically and taxonomically widespread in fish species across the globe with potentially major implications for commercial fisheries and oceanic food webs.

microbiology↗

Apicomplexans predict thermal stress mortality in the Mediterranean coral Paramuricea clavata

The octocoral Paramuricea clavata is an ecosystem architect of the Mediterranean temperate reefs that is currently threatened by episodic mass mortality events related to global warming. Local average thermal regimes nor recent thermal history have been shown to play a significant role in population thermotolerance in this species. The microbiome, however, may play an active role in the thermal stress susceptibility of corals, potentially holding the answer as to why corals show differential sensitivity to heat-stress. To investigate this, the prokaryotic and eukaryotic microbiome of P. clavata collected from around the Mediterranean was characterized before experimental heat-stress to determine if its microbial composition influences the thermal response of the holobiont. We found that the prokaryotic community was not informative in predicting the thermal susceptibility of P. clavata. On the other hand, members of P. clavatas microeukaryotic community were significantly correlated with thermal stress sensitivity. Syndiniales from the Dino-Group I Clade 1 were significantly enriched in thermally resistant corals, while the apicomplexan corallicolids were significantly enriched in thermally susceptible corals. Corallicolids are associated with 70% of coral genera around the world, yet the ecological role of this general anthozoan symbiont has yet to be determined. We hypothesize that P. clavata mortality following heat-stress may be caused by a shift from apparent commensalism to parasitism in the corallicolid-coral host relationship driven by the added stress. Our results show the potential importance of corallicolids and the rest of the microeukaryotic community of corals to understanding thermal stress response in corals and provides a useful tool to guide conservation efforts and future research into coral-associated microeukaryotes.

microbiology↗

Microniche sampling of the microbiome in the Starlet Sea Anemone, Nematostella vectensis, reveals a compartment-specific dominance of Spirochetes

Sampling of different body regions can reveal highly specialized bacterial associations within the holobiont and facilitate identification of core microbial symbionts that would otherwise be overlooked by bulk sampling methods. Here we characterized compartment-specific associations present within the model cnidarian Nematostella vectensis by dividing its morphology into three distinct body regions. This sampling design allowed us to uncover a capitulum-specific dominance of spirochetes within N. vectensis. Bacteria from the family Spirochaetaceae made up 66% of the community in the capitulum, while only representing 1.2% and 0.1% of the communities in the mesenteries and physa, respectively. A phylogenetic analysis of the predominant spirochete sequence recovered from N. vectensis showed a close relation to spirochetes previously recovered from wild N. vectensis. These sequences clustered closer to the recently described genus Oceanispirochaeta, rather than Spirochaeta perfilievii, supporting them as members of this clade. This suggests a consistent and potentially important association between N. vectensis and spirochetes from the order Spirochaetales.

microbiology↗