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Scientific Reports Mar 2024Coral reef ecosystems supported by environmentally sensitive reef-building corals face serious threats from human activities. Our understanding of these reef threats is...
Coral reef ecosystems supported by environmentally sensitive reef-building corals face serious threats from human activities. Our understanding of these reef threats is hampered by the lack of sufficiently sensitive coral environmental impact assessment systems. In this study, we established a platform for metabolomic analysis at the single-coral-polyp level using state-of-the-art mass spectrometry (probe electrospray ionization/tandem mass spectrometry; PESI/MS/MS) capable of fine-scale analysis. We analyzed the impact of the organic UV filter, benzophenone (BP), which has a negative impact on corals. We also analyzed ammonium and nitrate samples, which affect the environmental sensitivity of coral-zooxanthella (Symbiodiniaceae) holobionts, to provide new insights into coral biology with a focus on metabolites. The method established in this study breaks new ground by combining PESI/MS/MS with a technique for coral polyps that can control the presence or absence of zooxanthellae in corals, enabling functions of zooxanthellae to be assessed on a polyp-by-polyp basis for the first time. This system will clarify biological mechanisms of corals and will become an important model system for environmental impact assessment using marine organisms.
Topics: Humans; Animals; Anthozoa; Ecosystem; Tandem Mass Spectrometry; Coral Reefs; Dinoflagellida; Polyps
PubMed: 38443414
DOI: 10.1038/s41598-024-53294-8 -
Microbiome Feb 2024Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the...
BACKGROUND
Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system.
RESULTS
We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was concealed by body shrinkage of the starving animals, resulting in what could be referred to as "invisible" bleaching.
CONCLUSIONS
Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in rapidly warming oceans. Video Abstract.
Topics: Animals; Ecosystem; Symbiosis; Cnidaria; Heat-Shock Response; Coral Reefs; Dinoflagellida; Anthozoa
PubMed: 38424629
DOI: 10.1186/s40168-023-01738-0 -
Scientific Reports Feb 2024Protists make up the vast diversity of eukaryotic life and play a critical role in biogeochemical cycling and in food webs. Because of their small size, cryptic life...
Protists make up the vast diversity of eukaryotic life and play a critical role in biogeochemical cycling and in food webs. Because of their small size, cryptic life cycles, and large population sizes, our understanding of speciation in these organisms is very limited. We performed population genomic analyses on 153 strains isolated from eight populations of the recently radiated dinoflagellate genus Apocalathium, to explore the drivers and mechanisms of speciation processes. Species of this genus inhabit both freshwater and saline habitats, lakes and seas, and are found in cold temperate environments across the world. RAD sequencing analyses revealed that the populations were overall highly differentiated, but morphological similarity was not congruent with genetic similarity. While geographic isolation was to some extent coupled to genetic distance, this pattern was not consistent. Instead, we found evidence that the environment, specifically salinity, is a major factor in driving ecological speciation in Apocalathium. While saline populations were unique in loci coupled to genes involved in osmoregulation, freshwater populations appear to lack these. Our study highlights that adaptation to freshwater through loss of osmoregulatory genes may be an important speciation mechanism in free-living aquatic protists.
Topics: Salinity; Metagenomics; Ecosystem; Lakes; Dinoflagellida; Phylogeny; Genetic Speciation
PubMed: 38424140
DOI: 10.1038/s41598-024-55362-5 -
ISME Communications Jan 2024Microbial associations that result in phytoplankton mortality are important for carbon transport in the ocean. This includes parasitism, which in microbial food webs is...
Microbial associations that result in phytoplankton mortality are important for carbon transport in the ocean. This includes parasitism, which in microbial food webs is dominated by the marine alveolate group, Syndiniales. Parasites are expected to contribute to carbon recycling via host lysis; however, knowledge on host dynamics and correlation to carbon export remain unclear and limit the inclusion of parasitism in biogeochemical models. We analyzed a 4-year 18S rRNA gene metabarcoding dataset (2016-19), performing network analysis for 12 discrete depths (1-1000 m) to determine Syndiniales-host associations in the seasonally oligotrophic Sargasso Sea. Analogous water column and sediment trap data were included to define environmental drivers of Syndiniales and their correlation with particulate carbon flux (150 m). Syndiniales accounted for 48-74% of network edges, most often associated with Dinophyceae and Arthropoda (mainly copepods) at the surface and Rhizaria (Polycystinea, Acantharea, and RAD-B) in the aphotic zone. Syndiniales were the only eukaryote group to be significantly (and negatively) correlated with particulate carbon flux, indicating their contribution to flux attenuation via remineralization. Examination of Syndiniales amplicons revealed a range of depth patterns, including specific ecological niches and vertical connection among a subset (19%) of the community, the latter implying sinking of parasites (infected hosts or spores) on particles. Our findings elevate the critical role of Syndiniales in marine microbial systems and reveal their potential use as biomarkers for carbon export.
PubMed: 38419659
DOI: 10.1093/ismeco/ycae014 -
PloS One 2024Widespread coral bleaching has generally been linked to high water temperatures at larger geographic scales. However, the bleaching response can be highly variable among...
Widespread coral bleaching has generally been linked to high water temperatures at larger geographic scales. However, the bleaching response can be highly variable among individual of the same species, between different species, and across localities; what causes this variability remains unresolved. Here, we tracked bleached and non-bleached colonies of Acropora muricata to see if they recovered or died following a stress event inside the semi-enclosed lagoon of Bouraké (New Caledonia), where corals are long-term acclimatized to extreme conditions of temperature, pH and dissolved oxygen, and at a nearby control reef where conditions are more benign. We describe Symbiodiniaceae community changes based on next-generation sequencing of the ITS2 marker, metabolic responses, and energetic reserve measures (12 physiological traits evaluated) during the La Niña warm and rainy summer in 2021. Widespread coral bleaching (score 1 and 2 on the coral colour health chart) was observed only in Bouraké, likely due to the combination of the high temperatures (up to 32°C) and heavy rain. All colonies (i.e., Bouraké and reference site) associated predominantly with Symbiodinaceae from the genera Cladocopium. Unbleached colonies in Bouraké had a specific ITS2-type profile (proxies for Symbiodiniaceae genotypes), while the bleached colonies in Bouraké had the same ITS2-type profile of the reef control colonies during the stress event. After four months, the few bleached colonies that survived in Bouraké (B2) acquired the same ITS2 type profiles of the unbleached colonies in Bouraké. In terms of physiological performances, all bleached corals showed metabolic depression (e.g., Pgross and Rdark). In contrast, unbleached colonies in Bouraké maintained higher metabolic rates and energetic reserves compared to control corals. Our study suggests that Acropora muricata enhanced their resistance to bleaching thanks to specific Symbiodiniaceae associations, while energetic reserves may increase their resilience after stress.
Topics: Animals; Coral Bleaching; Anthozoa; Temperature; Dinoflagellida; Seasons; Coral Reefs; Symbiosis
PubMed: 38416713
DOI: 10.1371/journal.pone.0296902 -
Nature Communications Feb 2024Predicting the magnitude of herbicide impacts on marine primary productivity remains challenging because the extent of worldwide herbicide pollution in coastal waters...
Predicting the magnitude of herbicide impacts on marine primary productivity remains challenging because the extent of worldwide herbicide pollution in coastal waters and the concentration-response relationships of phytoplankton communities to multiple herbicides are unclear. By analyzing the spatiotemporal distribution of herbicides at 661 bay and gulf stations worldwide from 1990 to 2022, we determined median, third quartile and maximum concentrations of 12 triazine herbicides of 0.18 nmol L, 1.27 nmol L and 29.50 nmol L (95%Confidence Interval: CI 1.06, 1.47), respectively. Under current herbicide stress, phytoplankton primary productivity was inhibited by more than 5% at 25% of the sites and by more than 10% at 10% of the sites (95%CI 3.67, 4.34), due to the inhibition of highly abundant sensitive species, community structure/particle size succession (from Bacillariophyta to Dinophyceae and from nano-phytoplankton to micro-phytoplankton), and resulting growth rate reduction. Concurrently, due to food chain cascade effects, the dominant micro-zooplankton population shifted from larger copepod larvae to smaller unicellular ciliates, which might prolong the transmission process in marine food chain and reduce the primary productivity transmission efficiency. As herbicide application rates on farmlands worldwide are correlated with residues in their adjacent seas, a continued future increase in herbicide input may seriously affect the stability of coastal waters.
Topics: Animals; Herbicides; Zooplankton; Phytoplankton; Seawater; Diatoms; Ecosystem
PubMed: 38413588
DOI: 10.1038/s41467-024-46059-4 -
Ecotoxicology and Environmental Safety Mar 2024Filter-feeding bivalves could accumulate paralytic shellfish toxins (PSTs) produced by harmful dinoflagellates through diet. Despite that bivalves are resistant to these...
Filter-feeding bivalves could accumulate paralytic shellfish toxins (PSTs) produced by harmful dinoflagellates through diet. Despite that bivalves are resistant to these neurotoxins due to possessing PST-resistant sodium channel, exposure to PSTs-producing dinoflagellates impair bivalve survival. We hypothesized that ingesting PSTs-producing dinoflagellates may influence the gut microbiota, and then the health of bivalves. To test this idea, we compared the gut microbiota of the scallop Patinopecten yessoensis, after feeding with PST-producing or non-toxic dinoflagellates. Exposure to PSTs-producing dinoflagellates resulted in a decline of gut microbial diversity and a disturbance of community structure, accompanied by a significant increase in the abundance and richness of pathogenic bacteria, represented by Vibrio. Moreover, network analysis demonstrated extensive positive correlations between pathogenic bacteria abundances and PSTs concentrations in the digestive glands of the scallops. Furthermore, isolation of a dominant Vibrio strain and its genomic analysis revealed a variety of virulence factors, including the tolC outer membrane exporter, which were expressed in the gut microbiota. Finally, the infection experiment demonstrated scallop mortality caused by the isolated Vibrio strain; further, the pathogenicity of this Vibrio strain was attenuated by a mutation in the tolC gene. Together, these findings demonstrated that the PSTs may affect gut microbiota via direct and taxa-specific interactions with opportunistic pathogens, which proliferate after transition from seawater to the gut environment. The present study has revealed novel mechanisms towards deciphering the puzzles in environmental disturbances-caused death of an important aquaculture species.
Topics: Animals; Dinoflagellida; Dysbiosis; Gastrointestinal Microbiome; Toxins, Biological; Pectinidae; Bivalvia; Shellfish; Shellfish Poisoning
PubMed: 38412634
DOI: 10.1016/j.ecoenv.2024.116146 -
Toxins Feb 2024At the end of summer 2020, a moderate (~10 cells L) bloom of potential fish-killing spp. was detected in samples from a 24 h study focused on spp. in the outer reaches...
At the end of summer 2020, a moderate (~10 cells L) bloom of potential fish-killing spp. was detected in samples from a 24 h study focused on spp. in the outer reaches of the Pitipalena-Añihue Marine Protected Area. Previous events with devastating effects on caged salmon and the wild fauna of Chilean Patagonia had been restricted to offshore waters, eventually reaching the southern coasts of Chiloé Island through the channel connecting the Chiloé Inland Sea to the Pacific Ocean. This event occurred at the onset of the COVID-19 lockdown when monitoring activities were slackened. A few salmon mortalities were related to other fish-killing species (e.g., ). As in the major event in 1999, the austral summer of 2020 was characterised by negative anomalies in rainfall and river outflow and a severe drought in March. spp. appeared to have been advected in a warm (14-15 °C) surface layer of estuarine saline water (S > 21). A lack of daily vertical migration patterns and cells dispersed through the whole water column suggested a declining population. Satellite images confirmed the decline, but gave evidence of dynamic multifrontal patterns of temperature and chl distribution. A conceptual circulation model is proposed to explain the hypothetical retention of the bloom by a coastally generated eddy coupled with the semidiurnal tides at the mouth of Pitipalena Fjord. Thermal fronts generated by (topographically induced) upwelling around the Tic Toc Seamount are proposed as hot spots for the accumulation of swimming dinoflagellates in summer in the southern Chiloé Inland Sea. The results here provide helpful information on the environmental conditions and water column structure favouring occurrence. Thermohaline properties in the surface layer in summer can be used to develop a risk index (positive if the EFW layer is thin or absent).
Topics: Animals; Dinoflagellida; Estuaries; Chile; Ecosystem; Oceans and Seas; Fishes; Salmon; Harmful Algal Bloom
PubMed: 38393154
DOI: 10.3390/toxins16020077 -
Plant Physiology Apr 2024
Topics: Dinoflagellida; Photosystem II Protein Complex; Photosystem I Protein Complex
PubMed: 38386295
DOI: 10.1093/plphys/kiae093 -
The Science of the Total Environment Apr 2024As mass coral bleaching events become more frequent, it is increasingly important to elucidate the factors underlying coral susceptibility and survival. We measured...
As mass coral bleaching events become more frequent, it is increasingly important to elucidate the factors underlying coral susceptibility and survival. We measured photosynthesis, respiration, and O concentration at the coral tissue surface, Symbiodiniaceae genotypes, and energy metabolic enzyme activities in Agaricia agaricites and Orbicella franksi throughout experimentally-induced thermal bleaching (+3 °C). A. agaricites colonies started to bleach two days into the thermal treatment and were fully bleached between Days 19-31. In contrast, O. franksi colonies only started to bleach on Day 12 and five colonies fully bleached between Days 24-38 while the remining three colonies took up 55 days. Both species experienced decreased photosynthesis and respiration rates as bleaching progressed. As a result, daytime O concentration at the coral surface shifted from hyperoxia in unbleached corals to normoxia in partially bleached corals, and to near hypoxia in fully bleached corals. Additionally, nighttime tissue surface O concentration shifted from hypoxia to normoxia, likely resulting from decreased symbiotic algae density, respiration, and photosynthates that fuel coral aerobic respiration. Genetic profiling of internal transcribed spacer 2 (ITS2) revealed differences in Symbiodiniaceae clade proportions between control and bleached colonies. Activity levels of energy metabolic enzymes did not significantly vary between control and bleached A. agaricites, but malate dehydrogenase and strombine dehydrogenase activities were significantly higher in bleached O. franksi colonies compared to controls. These differences were driven by the three O. franksi colonies that took the longest to bleach and contained >98 % Durusdinium sp. D1. The shifts in O dynamics within the microhabitat of bleached corals may have important implications for the metabolism of the coral holobiont while the changes in Symbiodiniaceae ITS2 profile and the upregulation of energy metabolic enzymes identify a potential factor contributing to bleaching dynamics.
Topics: Animals; Anthozoa; Oxygen; Caribbean Region; Dinoflagellida; Energy Metabolism; Hypoxia; Coral Reefs
PubMed: 38360316
DOI: 10.1016/j.scitotenv.2024.170753