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1.
Proc Biol Sci ; 290(2009): 20231476, 2023 10 25.
Article in English | MEDLINE | ID: mdl-37848062

ABSTRACT

Reef-building crustose coralline algae (CCA) are known to facilitate the settlement and metamorphosis of scleractinian coral larvae. In recent decades, CCA coverage has fallen globally and degrading environmental conditions continue to reduce coral survivorship, spurring new restoration interventions to rebuild coral reef health. In this study, naturally produced chemical compounds (metabolites) were collected from two pantropical CCA genera to isolate and classify those that induce coral settlement. In experiments using four ecologically important Caribbean coral species, we demonstrate the applicability of extracted, CCA-derived metabolites to improve larval settlement success in coral breeding and restoration efforts. Tissue-associated CCA metabolites induced settlement of one coral species, Orbicella faveolata, while metabolites exuded by CCA (exometabolites) induced settlement of three species: Acropora palmata, Colpophyllia natans and Orbicella faveolata. In a follow-up experiment, CCA exometabolites fractionated and preserved using two different extraction resins induced the same level of larval settlement as the unfractionated positive control exometabolites. The fractionated CCA exometabolite pools were characterized using liquid chromatography tandem mass spectrometry, yielding 145 distinct molecular subnetworks that were statistically defined as CCA-derived and could be classified into 10 broad chemical classes. Identifying these compounds can reveal their natural prevalence in coral reef habitats and facilitate the development of new applications to enhance larval settlement and the survival of coral juveniles.


Subject(s)
Anthozoa , Animals , Larva , Cues , Coral Reefs , Ecosystem
2.
Mar Pollut Bull ; 194(Pt B): 115354, 2023 Sep.
Article in English | MEDLINE | ID: mdl-37573671

ABSTRACT

A coral community was examined on a semi-submersible platform that was moored at the leeward side of Curaçao, in the southern Caribbean, from August 2016 until August 2017. This community included several non-native or cryptogenic species. Among them were two scleractinian corals (Tubastraea coccinea and T. tagusensis) and two octocorals (Chromonephthea sp. and an unidentified Nephtheidae sp.). This is the first reported presence of T. tagusensis in the southern Caribbean, and the genus Chromonephthea in the Caribbean region. An ascidian, Perophora cf. regina, is also reported from the southern Caribbean for the first time, as well as a coral-associated vermetid gastropod, Petaloconchus sp., first recorded in the Caribbean in 2014. Lack of biofouling management could potentially harm indigenous marine fauna through the introduction of non-native species. Therefore monitoring communities associated with semi-submersible platforms is essential to track the presence and dispersal of non-native, potentially invasive species.


Subject(s)
Anthozoa , Biofouling , Animals , Caribbean Region , Introduced Species , Curacao , Coral Reefs
3.
Funct Ecol ; 36(8): 2104-2118, 2022 Aug.
Article in English | MEDLINE | ID: mdl-36247100

ABSTRACT

The increased release of dissolved organic matter (DOM) by algae has been associated with the fast but inefficient growth of opportunistic microbial pathogens and the ongoing degradation of coral reefs. Turf algae (consortia of microalgae and macroalgae commonly including cyanobacteria) dominate benthic communities on many reefs worldwide. Opposite to other reef algae that predominantly release DOM during the day, turf algae containing cyanobacteria may additionally release large amounts of DOM at night. However, this night-DOM release and its potential contribution to the microbialization of reefs remains to be investigated.We first tested the occurrence of hypoxic conditions at the turf algae-water interface, as a lack of oxygen will facilitate the production and release of fermentation intermediates as night-time DOM. Second, the dissolved organic carbon (DOC) release by turf algae was quantified during day time and nighttime, and the quality of day and night exudates as food for bacterioplankton was tested. Finally, DOC release rates of turf algae were combined with estimates of DOC release based on benthic community composition in 1973 and 2013 to explore how changes in benthic community composition affected the contribution of night-DOC to the reef-wide DOC production.A rapid shift from supersaturated to hypoxic conditions at the turf algae-water interface occurred immediately after the onset of darkness, resulting in night-DOC release rates similar to those during daytime. Bioassays revealed major differences in the quality between day and night exudates: Night-DOC was utilized by bacterioplankton two times faster than day-DOC, but yielded a four times lower growth efficiency. Changes in benthic community composition were estimated to have resulted in a doubling of DOC release since 1973, due to an increasing abundance of benthic cyanobacterial mats (BCMs), with night-DOC release by BCMs and turf algae accounting for >50% of the total release over a diurnal cycle.Night-DOC released by BCMs and turf algae is likely an important driver in the microbialization of reefs by stimulating microbial respiration at the expense of energy and nutrient transfer to higher trophic levels via the microbial loop, thereby threatening the productivity and biodiversity of these unique ecosystems. Read the free Plain Language Summary for this article on the Journal blog.


El incremento de la liberación de materia orgánica disuelta (MOD) por parte de las algas se ha asociado con el crecimiento rápido pero ineficaz de microorganismos patógenos oportunistas y la continua degradación de los arrecifes coralinos. Los céspedes algales (consorcios de micro y macroalgas que suelen incluir cianobacterias) dominan las comunidades bentónicas de muchos arrecifes de todo el mundo. A diferencia de otras algas de arrecife que liberan predominantemente MOD durante el día, los céspedes algales que contienen cianobacterias pueden liberar adicionalmente grandes cantidades de MOD durante la noche. Sin embargo, esta liberación nocturna de MOD y su potencial contribución a la microbialización de los arrecifes aún falta por ser investigada.En primer lugar, investigamos la existencia de condiciones de hipoxia en la interfase entre los céspedes algales y el agua, ya que la falta de oxígeno facilitaría la producción y liberación de productos intermedios de fermentación como MOD nocturna. En segundo lugar, cuantificamos la liberación de carbono orgánico disuelto (COD) por los céspedes algales durante el día y la noche, y se comprobó la calidad de los exudados diurnos y nocturnos como alimento para el bacterioplancton. Finalmente, las tasas de liberación de MOD de los céspedes algales se combinaron con las estimaciones de liberación de COD basadas en la composición de la comunidad bentónica en 1973 y 2013 para explorar cómo los cambios en la composición de la comunidad bentónica afectaron a la contribución de MOD nocturna y a su vez a la producción de COD en todo el arrecife.En ausencia de luz, se produjo inmediatamente un cambio rápido de condiciones sobresaturadas a condiciones hipóxicas en la interfaz entre los céspedes algales y el agua, lo que dio lugar a tasas de liberación de COD nocturnas similares a las diurnas. Los bioensayos revelaron importantes diferencias en la calidad de los exudados diurnos y nocturnos: el bacterioplancton utilizó el COD nocturno dos veces más rápido que el COD diurno, pero su eficiencia de crecimiento fue cuatro veces menor. Se estimó que los cambios en la composición de la comunidad bentónica han dado lugar a una duplicación de la liberación de MOD desde 1973 debido a la creciente abundancia de tapetes de cianobacterias bentónicas, y que la liberación nocturna de COD por parte de estos tapetes y los céspedes algales representa >50% de la liberación total durante un ciclo diurno.El COD nocturno que es liberado por los tapetes de cianobacterias bentónicas y los céspedes algales es probablemente un importante promotor de la microbialización de los arrecifes al estimular la respiración microbiana a expensas de la transferencia de energía y nutrientes a los niveles tróficos superiores a través del bucle microbiano y, por tanto, amenaza la productividad y la biodiversidad de estos ecosistemas únicos.

4.
PLoS One ; 17(9): e0274088, 2022.
Article in English | MEDLINE | ID: mdl-36095015

ABSTRACT

Larval settlement in wave-dominated, nearshore environments is the most critical life stage for a vast array of marine invertebrates, yet it is poorly understood and virtually impossible to observe in situ. Using a custom-built flume tank that mimics the oscillatory fluid flow over a shallow coral reef, we isolated the effect of millimeter-scale benthic topography and showed that it increases the settlement of slow-swimming coral larvae by an order of magnitude relative to flat substrates. Particle tracking velocimetry of flow fields revealed that millimeter-scale ridges introduced regions of flow recirculation that redirected larvae toward the substrate surface and decreased the local fluid speed, effectively increasing the window of time for larvae to settle. Regions of recirculation were quantified using the Q-criterion method of vortex identification and correlated with the settlement locations of larvae for the first time. In agreement with experiments, computational fluid dynamics modeling and agent-based larval simulations also showed significantly higher settlement onto ridged substrates. Additionally, in contrast to previous reports on the effect of micro-scale substrate topography, we found that these topographies did not produce key hydrodynamic features linked to increased settlement. These findings highlight how physics-based substrate design can create new opportunities to increase larval recruitment for ecosystem restoration.


Subject(s)
Anthozoa , Animals , Coral Reefs , Ecosystem , Larva , Swimming
5.
Curr Biol ; 32(17): 3855-3861.e3, 2022 09 12.
Article in English | MEDLINE | ID: mdl-35952668

ABSTRACT

Sponges, among the oldest extant multicellular organisms on Earth,1 play a key role in the cycling of nutrients in many aquatic ecosystems.2-5 They need to employ strategies to prevent clogging of their internal filter system by solid wastes,6-8 but self-cleaning mechanisms are largely unknown. It is commonly assumed that sponges remove solid waste with the outflowing water through distinct outflow openings (oscula).3,9 Here, we present time-lapse video footage and analyses of sponge waste revealing a completely different mechanism of particle removal in the Caribbean tube sponge Aplysina archeri. This sponge actively moves particle-trapping mucus against the direction of its internal water flow and ejects it into the surrounding water from its seawater inlet pores (ostia) through periodic surface contractions that have been described earlier as "sneezing."10,11 Visually, it appears as if the sponge is continuously streaming mucus-embedded particles and sneezes to shed this particulate waste, resulting in a notable flux of detritus that is actively consumed by sponge-associated fauna. The new data are used to estimate production of detritus for this abundant sponge on Caribbean coral reefs. Last, we discuss why waste removal from the sponge inhalant pores may be a common feature among sponges and compare the process in sponges to equivalent mechanisms of mucus transport in other animals, including humans.


Subject(s)
Ecosystem , Porifera , Animals , Bays , Coral Reefs , Humans , Mucus , Seawater , Sneezing , Water
6.
Sci Adv ; 8(35): eabn0707, 2022 09 02.
Article in English | MEDLINE | ID: mdl-36044584

ABSTRACT

Since 1892, it has been widely assumed that somatic mutations are evolutionarily irrelevant in animals because they cannot be inherited by offspring. However, some nonbilaterians segregate the soma and germline late in development or never, leaving the evolutionary fate of their somatic mutations unknown. By investigating uni- and biparental reproduction in the coral Acropora palmata (Cnidaria, Anthozoa), we found that uniparental, meiotic offspring harbored 50% of the 268 somatic mutations present in their parent. Thus, somatic mutations accumulated in adult coral animals, entered the germline, and were passed on to swimming larvae that grew into healthy juvenile corals. In this way, somatic mutations can increase allelic diversity and facilitate adaptation across habitats and generations in animals.


Subject(s)
Anthozoa , Animals , Anthozoa/genetics , Biological Evolution , Coral Reefs , Ecosystem , Germ Cells , Mutation
7.
Coral Reefs ; 40(4): 1137-1153, 2021.
Article in English | MEDLINE | ID: mdl-34720372

ABSTRACT

A paramount challenge in coral reef ecology is to estimate the abundance and composition of the communities residing in such complex ecosystems. Traditional 2D projected surface cover estimates neglect the 3D structure of reefs and reef organisms, overlook communities residing in cryptic reef habitats (e.g., overhangs, cavities), and thus may fail to represent biomass estimates needed to assess trophic ecology and reef function. Here, we surveyed the 3D surface cover, biovolume, and biomass (i.e., ash-free dry weight) of all major benthic taxa on 12 coral reef stations on the island of Curaçao (Southern Caribbean) using structure-from-motion photogrammetry, coral point counts, in situ measurements, and elemental analysis. We then compared our 3D benthic community estimates to corresponding estimates of traditional 2D projected surface cover to explore the differences in benthic community composition using different metrics. Overall, 2D cover was dominated (52 ± 2%, mean ± SE) by non-calcifying phototrophs (macroalgae, turf algae, benthic cyanobacterial mats), but their contribution to total reef biomass was minor (3.2 ± 0.6%). In contrast, coral cover (32 ± 2%) more closely resembled coral biomass (27 ± 6%). The relative contribution of erect organisms, such as gorgonians and massive sponges, to 2D cover was twofold and 11-fold lower, respectively, than their contribution to reef biomass. Cryptic surface area (3.3 ± 0.2 m2 m-2 planar reef) comprised half of the total reef substrate, rendering two thirds of coralline algae and almost all encrusting sponges (99.8%) undetected in traditional assessments. Yet, encrusting sponges dominated reef biomass (35 ± 18%). Based on our quantification of exposed and cryptic reef communities using different metrics, we suggest adjustments to current monitoring approaches and highlight ramifications for evaluating the ecological contributions of different taxa to overall reef function. To this end, our metric conversions can complement other benthic assessments to generate non-invasive estimates of the biovolume, biomass, and elemental composition (i.e., standing stocks of organic carbon and nitrogen) of Caribbean coral reef communities. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00338-021-02118-6.

8.
Proc Natl Acad Sci U S A ; 118(38)2021 09 21.
Article in English | MEDLINE | ID: mdl-34493583

ABSTRACT

Assisted gene flow (AGF) is a conservation intervention to accelerate species adaptation to climate change by importing genetic diversity into at-risk populations. Corals exemplify both the need for AGF and its technical challenges; corals have declined in abundance, suffered pervasive reproductive failures, and struggled to adapt to climate change, yet mature corals cannot be easily moved for breeding, and coral gametes lose viability within hours. Here, we report the successful demonstration of AGF in corals using cryopreserved sperm that was frozen for 2 to 10 y. We fertilized Acropora palmata eggs from the western Caribbean (Curaçao) with cryopreserved sperm from genetically distinct populations in the eastern and central Caribbean (Florida and Puerto Rico, respectively). We then confirmed interpopulation parentage in the Curaçao-Florida offspring using 19,696 single-nucleotide polymorphism markers. Thus, we provide evidence of reproductive compatibility of a Caribbean coral across a recognized barrier to gene flow. The 6-mo survival of AGF offspring was 42%, the highest ever achieved in this species, yielding the largest wildlife population ever raised from cryopreserved material. By breeding a critically endangered coral across its range without moving adults, we show that AGF using cryopreservation is a viable conservation tool to increase genetic diversity in threatened marine populations.


Subject(s)
Anthozoa/genetics , Gene Flow/genetics , Spermatozoa/physiology , Animals , Conservation of Natural Resources/methods , Coral Reefs , Cryopreservation/methods , Endangered Species , Fertilization/genetics , Florida , Genetics, Population/methods , Germ Cells/physiology , Male , Puerto Rico , Reproduction/genetics
9.
PeerJ ; 9: e11213, 2021.
Article in English | MEDLINE | ID: mdl-34249480

ABSTRACT

Reef-building corals are ecosystem engineers that compete with other benthic organisms for space and resources. Corals harvest energy through their surface by photosynthesis and heterotrophic feeding, and they divert part of this energy to defend their outer colony perimeter against competitors. Here, we hypothesized that corals with a larger space-filling surface and smaller perimeters increase energy gain while reducing the exposure to competitors. This predicted an association between these two geometric properties of corals and the competitive outcome against other benthic organisms. To test the prediction, fifty coral colonies from the Caribbean island of Curaçao were rendered using digital 3D and 2D reconstructions. The surface areas, perimeters, box-counting dimensions (as a proxy of surface and perimeter space-filling), and other geometric properties were extracted and analyzed with respect to the percentage of the perimeter losing or winning against competitors based on the coral tissue apparent growth or damage. The increase in surface space-filling dimension was the only significant single indicator of coral winning outcomes, but the combination of surface space-filling dimension with perimeter length increased the statistical prediction of coral competition outcomes. Corals with larger surface space-filling dimensions (Ds > 2) and smaller perimeters displayed more winning outcomes, confirming the initial hypothesis. We propose that the space-filling property of coral surfaces complemented with other proxies of coral competitiveness, such as life history traits, will provide a more accurate quantitative characterization of coral competition outcomes on coral reefs. This framework also applies to other organisms or ecological systems that rely on complex surfaces to obtain energy for competition.

10.
J Eukaryot Microbiol ; : e12852, 2021 Mar 25.
Article in English | MEDLINE | ID: mdl-33768669

ABSTRACT

Corals (Metazoa; Cnidaria; Anthozoa) have recently been shown to play host to a widespread and diverse group of intracellular symbionts of the phylum Apicomplexa. These symbionts, colloquially called "corallicolids", are mostly known through molecular analyses, and no formal taxonomy has been proposed. Another apicomplexan, Gemmocystis cylindrus (described from the coral Dendrogyra cylindrus), may be related to corallicolids, but lacks molecular data. Here, we isolate and describe motile trophozoite (feeding) corallicolids cells using microscopic (light, SEM, and TEM) and molecular phylogenetic analysis to provide the basis for a formal description. Phylogenetic analyses using nuclear and plastid rRNA operons, and three mitochondrial protein sequences derived from single cell transcriptomes, all confirm that these organisms fall into a discrete deep-branching clade within the Apicomplexa not closely related to any known species or major subgroup. As a result, we assign this clade to a new order, Corallicolida ord. nov., and family, Corallicolidae fam. nov. We describe a type species, Corallicola aquarius gen. nov. sp. nov. from its Rhodactis sp. host, and also describe a second species, Anthozoaphila gnarlus gen. nov. sp. nov., from the coral host Madracis mirabilis. Finally, we propose reassigning the incertae sedis taxon G. cylindrus from the order Agamococcidiorida to the Corallicolida, based on similarities in morphology and host localization to that of the corallicolids.

11.
Proc Natl Acad Sci U S A ; 117(24): 13588-13595, 2020 06 16.
Article in English | MEDLINE | ID: mdl-32482859

ABSTRACT

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral-turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.


Subject(s)
Anthozoa/metabolism , Chlorophyta/metabolism , Animals , Anthozoa/chemistry , Anthozoa/microbiology , Anthozoa/parasitology , Bacteria/classification , Bacteria/genetics , Bacteria/isolation & purification , Bacteria/metabolism , Chlorophyta/chemistry , Coral Reefs , Ecosystem , Metagenomics , Microbiota
12.
Science ; 366(6463): 326-334, 2019 10 18.
Article in English | MEDLINE | ID: mdl-31624206

ABSTRACT

Collective cell contractions that generate global tissue deformations are a signature feature of animal movement and morphogenesis. However, the origin of collective contractility in animals remains unclear. While surveying the Caribbean island of Curaçao for choanoflagellates, the closest living relatives of animals, we isolated a previously undescribed species (here named Choanoeca flexa sp. nov.) that forms multicellular cup-shaped colonies. The colonies rapidly invert their curvature in response to changing light levels, which they detect through a rhodopsin-cyclic guanosine monophosphate pathway. Inversion requires actomyosin-mediated apical contractility and allows alternation between feeding and swimming behavior. C. flexa thus rapidly converts sensory inputs directly into multicellular contractions. These findings may inform reconstructions of hypothesized animal ancestors that existed before the evolution of specialized sensory and contractile cells.


Subject(s)
Choanoflagellata/physiology , Light , Actomyosin/metabolism , Animals , Biological Evolution , Choanoflagellata/cytology , Cyclic GMP/metabolism , Microvilli/physiology , Movement , Phosphoric Diester Hydrolases/metabolism , Protozoan Proteins/metabolism , Sensory Rhodopsins/metabolism
13.
Environ Microbiol ; 21(10): 3855-3861, 2019 10.
Article in English | MEDLINE | ID: mdl-31278828

ABSTRACT

The application of metabarcoding to study animal-associated microeukaryotes has been restricted because the universal barcode used to study microeukaryotic ecology and distribution in the environment, the Small Subunit of the Ribosomal RNA gene (18S rRNA), is also present in the host. As a result, when host-associated microbial eukaryotes are analysed by metabarcoding, the reads tend to be dominated by host sequences. We have done an in silico validation against the SILVA 18S rRNA database of a non-metazoan primer set (primers that are biased against the metazoan 18S rRNA) that recovers only 2.6% of all the metazoan sequences, while recovering most of the other eukaryotes (80.4%). Among metazoans, the non-metazoan primers are predicted to amplify 74% of Porifera sequences, 4% of Ctenophora, and 15% of Cnidaria, while amplifying almost no sequences within Bilateria. In vivo, these non-metazoan primers reduce significantly the animal signal from coral and human samples, and when compared against universal primers provide at worst a 2-fold decrease in the number of metazoan reads and at best a 2800-fold decrease. This easy, inexpensive, and near-universal method for the study of animal-associated microeukaryotes diversity will contribute to a better understanding of the microbiome.


Subject(s)
Cnidaria/genetics , Ctenophora/genetics , DNA Barcoding, Taxonomic/methods , DNA Primers/genetics , Porifera/genetics , Animals , Databases, Nucleic Acid , Genes, rRNA/genetics , Humans , Phylogeny , RNA, Ribosomal, 18S/genetics
14.
PLoS One ; 14(6): e0217589, 2019.
Article in English | MEDLINE | ID: mdl-31194756

ABSTRACT

Effective assessments of the status of Caribbean fish communities require historical baselines to adequately understand how much fish communities have changed through time. To identify such changes and their causes, we compiled a historical overview using data collected at the beginning (1905-1908), middle (1958-1965) and end (1984-2016) of the 20th century, of the artisanal fishing practices and their effects on fish populations around Curaçao, a small island in the southern Caribbean. We documented historical trends in total catch, species composition, and catch sizes per fisher per month for different types of fisheries and related these to technological and environmental changes affecting the island's fisheries and fish communities. We found that since 1905, fishers targeted species increasingly farther from shore after species occurring closer to shore had become rare. This resulted in surprisingly similar catches in terms of weight, but not composition. Large predatory reef fishes living close to shore (e.g., large Epinephelid species) had virtually disappeared from catches around the mid-20th century, questioning the use of data from this period as baseline data for modern day fish assessments. Secondly, we compared fish landings to in-situ counts from 1969 to estimate the relative contributions of habitat destruction and overfishing to the changes in fish abundance around Curaçao. The decline in coral dominated reef communities corresponded to a concurrent decrease in the abundance and diversity of smaller reef fish species not targeted by fishers, suggesting habitat loss, in addition to fishing, caused the observed declines in reef fish abundance around Curaçao.


Subject(s)
Conservation of Natural Resources/trends , Fisheries/statistics & numerical data , Population Dynamics/trends , Animals , Caribbean Region/epidemiology , Conservation of Natural Resources/statistics & numerical data , Curacao , Ecosystem , Fishes , History, 20th Century , History, 21st Century
15.
Nature ; 568(7750): 103-107, 2019 04.
Article in English | MEDLINE | ID: mdl-30944491

ABSTRACT

Apicomplexa is a group of obligate intracellular parasites that includes the causative agents of human diseases such as malaria and toxoplasmosis. Apicomplexans evolved from free-living phototrophic ancestors, but how this transition to parasitism occurred remains unknown. One potential clue lies in coral reefs, of which environmental DNA surveys have uncovered several lineages of uncharacterized basally branching apicomplexans1,2. Reef-building corals have a well-studied symbiotic relationship with photosynthetic Symbiodiniaceae dinoflagellates (for example, Symbiodinium3), but the identification of other key microbial symbionts of corals has proven to be challenging4,5. Here we use community surveys, genomics and microscopy analyses to identify an apicomplexan lineage-which we informally name 'corallicolids'-that was found at a high prevalence (over 80% of samples, 70% of genera) across all major groups of corals. Corallicolids were the second most abundant coral-associated microeukaryotes after the Symbiodiniaceae, and are therefore core members of the coral microbiome. In situ fluorescence and electron microscopy confirmed that corallicolids live intracellularly within the tissues of the coral gastric cavity, and that they possess apicomplexan ultrastructural features. We sequenced the genome of the corallicolid plastid, which lacked all genes for photosystem proteins; this indicates that corallicolids probably contain a non-photosynthetic plastid (an apicoplast6). However, the corallicolid plastid differs from all other known apicoplasts because it retains the four ancestral genes that are involved in chlorophyll biosynthesis. Corallicolids thus share characteristics with both their parasitic and their free-living relatives, which suggests that they are evolutionary intermediates and implies the existence of a unique biochemistry during the transition from phototrophy to parasitism.


Subject(s)
Anthozoa/parasitology , Apicomplexa/genetics , Apicomplexa/metabolism , Chlorophyll/biosynthesis , Genes, Protozoan/genetics , Phylogeny , Animals , Apicomplexa/cytology , Coral Reefs , Dinoflagellida/cytology , Dinoflagellida/genetics , Dinoflagellida/metabolism , Genome, Protozoan/genetics , Photosynthesis , Plastids/genetics , Symbiosis
16.
Nat Commun ; 10(1): 1691, 2019 04 12.
Article in English | MEDLINE | ID: mdl-30979882

ABSTRACT

On coral reefs, microorganisms are essential for recycling nutrients to primary producers through the remineralization of benthic-derived organic matter. Diel investigations of reef processes are required to holistically understand the functional roles of microbial players in these ecosystems. Here we report a metagenomic analysis characterizing microbial communities in the water column overlying 16 remote forereef sites over a diel cycle. Our results show that microbial community composition is more dissimilar between day and night samples collected from the same site than between day or night samples collected across geographically distant reefs. Diel community differentiation is largely driven by the flux of Psychrobacter sp., which is two-orders of magnitude more abundant during the day. Nighttime communities are enriched with species of Roseobacter, Halomonas, and Alteromonas encoding a greater variety of pathways for carbohydrate catabolism, further illustrating temporal patterns of energetic provisioning between different marine microbes. Dynamic diel fluctuations of microbial populations could also support the efficient trophic transfer of energy posited in coral reef food webs.


Subject(s)
Coral Reefs , Microbiota , Photoperiod , Alteromonas , Ecosystem , Environmental Monitoring , Halomonas , Organic Chemicals/chemistry , Pacific Ocean , Psychrobacter , RNA, Ribosomal/chemistry , Roseobacter
17.
Mol Ecol ; 28(1): 141-155, 2019 01.
Article in English | MEDLINE | ID: mdl-30506836

ABSTRACT

Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef-building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.


Subject(s)
Anthozoa/physiology , Biological Evolution , Ecology , Symbiosis/genetics , Animals , Anthozoa/genetics , Caribbean Region , Coral Reefs , Dinoflagellida/genetics , Dinoflagellida/growth & development , Larva/genetics , Photosynthesis/genetics
18.
J Eukaryot Microbiol ; 66(4): 600-607, 2019 07.
Article in English | MEDLINE | ID: mdl-30480347

ABSTRACT

We describe the monoxenous trypanosomatids parasitizing true bugs and flies on the island of Curaçao. Out of 248 examined true bugs belonging to 17 species, 93 individuals were found to be infected (overall 38% prevalence) by at least one trypanosomatid species (referred to as typing units; TUs). Out of 80 flies, six were infected. All detected trypanosomatids were compared based on their 18S rRNA sequences with TUs parasitizing bugs and flies described from mainland South America, allowing us to assess their diversity and distribution. Besides Leptomonas pyrrhocoris and Leptomonas seymouri, two known species of the subfamily Leishmaniinae, our analysis revealed six new TUs falling into the groups 'jaculum', Blastocrithidia and Herpetomonas. Moreover, two new members of the genus Phytomonas and three new TUs belonging to the monophyletic group designated as 'new clade II' sensu Mol. Phylogenet. Evol, 69, 255 (2013) were isolated. The detected trypanosomatids were characterized by moderate diversity (13 TUs) species richness. Out of nine and four TUs from the heteropteran and dipteran hosts, respectively, 11 TUs have not been encountered before. Although a sampling bias may partially affect the comparison between trypanosomatid communities on Curaçao and the mainland, the high proportion of unique TUs from the former location suggests that the prominent role of islands in increasing the global diversity of macroscopic organisms may also extend to their protistan parasites.


Subject(s)
Diptera/parasitology , Heteroptera/parasitology , Trypanosomatina/isolation & purification , Animals , Curacao , Phylogeny , RNA, Protozoan/analysis , RNA, Ribosomal, 18S/analysis , Trypanosomatina/classification , Trypanosomatina/genetics
19.
PLoS One ; 13(1): e0189355, 2018.
Article in English | MEDLINE | ID: mdl-29309413

ABSTRACT

To inform a community-based ocean zoning initiative, we conducted an intensive ecological assessment of the marine ecosystems of Barbuda, West Indies. We conducted 116 fish and 108 benthic surveys around the island, and measured the abundance and size structure of lobsters and conch at 52 and 35 sites, respectively. We found that both coral cover and fish biomass were similar to or lower than levels observed across the greater Caribbean; live coral cover and abundance of fishery target species, such as large snappers and groupers, was generally low. However, Barbuda lacks many of the high-relief forereef areas where similar work has been conducted in other Caribbean locations. The distribution of lobsters was patchy, making it difficult to quantify density at the island scale. However, the maximum size of lobsters was generally larger than in other locations in the Caribbean and similar to the maximum size reported 40 years ago. While the lobster population has clearly been heavily exploited, our data suggest that it is not as overexploited as in much of the rest of the Caribbean. Surveys of Barbuda's Codrington Lagoon revealed many juvenile lobsters, but none of legal size (95 mm carapace length), suggesting that the lagoon functions primarily as nursery habitat. Conch abundance and size on Barbuda were similar to that of other Caribbean islands. Our data suggest that many of the regional threats observed on other Caribbean islands are present on Barbuda, but some resources-particularly lobster and conch-may be less overexploited than on other Caribbean islands. Local management has the potential to provide sustainability for at least some of the island's marine resources. We show that a rapid, thorough ecological assessment can reveal clear conservation opportunities and facilitate rapid conservation action by providing the foundation for a community-driven policymaking process at the island scale.


Subject(s)
Ecosystem , Fisheries , Marine Biology , Oceans and Seas , Animals , Antigua and Barbuda , Biodiversity , Conservation of Natural Resources
20.
Sci Rep ; 7(1): 18076, 2017 12 22.
Article in English | MEDLINE | ID: mdl-29273761

ABSTRACT

The use of sexually propagated corals is gaining popularity as an approach for reef restoration. However, manually attaching substrates with recently settled corals to the reef using binding materials is both time-consuming and expensive, limiting the use of this technique to small spatial scales. We present a novel approach whereby young corals are 'seeded' on the reef without the need for manual attachment to the benthos. We tested two tetrapod-shaped concrete substrates (7.9 and 9.8 cm in diameter) on which coral larvae were settled. The tetrapods were efficiently deployed by wedging them in reef crevices, in 1.5 to 7% of the time required for traditional outplanting techniques. Seeding tetrapods was most effective in reefs with moderately to highly complex topographies, where they rapidly became lodged in crevices or cemented to the benthos by encrusting organisms. After one year, average recruit survival was 9.6% and 67% of tetrapods still harboured at least one coral colony, and overall, this approach resulted in a 5 to 18 fold reduction in outplanting costs compared to common outplanting methods. This seeding approach represents a substantial reduction in costs and time required to introduce sexually propagated corals to reefs, and could possibly enable larger scale reef restoration.


Subject(s)
Anthozoa , Conservation of Natural Resources/economics , Coral Reefs , Ecosystem , Animals , Population Dynamics , Reproduction
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