Freshw. 105, 1545215457. Nakamura et al., Reference Nakamura, Tachikawa, Kitamura, Ohno, Suganuma and Uemura2008; von Reumont et al., Reference von Reumont, Campbell, Richter, Hering, Sykes, Hetmank, Jenner and Bleidorn2014), but some studies have shed doubt on this interpretation. Additionally, juveniles and adults may be transported on ship hulls, natural and anthropogenic marine debris, or live rock in the aquarium trade. To account for all of the possible transcripts that could have been expressed under varying levels of DO, we assembled and annotated a super transcriptome with the sequences (N=11) from the Florida collections, Brazilian collections, and the chronic hypoxia studies with default Trinity63 parameters and following the Trinotate pipeline (version 3.0.2)64, respectively. the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Breitburg, D. et al. PubMed Central Responses of seven species of native freshwater fish and a shrimp to low levels of dissolved oxygen. 22, 22802291 (2013). Internet Explorer). However, few studies have examined the differential expression of the two HIF subunits in response to different levels of hypoxia. 73, 365373 (2000). Stud. Barbieri, Michele Log fold change (FC) values|1| were identified as differentially expressed features (DEFs) (genes [DEGs] and transcripts [DETs]) with a false discovery rate (FDR) p value<0.05. Ann. Localized reactions in the affected area include an acute, intense stinging pain, itchiness, numbness and swelling (Smith, Reference Smith2002). C: Toxicol. 1b) which is abundant and widespread throughout the tropical and subtropical Atlantic. obs.). Biol. Holford, Mand Ecol. Proc. } Low dissolved oxygen (DO), or hypoxia, events are increasing in area, frequency and duration as the oceans continue to warm and anthropogenic nutrient runoff to coastal ecosystems continues1,2,3. Li, T. & Brouwer, M. Hypoxia-inducible factor, gsHIF, of the grass shrimp Palaemonetes pugio: Molecular characterization and response to hypoxia. Giannetto, A. et al. Hermodice carunculata is also frequently reported from marine and anchialine caves in the Caribbean (Frontana-Uribe & Sols-Weiss, Reference Frontana-Uribe and Sols-Weiss2011), the Mediterranean (Gerovasileiou et al., Reference Gerovasileiou, Chintiroglou, Vafidis, Koutsoubas, Sini, Dailianis, Issaris, Akritopoulou, Dimarchopoulou and Voutsiadou2015; Knittweis et al., Reference Knittweis, Chevaldonn, Ereskovsky, Schembri and Borg2015) and the Azores (Micael et al., Reference Micael, Azevedo and Costa2006), ranging from the cave entrance to the dark zone. ADS According to their study, the calcium carbonate is deposited after the large central microvilli of the chaetoblast retract and their canals fuse together. Stke 407, 13 (2007). Cluster 8 genes had inverse expression trends between hypoxic and normoxic timepoints and contained genes associated with epidermal growth factor-, actin-, and Notch-binding. Acad. This short-term response to intermittent hypoxic stress may increase blood flow and oxygen transport to maintain necessary metabolic functions during times of lowered oxygen conditions. Future studies should also consider the effects of ocean acidification on this calcifying annelid. 17-estradiol represses myogenic differentiation by increasing ubiquitin-specific peptidase 19 through estrogen receptor . J. Biol. Mar. In the meantime, to ensure continued support, we are displaying the site without styles Simonini, Roberto The hydrothermal vent-inhabiting Paralvinella sp. The head is shown on the first segment and includes the eyes and other sensory organs. Semenza, G. L. Hypoxia-inducible factor 1 (HIF-1) pathway. Change 4, 969976 (2014). Open 8, bio37630 (2019). Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Mild comparison (Fig. Environ. 3, 133143 (2010). Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia. Mar. McIntosh (Reference McIntosh1885) mentions a large specimen of H. carunculata swimming near the water surface. 2020. For example, we saw a down-regulation of ATP synthase and cytochrome c oxidase, key members of the electron transport (Table 4). Nat. Nat. Values within the heatmap are counts per million (CPM) that that have been selected as differentially expressed based on log fold-change (FC) values with a1 cutoff. Thank you for visiting nature.com. Cassiopea contains numerous toxins, indicating that H. carunculata may sequester their toxins from various benthic cnidarians (Radwan et al., Reference Radwan, Romn, Baksi and Burnett2005; Stoner & Layman, Reference Stoner and Layman2015). Boutet, I., Jollivet, D., Shillito, B., Moraga, D. & Tanguy, A. Molecular identification of differentially regulated genes in the hydrothermal-vent species Bathymodiolus thermophilus and Paralvinella pandorae in response to temperature. Has data issue: false Although the bearded fireworm is motile, its slow speed and limited movement range are likely to impede its escape from a large-area hypoxic event. Deep Sea Res. You are using a browser version with limited support for CSS. Fibropellin-1, related to Notch protein-binding, was recently shown to have drastically increased in expression post chronic hypoxia in the clam Ruditapes philippinarum81. and HSP90 is a heat shock protein that stabilizes HIF1- until (under normoxic conditions) O2 facilitates the hydroxylation of HIF-1 at two proline residues with proline hydroxylase (PHD) and one asparagine residue with factor inhibiting HIF-1 hydroxylation (FIH) (created and modified from Liu and Semenza 2007). Part II 56, 488502 (2009). PeerJ 4, e1956 (2016). Sci. Diaz, R. J. This is a photography of a protected area of Portugal indexed in the World Database on Protected Areas with the ID: Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States. In the Azores, H. carunculata has been reported from the shallow-water hydrothermal vents at D. Joo de Castro Seamount (Cardigos et al., Reference Cardigos, Colao, Dando, vila, Sarradin, Tempera, Conceio, Pascoal and Serro Santos2005). Part II 51, 24752490 (2004). Rosa, Marcos Rogerio (B) SEM of a chaetal tip, showing the serration. We review its environmental tolerances, defence mechanisms and feeding habits to evaluate its potential to survive in changing ocean conditions, to increasingly emerge as a nuisance species and to invade new geographic areas. However, because of its cryptic nature, little is known about its ecology. However, the time course cluster analysis revealed some expression trends depending on time points (Table 5). Witman, J. D. Effects of predation by the fireworm Hermodice carunculata on milleporid hydrocorals. Hypoxia-inducible factor and Hif-prolyl hydroxylase characterization and gene expression in short-time air-exposed Mytilus galloprovincialis. Potamodromous fish movements under multiple stressors: Connectivity reduction and oxygen depletion. Francini Filho, Ronaldo Bastos & Ritter, C. Direct and indirect effects of hypoxia on benthos in Corpus Christi Bay, Texas, USA. Hermodice carunculata (Pallas, 1766) is an amphinomid annelid (Fig. Genes and transcripts were analyzed for differential expression with the Generalized Linear Model statistical test which is robust to low replicate numbers. The objectives of this study were to characterize gene expression responses in H. carunculata (1) under chronic Mild and Moderate hypoxia (as defined above) and (2) under severe intermittent hypoxia. Fireworms exhibit both asexual and sexual reproduction. Structural and functional analysis of coral Hypoxia Inducible Factor. Zanetti, Federica In the coral conservation community, H. carunculata has a bad reputation, not only because it feeds on live corals, especially new recruits (Miller & Williams, Reference Miller and Williams2007; Miller et al., Reference Miller, Lohr, Cameron, Williams and Peters2014), but also because it can act as a vector and reservoir for coral pathogens. This brings scientists closer to being able to isolate the protein that is causing the light. Oyster summer morality risks associated with environmental stress. Prevedelli, Daniela These annelids do not differ from the other annelids impact that they have on the environment. In particular, it may interfere with coral reef restoration efforts due to its feeding behaviour (Bruckner & Bruckner, Reference Bruckner and Bruckner2001; Wolf & Nugues, Reference Wolf and Nugues2013; Miller et al., Reference Miller, Lohr, Cameron, Williams and Peters2014). Marques, I. J. et al. C. J. Grimes. Cell 30, 393402 (2008). Biochem. DO levels were controlled by the influx of nitrogen gas (Radnor nitrogen from Airgas Welding Supplies, TX, USA) and controlled with Neptune Systems Apex Jr. Since this protein is involved with new growth of cancerous tumors and other cell types (such as blood vessels78), the higher expression after chronic Moderate and intermittent hypoxia supports the idea that lowered oxygen levels triggers growth in specific cell types. J. Biol. Kanaoka, Y. Differentially expressed genes (a, b) and transcripts (c, d) from chronic hypoxia treatments. 2023. Organisms were collected under the Florida Fish and Wildlife Conservation Commission (FWC) Special Activity License (SAL-17-1946-SR). & Cyronak, T. Benthic coral reef calcium carbonate dissolution in an acidifying ocean. Although the Fireworm prefers the tissue of Cnidarians, they will readily accept and thrive on alternative foods in captivity. CAS J. Exp. Natl. PubMed Central This sensation lasts up to a few hours, but a painful tingling can continue to be felt around the area of contact. 1a). Article Cite this article. PLoS ONE 7, e44621 (2012). Then, kallisto produces transcript counts for each sample which were then converted to gene counts with tximport (version 1.10.1)67 and analyzed for differential gene expression with edgeR (version 3.24.3)68. Biotechnol. J. Comp. (Gleibs et al., Reference Gleibs, Mebs and Werding1995). Likewise, hypoxia-triggered up-regulation of Notch-binding proteins has been shown to increase tracheal formation in insects79. This study showed that six hours of hypoxia exposure is sufficient to initiate molecular pathways for epithelial morphogenesis and blood vessel remodeling, providing further support that morphological changes of respiratory structures are not reliable taxonomic characters in amphinomids (or even possibly in annelids in general). Hermodice carunculata is primarily reported from warmer waters, but one questionable record exists from as far north as the Dogger Bank in the North Sea (Fauvel, Reference Fauvel1923). Ecol. The consistent higher expression of hematopoietic prostaglandin D synthase (Cluster 3) after the hypoxic timepoints suggests physiological responses related to vasodilation and inhibition of clotting so that blood transporting oxygen can flow more freely73. Grimes, C. J., Capps, C., Petersen, L. H. & Schulze, A. Grimes, C.J., Petersen, L.H. Fireworms are predators that feed on soft and hard corals, anemones, and small crustaceans. Int. Our findings suggest that H. carunculata is likely to tolerate, and be resilient to, predicted future hypoxia conditions. Web. They engulf the last few centimeters of the tip of a branching coral inside its pharynx and remove the coral tissue right from the skeleton. Our chronic hypoxia experiments showed that Notch-binding was up-regulated in the Moderate treatment compared to the Mild but was down-regulated in the Mild treatment compared to Normal indicating a differential response that is dependent on DO levels. and One factor that could potentially affect it negatively is ocean acidification, as a diminished pH could interfere with the formation or structural integrity of the calcified chaetae, a key feature for its survival. Soanez-Organis, J. G. et al. See 33 for more detailed descriptions and a diagram of the experimental setup. Correspondence to Biol. Seixas, Victor Corra https://www.biobam.com/omicsbox (2019). http://www.botany.hawaii.edu/basch/uhnpscesu/htms/kahoinvr/images/amphin/k044x7.jpg, http://www.uwphotographyguide.com/images/birwin-uv-light-5.jpg. Google Scholar. Comp. Here we report ecological data and fireworm abundances . The worms used in this study had likely never been exposed to hypoxia before, so it is not surprising that we see different expression trends at timepoint 1 and 3. Ahrens, J. Amphinomid chaetae are unique in that they contain calcium carbonate in addition to chitin (Gustafson, Reference Gustafson1930). Altun, M. et al. Chem. PLoS ONE 12, e0186262 (2017). 2021. J. Exp. Krelj, Maja Typically, under hypoxic conditions, HIF-1 is protected from proteasomal degradation by Usp19, but the expression trends (higher expression after first hypoxic exposure) here suggest there may be another protective mechanism for HIF-1 in the fireworm and potentially other animals. The texture of the chaetae may be erodible and may depend on the status of regeneration after they have been shed. Google Scholar. Article We also analyzed the transcripts abundances in edgeR (according to the same protocol) for comparison of genes with transcripts due to the issues with detecting true isoforms from chimeras and gene fragments when utilizing a reference transcriptome instead of a reference genome. Fig. Contigs with BLAST hits corresponding to Viruses, Bacteria, or Archaea were removed from this analysis. The Animal Diversity Web (online). & Schulze, A. Recently Ladd & Shantz (Reference Ladd and Shantz2016) published the first observations of two fish species, the white grunt (Haemulon plumierii) and the sand tilefish (Malacanthus plumieri) feeding on H. carunculata in Florida. Costa-Paiva, E. M., Schrago, C. G., Coates, C. J. https://doi.org/10.1038/s41598-021-90540-9, DOI: https://doi.org/10.1038/s41598-021-90540-9. When organisms undergo intermittent hypoxia, they must be able to handle times of low oxygen and high oxygen when the reactive oxygen species increase which threaten cell health and structure which can result from the formation of reactive oxygen species under hypoxia or upon reoxygenation61,62. Bearded Fireworm Description. Murphy, J. W. & Richmond, R. H. Changes to coral health and metabolic activity under oxygen deprivation. and 2021. 5) further indicates a modulated response to chronic hypoxia exposure dependent upon DO level. Article However,because of its cryptic nature, little is known. Mol. CAS Apart from pelagic larvae, H. carunculata may also disperse by rafting. Water 11, 642 (2019). Conesa, A., Nueda, M. J., Ferrer, A. Filamin A (FLNA) is required for cellcell contact in vascular development and cardiac morphogenesis. Ecol. Unfortunately, little is known about the larval development of the species. Preliminary investigation of H. carunculatas transcriptome revealed homologs necessary for hypoxic response (such as HIF-1, ARNT, VHL, TRP1A, PHD, etc.). Grimes, Candace J. Biol. They arent a threat to humans unless a careless diver swims to close and brushes against their bristles. Differential gene expression will help detect additional physiological processes that affect overall organismal functioning and find explanations for the environmental hardiness of H. carunculata. The body consists of 60 to 150 identical segments separated from each other by a thin white line and protected by cuticles. Taylor, C. T. & McElwain, J. C. Ancient atmospheres and the evolution of oxygen sensing via the hypoxia-inducible factor in metazoans. In the short term, we predict that H. carunculata will be able to withstand many future ecological challenges and possibly contribute to coral reef decline. Heatmap of the top 44 differentially expressed genes for each sample after the intermittent hypoxia trial with the treatments and timepoints. In this context, Hermodice carunculata (Pallas, 1766) is a selective scavenger/carnivore polychaete species (known as a fireworm) that, in recent years, has exhibited a northern expansion along . Nallapalli, R. K. et al. 75, 251262 (2011). Ecol. Article Apart from the head and terminal segments, all the segments are identical, each with a pair of flattened, fleshy lobe like paddles called parapodia, which are used for swimming, burrowing and creating a feeding current. These beautiful flattened segmented worms, reaching 35.6 cm (typically 7-10 cm) in length, with groups of white bristles along each side. 17, 768781 (2015). PubMed More notably, however, in rare cases, systemic reactions such as nausea, cardiac and respiratory problems can occur (Ottuso, Reference Ottuso2013). | Questions or Comments. Under hypoxic conditions, HIF-1 is not hydroxylated and forms a heterodimer with the ARNT and relocates from the cytoplasm to the nucleus as a functional transcription factor to trigger downstream responses31. These include: squid, clam, shrimp, krill, shrimp, and mussels. Data analyses and interpretation: C.J.G. PubMed polychaete Table of Contents Home Science Bugs, Mollusks & Other Invertebrates Worms & Annelids polychaete Righi, Sara B. et al. Family description (Amphinomidae) Bristle worms are found in most aquariums. Freshwat. The term hypoxic is context-specific and can either refer to the level at which an organism responds to low oxygen conditions or to the environment in which the organism resides. Vreeland, H. & Lasker, H. Selective feeding of the polychaete Hermodice carunculata Pallas on Caribbean gorgonians. The vinegar may dissolve the calcium carbonate in the chaetae. Encarnao, Joo Hughes, D. J. et al. Although no toxins specifically associated with the chaetae have been identified to date, there are indications that venoms are utilized. Cluster 2 genes, consisting primarily of heme-binding, metabolism, and translation features, increased after both hypoxic and normoxic timepoints; however, the increase at hypoxia timepoints was more drastic. Ubiquitin-specific protease 19 (USP19) regulates hypoxia-inducible factor 1 (HIF-1) during hypoxia. carunculata willbe ableto withstandmany futureecological chal-lenges and possibly contribute to coral reef decline. The bearded fireworm, Hermodice carunculata, is a common species in the marine annelid taxon Amphinomidae. Di Camillo, Cristina 572, 520525 (2016). Righi, Sara They are the largest and most primitive group of annelids of . Grimes, C. J., Paiva, P. C., Petersen, L. H. & Schulze, A. Part II 47, 189226 (2000). The bearded fireworm (Hermodice carunculata) is a type of marine bristleworm belonging to the Amphinomidae family, native to the tropical Atlantic Ocean and the Mediterranean Sea. The neuropodial tuft probably only contains a single type of chaetae (Gustafson, Reference Gustafson1930). Ser. Close this message to accept cookies or find out how to manage your cookie settings. Huggett, J. Schulze, Anja PubMed However, heme-transporter activity (proton-coupled folate transporter) was down-regulated at the hypoxic timepoints and protein ubiquitination was down-regulated at the normoxic timepoints. UK. & Griffiths, C. Some relationships between elevation, physico-chemical variables and biota of intertidal rock pools. Toso, A. & Rosenberg, R. Marine benthic hypoxia: A review of its ecological effects and the behavioural responses of benthic macrofauna. Natl. Cruz Ramos, Mariel A. Protection of host anemones by snapping shrimp: a case for symbiotic mutualism? Hermodice carunculata is common in Caribbean coral reefs, including reef crests exposed at low tide, with significant short-term fluctuations in temperature, salinity and dissolved oxygen. A better understanding of organismal responses to hypoxia in individual species is a crucial step for predicting ecosystem responses. & Halanych, K. M. Discovery of novel hemocyanin-like genes in Metazoans. This implies that downstream hypoxia responses may not only be triggered through oxygen-dependent degradation of HIF-1, but possibly also through a modulation of expression levels depending on DO levels. The up-regulation of Notch proteins, associated with development (especially that of the heart) under hypoxia conditions has been described in zebrafish, Danio rerio32. Fai, Sergio Harborne, A. R., Rogers, A., Bozec, Y.-M. & Mumby, P. J. The temperature in the aquaria tanks were maintained at 20.11.5 C. https://doi.org/10.1093/bioinformatics/btu333 (2014). Wannamaker, C. M. & Rice, J. The most well know trait of the Fireworm is there bioluminescence during sexual activity. Soneson, C., Love, M. I. Sumida, Paulo Yukio Gomes 249, 145163 (2000). Clim. 2020. for this article. 92, 55105514 (1995). & Rosenberg, R. Marine benthic hypoxia: A review of its ecological effects and the behavioural responses of benthic macrofauna. The bearded fireworm is a voracious predator that supplements its diet with plant material. While most of the differentially expressed genes in the Fig. The increase in expression of genes related to epithelial morphogenesis after 6 h (Table 5) may be the first sign of increasing branchial filament formation in this species to cope with hypoxic conditions, which occurs both under intermittent38 and chronic hypoxia39. If they can understand how it is possible to keep light so stable for such a long time, it would provide opportunities to use that protein or reaction in biomedical, bioengineering and other fields-the same way other proteins have been used. Simonini, Roberto [4], https://en.wikipedia.org/w/index.php?title=Hermodice_carunculata&oldid=1150830341, This page was last edited on 20 April 2023, at 11:03. Usp19 interacts with the N-terminus of HIF-1 which is also where the chaperone, Heat shock protein 90 (Hsp90), associates to stabilize HIF-1 (Fig. The HIF transcription factor consists of two constitutively expressed subunits known as HIF-1 and aryl hydrocarbon nuclear translator (ARNT) or HIF-1 (Fig. Goes without saying that we neither poke or prod with our fingers while diving! Most notably, branchial surface area increases in response to both intermittent38 and chronic39 hypoxia. Scientific name Hermodice Carunculata, the Bearded Fireworms grow to a size of 5cm to 10cm but can reach up to 35cm in length. "useRatesEcommerce": true Lenihan, H. S. & Peterson, C. H. How habitat degradation through fishery disturbance enhances impacts of hypoxia on oyster reefs. Sci. On the left, we compared the chronic hypoxia treatments (a, c), and on the right, (b, d) those worms in captivity for the chronic hypoxia trial were compared to those sampled from the natural environment (Brazil and Florida). and Arias-Gonzlez, Jess Ernesto Sahlmann, A., Wolf, R., Holth, T. F., Titelman, J. Mar. Ecol. Biol. Vaquer-Sunyer, R. & Duarte, C. M. Thresholds of hypoxia for marine biodiversity. PubMed They have also been found at or near the surface in flotsam and can occur to at least 60m. They are often strikingly beautiful and very colorful and, unlike the other two groups of annelids. Background: The amphinomid polychaete Hermodice carunculata is a cosmopolitan and ecologically important omnivore in coral reef ecosystems, preying on a diverse suite of reef organisms and potentially acting as a vector for coral disease. 2018. Our control DO levels were similar to prevailing conditions around the time of capture of the field-collected specimens; consequently, the fewest DEFs were found between the Normal treatment and the field-collected worms. Research conducted by Scripps marine biologists reveals that the worms also may use the light as a defensive measure. Description This worm preys on soft corals and anemones but it is rare in home aquariums. Petersen, Lene H. Chemosphere 153, 198204 (2016). Cluster 1 contained genes associated with epithelial cell morphogenesis and metabolism and were expressed at higher levels after the first timepoint of hypoxia but decreased to around normal levels after the second 6-h hypoxia block (timepoint 3). They were fed 0.5 g of Loligo spp. 10, 222 (2009). J. Dev. :: SCRIPPS OCEANOGRAPHY NEWS : : Scripps Scientists Help Decode Mysterious Green Glow of the Sea ::. Light micrographs (LM) or scanning electron micrographs (SEM) of chaetal structure in Hermodice carunculata. Castelli, Alberto Predicted effects of climate change on northern Gulf of Mexico hypoxia. Biotechnol. We are only beginning to understand the long-term consequences of these environmental stressors, separately and in combination, on biological communities. Zoccola, D. et al. D. Meyer, pers. Continue Reading after the facts. Given documented physiological responses to chronic vs intermittent hypoxia, we can expect differences in gene expression patterns as well especially with regards to oxidative stress61,62. These symptoms can last up to several weeks. Morais, Pedro Annu. Multiple stressors and the functioning of coral reefs. However, it is important to note that a significant decrease in expression of Fibropellin-1 was seen after 5 and 8 days in the clam81. If Usp19 is absent under oxygen depletion, HIF-1 will follow an oxygen-independent pathway to degradation not shown in Fig. ADS Hermodice carunculata tolerates a wide range of environmental conditions, including temperature, salinity, oxygen saturation and various types of pollution. We used the TMM (trimmed-mean of M values) method for normalization of reads and CPM (counts per million) filter based on library sizes according to the edgeR protocol68. Hermodice carunculata is a common species of amphinomid polychaete with a distribution throughout the Atlantic Ocean, the Caribbean, Gulf of Mexico, Mediterranean and Red Seas (Yez-Rivera & Salazar-Vallejo, Reference Yez-Rivera and Salazar-Vallejo2011; Ahrens et al., Reference Ahrens, Borda, Barroso, Paiva, Campbell, Wolf, Nugues, Rouse and Schulze2013).
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