Browsing by Author "Correa, Adrienne M. S."

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    Building consensus around the assessment and interpretation of Symbiodiniaceae diversity
    (PeerJ, Inc, 2023) Davies, Sarah W.; Gamache, Matthew H.; Howe-Kerr, Lauren I.; Kriefall, Nicola G.; Baker, Andrew C.; Banaszak, Anastazia T.; Bay, Line Kolind; Bellantuono, Anthony J.; Bhattacharya, Debashish; Chan, Cheong Xin; Claar, Danielle C.; Coffroth, Mary Alice; Cunning, Ross; Davy, Simon K.; Campo, Javier del; Díaz-Almeyda, Erika M.; Frommlet, Jörg C.; Fuess, Lauren E.; González-Pech, Raúl A.; Goulet, Tamar L.; Hoadley, Kenneth D.; Howells, Emily J.; Hume, Benjamin C. C.; Kemp, Dustin W.; Kenkel, Carly D.; Kitchen, Sheila A.; LaJeunesse, Todd C.; Lin, Senjie; McIlroy, Shelby E.; McMinds, Ryan; Nitschke, Matthew R.; Oakley, Clinton A.; Peixoto, Raquel S.; Prada, Carlos; Putnam, Hollie M.; Quigley, Kate; Reich, Hannah G.; Reimer, James Davis; Rodriguez-Lanetty, Mauricio; Rosales, Stephanie M.; Saad, Osama S.; Sampayo, Eugenia M.; Santos, Scott R.; Shoguchi, Eiichi; Smith, Edward G.; Stat, Michael; Stephens, Timothy G.; Strader, Marie E.; Suggett, David J.; Swain, Timothy D.; Tran, Cawa; Traylor-Knowles, Nikki; Voolstra, Christian R.; Warner, Mark E.; Weis, Virginia M.; Wright, Rachel M.; Xiang, Tingting; Yamashita, Hiroshi; Ziegler, Maren; Correa, Adrienne M. S.; Parkinson, John Everett
    Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.
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    Consumer feces impact coral health in guild-specific ways
    (Frontiers Media S.A., 2023) Grupstra, Carsten G. B.; Howe-Kerr, Lauren I.; van der Meulen, Jesse A.; Veglia, Alex J.; Coy, Samantha R.; Correa, Adrienne M. S.
    Animal waste products are an important component of nutrient cycles and result in the trophic transmission of diverse microorganisms. There is growing recognition that the feces of consumers, such as predators, may impact resource species, their prey, via physical effects and/or microbial activity. We tested the effect of feces from distinct fish trophic groups on coral health and used heat-killed fecal controls to tease apart physical versus microbial effects of contact with fecal material. Fresh grazer/detritivore fish feces caused lesions more frequently on corals, and lesions were 4.2-fold larger than those from sterilized grazer/detritivore feces; in contrast, fresh corallivore feces did not cause more frequent or larger lesions than sterilized corallivore feces. Thus, microbial activity in grazer/detritivore feces, but not corallivore feces, was harmful to corals. Characterization of bacterial diversity in feces of 10 reef fish species, ranging from obligate corallivores to grazer/detritivores, indicated that our experimental findings may be broadly generalizable to consumer guild, since feces of some obligate corallivores contained ~2-fold higher relative abundances of coral mutualist bacteria (e.g., Endozoicomonadaceae), and lower abundances of the coral pathogen, Vibrio coralliilyticus, than feces of some grazer/detritivores. These findings recontextualize the ecological roles of consumers on coral reefs: although grazer/detritivores support coral reef health in various ways (e.g., promoting coral settlement and herbivory through the removal of detritus and sediments from the algal matrix), they also disperse coral pathogens. Corallivore predation can wound corals, yet their feces contain potentially beneficial coral-associated bacteria, supporting the hypothesized role of consumers, and corallivores in particular, in coral symbiont dispersal. Such consumer-mediated microbial dispersal as demonstrated here has broad implications for environmental management.
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    Endogenous viral elements reveal associations between a non-retroviral RNA virus and symbiotic dinoflagellate genomes
    (Springer Nature, 2023) Veglia, Alex J.; Bistolas, Kalia S. I.; Voolstra, Christian R.; Hume, Benjamin C. C.; Ruscheweyh, Hans-Joachim; Planes, Serge; Allemand, Denis; Boissin, Emilie; Wincker, Patrick; Poulain, Julie; Moulin, Clémentine; Bourdin, Guillaume; Iwankow, Guillaume; Romac, Sarah; Agostini, Sylvain; Banaigs, Bernard; Boss, Emmanuel; Bowler, Chris; de Vargas, Colomban; Douville, Eric; Flores, Michel; Forcioli, Didier; Furla, Paola; Galand, Pierre E.; Gilson, Eric; Lombard, Fabien; Pesant, Stéphane; Reynaud, Stéphanie; Sunagawa, Shinichi; Thomas, Olivier P.; Troublé, Romain; Zoccola, Didier; Correa, Adrienne M. S.; Vega Thurber, Rebecca L.
    Endogenous viral elements (EVEs) offer insight into the evolutionary histories and hosts of contemporary viruses. This study leveraged DNA metagenomics and genomics to detect and infer the host of a non-retroviral dinoflagellate-infecting +ssRNA virus (dinoRNAV) common in coral reefs. As part of the Tara Pacific Expedition, this study surveyed 269 newly sequenced cnidarians and their resident symbiotic dinoflagellates (Symbiodiniaceae), associated metabarcodes, and publicly available metagenomes, revealing 178 dinoRNAV EVEs, predominantly among hydrocoral-dinoflagellate metagenomes. Putative associations between Symbiodiniaceae and dinoRNAV EVEs were corroborated by the characterization of dinoRNAV-like sequences in 17 of 18 scaffold-scale and one chromosome-scale dinoflagellate genome assembly, flanked by characteristically cellular sequences and in proximity to retroelements, suggesting potential mechanisms of integration. EVEs were not detected in dinoflagellate-free (aposymbiotic) cnidarian genome assemblies, including stony corals, hydrocorals, jellyfish, or seawater. The pervasive nature of dinoRNAV EVEs within dinoflagellate genomes (especially Symbiodinium), as well as their inconsistent within-genome distribution and fragmented nature, suggest ancestral or recurrent integration of this virus with variable conservation. Broadly, these findings illustrate how +ssRNA viruses may obscure their genomes as members of nested symbioses, with implications for host evolution, exaptation, and immunity in the context of reef health and disease.
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    Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins
    (Oxford University Press, 2023) Howe-Kerr, Lauren I.; Knochel, Anna M.; Meyer, Matthew D.; Sims, Jordan A.; Karrick, Carly E.; Grupstra, Carsten G. B.; Veglia, Alex J.; Thurber, Andrew R.; Vega Thurber, Rebecca L.; Correa, Adrienne M. S.
    Filamentous viruses are hypothesized to play a role in stony coral tissue loss disease (SCTLD) through infection of the endosymbiotic dinoflagellates (Family Symbiodiniaceae) of corals. To evaluate this hypothesis, it is critical to understand the global distribution of filamentous virus infections across the genetic diversity of Symbiodiniaceae hosts. Using transmission electron microscopy, we demonstrate that filamentous virus-like particles (VLPs) are present in over 60% of Symbiodiniaceae cells (genus Cladocopium) within Pacific corals (Acropora hyacinthus, Porites c.f. lobata); these VLPs are more prevalent in Symbiodiniaceae of in situ colonies experiencing heat stress. Symbiodiniaceae expelled from A. hyacinthus also contain filamentous VLPs, and these cells are more degraded than their in hospite counterparts. Similar to VLPs reported from SCTLD-affected Caribbean reefs, VLPs range from ~150 to 1500 nm in length and 16–37 nm in diameter and appear to constitute various stages in a replication cycle. Finally, we demonstrate that SCTLD-affected corals containing filamentous VLPs are dominated by diverse Symbiodiniaceae lineages from the genera Breviolum, Cladocopium, and Durusdinium. Although this study cannot definitively confirm or refute the role of filamentous VLPs in SCTLD, it demonstrates that filamentous VLPs are not solely observed in SCTLD-affected corals or reef regions, nor are they solely associated with corals dominated by members of a particular Symbiodiniaceae genus. We hypothesize that filamentous viruses are a widespread, common group that infects Symbiodiniaceae. Genomic characterization of these viruses and empirical tests of the impacts of filamentous virus infection on Symbiodiniaceae and coral colonies should be prioritized.
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    Stony coral tissue loss disease induces transcriptional signatures of in situ degradation of dysfunctional Symbiodiniaceae
    (Springer Nature, 2023) Beavers, Kelsey M.; Van Buren, Emily W.; Rossin, Ashley M.; Emery, Madison A.; Veglia, Alex J.; Karrick, Carly E.; MacKnight, Nicholas J.; Dimos, Bradford A.; Meiling, Sonora S.; Smith, Tyler B.; Apprill, Amy; Muller, Erinn M.; Holstein, Daniel M.; Correa, Adrienne M. S.; Brandt, Marilyn E.; Mydlarz, Laura D.
    Stony coral tissue loss disease (SCTLD), one of the most pervasive and virulent coral diseases on record, affects over 22 species of reef-building coral and is decimating reefs throughout the Caribbean. To understand how different coral species and their algal symbionts (family Symbiodiniaceae) respond to this disease, we examine the gene expression profiles of colonies of five species of coral from a SCTLD transmission experiment. The included species vary in their purported susceptibilities to SCTLD, and we use this to inform gene expression analyses of both the coral animal and their Symbiodiniaceae. We identify orthologous coral genes exhibiting lineage-specific differences in expression that correlate to disease susceptibility, as well as genes that are differentially expressed in all coral species in response to SCTLD infection. We find that SCTLD infection induces increased expression of rab7, an established marker of in situ degradation of dysfunctional Symbiodiniaceae, in all coral species accompanied by genus-level shifts in Symbiodiniaceae photosystem and metabolism gene expression. Overall, our results indicate that SCTLD infection induces symbiophagy across coral species and that the severity of disease is influenced by Symbiodiniaceae identity.
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    Visualization of RNA virus infection in a marine protist with a universal biomarker
    (Springer Nature, 2023) Coy, Samantha R.; Utama, Budi; Spurlin, James W.; Kim, Julia G.; Deshmukh, Harshavardhan; Lwigale, Peter; Nagasaki, Keizo; Correa, Adrienne M. S.
    Half of the marine virosphere is hypothesized to be RNA viruses (kingdom Orthornavirae) that infect abundant micro-eukaryotic hosts (e.g. protists). To test this, quantitative approaches that broadly track infections in situ are needed. Here, we describe a technique—dsRNA-Immunofluorescence (dsRIF)—that uses a double-stranded RNA (dsRNA) targeting monoclonal antibody to assess host infection status based on the presence of dsRNA, a replicative intermediate of all Orthornavirae infections. We show that the dinoflagellate Heterocapsa circularisquama produces dsRIF signal ~ 1000 times above background autofluorescence when infected by the + ssRNA virus HcRNAV. dsRNA-positive virocells were detected across > 50% of the 48-h infection cycle and accumulated to represent at least 63% of the population. Photosynthetic and chromosomal integrity remained intact during peak replication, indicating HcRNAV infection does not interrupt these processes. This work validates the use of dsRIF on marine RNA viruses and their hosts, setting the stage for quantitative environmental applications that will accelerate understanding of virus-driven ecosystem impacts.