Title: Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins
Abstract 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 (genusCladocopium) 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 fromA. hyacinthusalso contain filamentous VLPs, and these cells are more degraded than theirin hospitecounterparts. 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 generaBreviolum, Cladocopium, andDurusdinium. 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. more »« less
Veglia, A. J.; Beavers, K.; Van Buren, E. W.; Meiling, S. S.; Muller, E. M.; Smith, T. B.; Holstein, D. M.; Apprill, A.; Brandt, M. E.; Mydlarz, L. D.; et al
(, Microbiology Resource Announcements)
Matthijnssens, Jelle
(Ed.)
ABSTRACT Stony coral tissue loss disease (SCTLD) is decimating Caribbean corals. Here, through the metatranscriptomic assembly and annotation of two alphaflexivirus-like strains, we provide genomic evidence of filamentous viruses in SCTLD-affected, -exposed, and -unexposed coral colonies. These data will assist in clarifying the roles of viruses in SCTLD.
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.; et al
(, Nature Communications)
Abstract 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 ofrab7, 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.
Grupstra, Carsten G. B.; Howe-Kerr, Lauren I.; Veglia, Alex J.; Bryant, Reb L.; Coy, Samantha R.; Blackwelder, Patricia L.; Correa, Adrienne M. S.
(, The ISME Journal)
Abstract Climate change-driven ocean warming is increasing the frequency and severity of bleaching events, in which corals appear whitened after losing their dinoflagellate endosymbionts (family Symbiodiniaceae). Viral infections of Symbiodiniaceae may contribute to some bleaching signs, but little empirical evidence exists to support this hypothesis. We present the first temporal analysis of a lineage of Symbiodiniaceae-infecting positive-sense single-stranded RNA viruses (“dinoRNAVs”) in coral colonies, which were exposed to a 5-day heat treatment (+2.1 °C). A total of 124 dinoRNAV major capsid protein gene “aminotypes” (unique amino acid sequences) were detected from five colonies of two closely related Pocillopora-Cladocopium (coral-symbiont) combinations in the experiment; most dinoRNAV aminotypes were shared between the two coral-symbiont combinations (64%) and among multiple colonies (82%). Throughout the experiment, seventeen dinoRNAV aminotypes were found only in heat-treated fragments, and 22 aminotypes were detected at higher relative abundances in heat-treated fragments. DinoRNAVs in fragments of some colonies exhibited higher alpha diversity and dispersion under heat stress. Together, these findings provide the first empirical evidence that exposure to high temperatures triggers some dinoRNAVs to switch from a persistent to a productive infection mode within heat-stressed corals. Over extended time frames, we hypothesize that cumulative dinoRNAV production in the Pocillopora-Cladocopium system could affect colony symbiotic status, for example, by decreasing Symbiodiniaceae densities within corals. This study sets the stage for reef-scale investigations of dinoRNAV dynamics during bleaching events.
Cróquer, Aldo; Weil, Ernesto; Rogers, Caroline S.
(, Frontiers in Marine Science)
null
(Ed.)
For several decades, white plagues (WPDs: WPD-I, II and III) and more recently, stony coral tissue loss disease (SCTLD) have significantly impacted Caribbean corals. These diseases are often difficult to separate in the field as they produce similar gross signs. Here we aimed to compare what we know about WPD and SCTLD in terms of: (1) pathology, (2) etiology, and (3) epizootiology. We reviewed over 114 peer-reviewed publications from 1973 to 2021. Overall, WPD and SCTLD resemble each other macroscopically, mainly due to the rapid tissue loss they produce in their hosts, however, SCTLD has a more concise case definition. Multiple-coalescent lesions are often observed in colonies with SCTLD and rarely in WPD. A unique diagnostic sign of SCTLD is the presence of bleached circular areas when SCTLD lesions are first appearing in the colony. The paucity of histopathologic archives for WPDs for multiple species across geographies makes it impossible to tell if WPD is the same as SCTLD. Both diseases alter the coral microbiome. WPD is controversially regarded as a bacterial infection and more recently a viral infection, whereas for SCTLD the etiology has not been identified, but the putative pathogen, likely to be a virus, has not been confirmed yet. Most striking differences between WPD and SCTLD have been related to duration and phases of epizootic events and mortality rates. While both diseases may become highly prevalent on reefs, SCTLD seems to be more persistent even throughout years. Both transmit directly (contact) and horizontally (waterborne), but organism-mediated transmission is only proven for WPD-II. Given the differences and similarities between these diseases, more detailed information is needed for a better comparison. Specifically, it is important to focus on: (1) tagging colonies to look at disease progression and tissue mortality rates, (2) tracking the fate of the epizootic event by looking at initial coral species affected, the features of lesions and how they spread over colonies and to a wider range of hosts, (3) persistence across years, and (4) repetitive sampling to look at changes in the microbiome as the disease progresses. Our review shows that WPDs and SCTLD are the major causes of coral tissue loss recorded in the Caribbean.
Howe-Kerr, Lauren I.; Grupstra, Carsten G. B.; Rabbitt, Kristen M.; Conetta, Dennis; Coy, Samantha R.; Klinges, J. Grace; Maher, Rebecca L.; McConnell, Kaitlin M.; Meiling, Sonora S.; Messyasz, Adriana; et al
(, ISME Communications)
Abstract Viruses can affect coral health by infecting their symbiotic dinoflagellate partners (Symbiodiniaceae). Yet, viral dynamics in coral colonies exposed to environmental stress have not been studied at the reef scale, particularly within individual viral lineages. We sequenced the viral major capsid protein (mcp) gene of positive-sense single-stranded RNA viruses known to infect symbiotic dinoflagellates (‘dinoRNAVs’) to analyze their dynamics in the reef-building coral, Porites lobata. We repeatedly sampled 54 colonies harboring Cladocopium C15 dinoflagellates, across three environmentally distinct reef zones (fringing reef, back reef, and forereef) around the island of Moorea, French Polynesia over a 3-year period and spanning a reef-wide thermal stress event. By the end of the sampling period, 28% (5/18) of corals in the fringing reef experienced partial mortality versus 78% (14/18) of corals in the forereef. Over 90% (50/54) of colonies had detectable dinoRNAV infections. Reef zone influenced the composition and richness of viral mcp amino acid types (‘aminotypes’), with the fringing reef containing the highest aminotype richness. The reef-wide thermal stress event significantly increased aminotype dispersion, and this pattern was strongest in the colonies that experienced partial mortality. These findings demonstrate that dinoRNAV infections respond to environmental fluctuations experienced in situ on reefs. Further, viral productivity will likely increase as ocean temperatures continue to rise, potentially impacting the foundational symbiosis underpinning coral reef ecosystems.
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., and Correa, Adrienne M. S. Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins. The ISME Journal 17.12 Web. doi:10.1038/s41396-023-01526-6.
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 virus-like particles are present in coral dinoflagellates across genera and ocean basins. The ISME Journal, 17 (12). https://doi.org/10.1038/s41396-023-01526-6
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., and Correa, Adrienne M. S.
"Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins". The ISME Journal 17 (12). Country unknown/Code not available: Nature Publishing Group. https://doi.org/10.1038/s41396-023-01526-6.https://par.nsf.gov/biblio/10471944.
@article{osti_10471944,
place = {Country unknown/Code not available},
title = {Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins},
url = {https://par.nsf.gov/biblio/10471944},
DOI = {10.1038/s41396-023-01526-6},
abstractNote = {Abstract 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 (genusCladocopium) 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 fromA. hyacinthusalso contain filamentous VLPs, and these cells are more degraded than theirin hospitecounterparts. 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 generaBreviolum, Cladocopium, andDurusdinium. 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.},
journal = {The ISME Journal},
volume = {17},
number = {12},
publisher = {Nature Publishing Group},
author = {Howe-Kerr, Lauren I. and Knochel, Anna M. and Meyer, Matthew D. and Sims, Jordan A. and Karrick, Carly E. and Grupstra, Carsten G. B. and Veglia, Alex J. and Thurber, Andrew R. and Vega Thurber, Rebecca L. and Correa, Adrienne M. S.},
}
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