Viral-Like Particles Are Associated With Endosymbiont Pathology in Florida Corals Affected by Stony Coral Tissue Loss Disease

Abstract

Stony coral tissue loss disease (SCTLD) was first documented in 2014 near the Port of Miami, Florida, and has since spread north and south along Florida’s Coral Reef, killing large numbers of more than 20 species of coral and leading to the functional extinction of at least one species, Dendrogyra cylindrus. SCTLD is assumed to be caused by bacteria based on presence of different molecular assemblages of bacteria in lesioned compared to apparently healthy tissues, its apparent spread among colonies, and cessation of spread of lesions in individual colonies treated with antibiotics. However, light microscopic examination of tissues of corals affected with SCTLD has not shown bacteria associated with tissue death. Rather, microscopy shows dead and dying coral cells and symbiotic dinoflagellates (endosymbionts) indicating a breakdown of host cell and endosymbiont symbiosis. It is unclear whether host cells die first leading to death of endosymbionts or vice versa. Based on microscopy, hypotheses as to possible causes of SCTLD include infectious agents not visible at the light microscopy level or toxicosis, perhaps originating from endosymbionts. To clarify this, we examined corals affected with SCTLD and apparently healthy corals using transmission electron microscopy. Endosymbionts in SCTLD-affected and apparently healthy corals consistently had varying degrees of pathology associated with elongated particles compatible in morphology with filamentous positive single-stranded RNA viruses of plants termed anisometric viral-like particles (AVLP). There was apparent progression from early to late replication of AVLP in the cytoplasm of endosymbionts adjacent to or at times within chloroplasts, with morphologic changes in chloroplasts consistent with those seen in plant cells infected by viruses. Coral host cell pathology appeared limited to massive proliferation and lysis of mucus cells. Based on these findings, we hypothesize that SCTLD is a viral disease of endosymbionts leading to coral host death. Efforts to confirm the presence of a virus associated with SCTLD through other means would be appropriate. These include showing the presence of a virus through molecular assays such as deep sequencing, attempts to grow this virus in the laboratory through culture of endosymbionts, localization of virus in tissue sections using immunohistochemistry or in situ hybridization, and experimental infection of known-virus-negative corals to replicate disease at the gross and microscopic level.

Advances in coral immunity ‘omics in response to disease outbreaks

“…The pathology of stony coral tissue loss disease (SCTLD) is characterized by the presence of multifocal lytic necrosis that starts within the gastrodermis and progresses to the outer epithelial layer Landsberg et al, 2020). First reported in 2014, this disease affects at least 24 different Caribbean coral species, is waterborne, and the causative agent is suspected to be microbial in origin (NOAA, 2018;Dobbelaere et al, 2020;Landsberg et al, 2020;Muller et al, 2020;Work et al, 2021). While the causative agent of the disease is still unknown, there is growing evidence that algal symbionts are tightly implicated in the etiology of this disease based on (1) histological studies showing rapid deterioration of gastrodermal cells Landsberg et al, 2020), (2) differential susceptibility of corals manipulated to host different Symbiodiniaceae (Dennison et al, 2021), (3) reduced incidence in bleached corals with reduced symbiont loads (Neely et al, 2020), and (4) correlations between SCTLD disease signs and the presence of viruses in associated Symbiodiniaceae (Work et al, 2021;Veglia et al, 2022).…”

Reef Sediments Can Act As a Stony Coral Tissue Loss Disease Vector

“…Likewise, examination of microbial communities in SCTLD-affected corals and their surrounding environments (e.g., water and sediments) have identified indicator bacterial taxa that distinguish healthy and infected individuals, including some previously-described coral pathogens (Meyer et al, 2019;Rosales et al, 2020;Ushijima et al, 2020;Becker et al, 2021). A recent microscopy-based study also posited that viruses may play a role in the onset of the disease through infection of Symbiodiniaceae (Work et al, 2021), although this hypothesis has not been tested experimentally.…”

Alphaflexivirus Genomes in Stony Coral Tissue Loss Disease-Affected, Disease-Exposed, and Disease-Unexposed Coral Colonies in the U.S. Virgin Islands

“…Viral infections of endosymbiotic dinoflagellates (family Symbiodiniaceae) within coral tissues are hypothesized to play a role in stony coral tissue loss disease (SCTLD) ( 1 ), a widespread disease that affects Caribbean stony corals ( 2 – 4 ). Here, we present high-quality draft genome sequences for two viruses in the family Alphaflexiviridae , coral holobiont-associated alphaflexvirus (CHFV) 1 and 2 ( Fig.…”