Disturbance Driven Colony Fragmentation as a Driver of a Coral Disease Outbreak

In September of 2010, Brewer’s Bay reef, located in St. Thomas (U.S. Virgin Islands), was simultaneously affected by abnormally high temperatures and the passage of a hurricane that resulted in the mass bleaching and fragmentation of its coral community. An outbreak of a rapid tissue loss disease among coral colonies was associated with these two disturbances. Gross lesion signs and lesion progression rates indicated that the disease was most similar to the Caribbean coral disease white plague type 1. Experiments indicated that the disease was transmissible through direct contact between colonies, and five-meter radial transects showed a clustered spatial distribution of disease, with diseased colonies being concentrated within the first meter of other diseased colonies. Disease prevalence and the extent to which colonies were bleached were both significantly higher on unattached colony fragments than on attached colonies, and disease occurred primarily on fragments found in direct contact with sediment. In contrast to other recent studies, disease presence was not related to the extent of bleaching on colonies. The results of this study suggest that colony fragmentation and contact with sediment played primary roles in the initial appearance of disease, but that the disease was capable of spreading among colonies, which suggests secondary transmission is possible through some other, unidentified mechanism

Gene expression of endangered coral (Orbicella spp.) in flower garden banks National Marine Sanctuary after Hurricane Harvey

About 190 km south of the Texas–Louisiana border, the East and West Flower Garden Banks (FGB) have maintained > 50% coral cover with infrequent and minor incidents of disease or bleaching since monitoring began in the 1970s. However, a mortality event, affecting 5.6 ha (2.6% of the area) of the East FGB, occurred in late July 2016 and coincided with storm-generated freshwater runoff extending offshore and over the reef system. To capture the immediate effects of storm-driven freshwater runoff on coral and symbiont physiology, we leveraged the heavy rainfall associated with Hurricane Harvey in late August 2017 by sampling FGB corals at two time points: September 2017, when surface water salinity was reduced (∼34 ppt); and 1 month later when salinity had returned to typical levels (∼36 ppt in October 2017). Tissue samples (N = 47) collected midday were immediately preserved for gene expression profiling from two congeneric coral species (Orbicella faveolata and Orbicella franksi) from the East and West FGB to determine the physiological consequences of storm-derived runoff. In the coral, differences between host species and sampling time points accounted for the majority of differentially expressed genes. Gene ontology enrichment for genes differentially expressed immediately after Hurricane Harvey indicated increases in cellular oxidative stress responses. Although tissue loss was not observed on FGB reefs following Hurricane Harvey, our results suggest that poor water quality following this storm caused FGB corals to experience sub-lethal stress. We also found dramatic expression differences across sampling time points in the coral’s algal symbiont, Breviolum minutum. Some of these differentially expressed genes may be involved in the symbionts’ response to changing environments, including a group of differentially expressed post-transcriptional RNA modification genes. In this study, we cannot disentangle the effects of reduced salinity from the collection time point, so these expression patterns could also be related to seasonality. These findings highlight the urgent need for continued monitoring of these reef systems to establish a baseline for gene expression of healthy corals in the FGB system across seasons, as well as the need for integrated solutions to manage stormwater runoff in the Gulf of Mexico.https://www.frontiersin.org/articles/10.3389/fmars.2019.00672/fullPublished versionPublished versio

Symbiont Community Diversity is More Variable in Corals That Respond Poorly to Stress

Coral reefs are declining globally as climate change and local water quality press environmental conditions beyond the physiological tolerances of holobionts—the collective of the host and its microbial symbionts. To assess the relationship between symbiont composition and holobiont stress tolerance, community diversity metrics were quantified for dinoflagellate endosymbionts (Family: Symbiodiniaceae) from eight Acropora millepora genets that thrived under or responded poorly to various stressors. These eight selected genets represent the upper and lower tails of the response distribution of 40 coral genets that were exposed to four stress treatments (and control conditions) in a 10-day experiment. Specifically, four ‘best performer’ coral genets were analyzed at the end of the experiment because they survived high temperature, high pCO2, bacterial exposure, or combined stressors, whereas four ‘worst performer’ genets were characterized because they experienced substantial mortality under these stressors. At the end of the experiment, seven of eight coral genets mainly hosted Cladocopium symbionts, whereas the eighth genet was dominated by both Cladocopium and Durusdinium symbionts. Symbiodiniaceae alpha and beta diversity were higher in worst performing genets than in best performing genets. Symbiont communities in worst performers also differed more after stress exposure relative to their controls (based on normalized proportional differences in beta diversity), than did best performers. A generalized joint attribute model estimated the influence of host genet and treatment on Symbiodiniaceae community composition and identified strong associations among particular symbionts and host genet performance, as well as weaker associations with treatment. Although dominant symbiont physiology and function contribute to host performance, these findings emphasize the importance of symbiont community diversity and stochasticity as components of host performance. Our findings also suggest that symbiont community diversity metrics may function as indicators of resilience and have potential applications in diverse disciplines from climate change adaptation to agriculture and medicine

Viral outbreak in corals associated with an in situ bleaching event: atypical herpes-like viruses and a new megavirus infecting Symbiodinium

Previous studies of coral viruses have employed either microscopy or metagenomics, but few have attempted to comprehensively link the presence of a virus-like particle (VLP) to a genomic sequence. We conducted transmission electron microscopy imaging and virome analysis in tandem to characterize the most conspicuous viral types found within the dominant Pacific reef-building coral genus Acropora. Collections for this study inadvertently captured what we interpret as a natural outbreak of viral infection driven by aerial exposure of the reef flat coincident with heavy rainfall and concomitant mass bleaching. All experimental corals in this study had high titers of viral particles. Three of the dominant VLPs identified were observed in all tissue layers and budding out from the epidermis, including viruses that were ∼70, ∼120, and ∼150 nm in diameter; these VLPs all contained electron dense cores. These morphological traits are reminiscent of retroviruses, herpesviruses, and nucleocytoplasmic large DNA viruses (NCLDVs), respectively. Some 300–500 nm megavirus-like VLPs also were observed within and associated with dinoflagellate algal endosymbiont (Symbiodinium) cells. Abundant sequence similarities to a gammaretrovirus, herpesviruses, and members of the NCLDVs, based on a virome generated from five Acropora aspera colonies, corroborated these morphology-based identifications. Additionally sequence similarities to two diagnostic genes, a MutS and (based on re-annotation of sequences from another study) a DNA polymerase B gene, most closely resembled Pyramimonas orientalis virus, demonstrating the association of a cosmopolitan megavirus with Symbiodinium. We also identified several other virus-like particles in host tissues, along with sequences phylogenetically similar to circoviruses, phages, and filamentous viruses. This study suggests that viral outbreaks may be a common but previously undocumented component of natural bleaching events, particularly following repeated episodes of multiple environmental stressors

Macroborer Presence on Corals Increases with Nutrient Input and Promotes Parrotfish Bioerosion

Bioerosion by reef-dwelling organisms influences net carbonate budgets on reefs worldwide. External bioeroders, such as parrotfish and sea urchins, and internal bioeroders, including sponges and lithophagid bivalves, are major contributors to bioerosion on reefs. Despite their importance, few studies have examined how environmental (e.g., nutrients) or biological drivers (e.g., the actions of other bioeroders) may influence bioeroder dynamics on reefs. For example, internal bioeroders could promote external bioerosion by weakening the coral skeletal matrix. Our study investigated: ( 1) whether nutrient supply influences the dynamics between internal and external bioeroders and ( 2) how the presence of a boring bivalve, Lithophaga spp., influences parrotfish bioerosion on massive Porites corals. We hypothesized that nutrient supply would be positively correlated with Lithophaga densities on massive Porites colonies, and that as bivalve density increased, the frequency and intensity of parrotfish bioerosion would increase. To test these hypotheses, we analyzed six time points over a 10-yr period from a time series of benthic images and nitrogen content of a dominant macroalga from the fringing reefs around Moorea, French Polynesia. We found Lithophaga densities were positively correlated with nitrogen availability. Further, massive Porites that are more infested with Lithophaga had both a higher probability of being bitten by parrotfish and a higher density of bite scars from parrotfishes. Our findings indicate that increasing nutrient availability may strengthen the relationship between internal and external bioeroders, suggesting that colonies at more eutrophic sites may experience higher bioerosion rates

Experimental transmission of Stony Coral Tissue Loss Disease results in differential microbial responses within coral mucus and tissue

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Huntley, N., Brandt, M., Becker, C., Miller, C., Meiling, S., Correa, A., Holstein, D., Muller, E., Mydlarz, L., Smith, T., & Apprill, A. Experimental transmission of Stony Coral Tissue Loss Disease results in differential microbial responses within coral mucus and tissue. ISME Communications, 2(1), (2022): 46, https://doi.org/10.1038/s43705-022-00126-3.Stony coral tissue loss disease (SCTLD) is a widespread and deadly disease that affects nearly half of Caribbean coral species. To understand the microbial community response to this disease, we performed a disease transmission experiment on US Virgin Island (USVI) corals, exposing six species of coral with varying susceptibility to SCTLD. The microbial community of the surface mucus and tissue layers were examined separately using a small subunit ribosomal RNA gene-based sequencing approach, and data were analyzed to identify microbial community shifts following disease acquisition, potential causative pathogens, as well as compare microbiota composition to field-based corals from the USVI and Florida outbreaks. While all species displayed similar microbiome composition with disease acquisition, microbiome similarity patterns differed by both species and mucus or tissue microhabitat. Further, disease exposed but not lesioned corals harbored a mucus microbial community similar to those showing disease signs, suggesting that mucus may serve as an early warning detection for the onset of SCTLD. Like other SCTLD studies in Florida, Rhodobacteraceae, Arcobacteraceae, Desulfovibrionaceae, Peptostreptococcaceae, Fusibacter, Marinifilaceae, and Vibrionaceae dominated diseased corals. This study demonstrates the differential response of the mucus and tissue microorganisms to SCTLD and suggests that mucus microorganisms may be diagnostic for early disease exposure.This work was funded by an International Coral Reef Society student grant to N.H., National Science Foundation (NSF) VI EPSCoR 0814417 and 1946412 and NSF (Biological Oceanography) award numbers 1928753 to MEB and TBS, 1928609 to AMSC, 1928817 to EMM, 19228771 to LDM, 1927277 to DMH as well as 1928761 and 1938112 to AA, NSF EEID award number 2109622 to MEB, AA, LDM, and AMSC, and a NOAA OAR Cooperative Institutes award to AA (#NA19OAR4320074). Samples were collected under permit #DFW19057U authorized by the Department of Planning and Natural Resources Coastal Zone Management

Alphaflexivirus genomes in stony coral tissue loss disease-affected, disease-exposed, and disease-unexposed coral colonies in the U.S. Virgin Islands

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Veglia, A., Beavers, K., Van Buren, E., Meiling, S., Muller, E., Smith, T., Holstein, D., Apprill, A., Brandt, M., Mydlarz, L., & Correa, A. Alphaflexivirus genomes in stony coral tissue loss disease-affected, disease-exposed, and disease-unexposed coral colonies in the U.S. Virgin Islands. Microbiology Resource Announcements, 11(2), (2022): e01199–e01121, https://doi.org/10.1128/mra.01199-21.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.This work was supported by the National Science Foundation (Biological Oceanography) award numbers 1928753 to M.E.B. and T.B.S., 1928609 to A.M.S.C., 1928817 to E.M.M., 19228771 to L.D.M., 1927277 to D.M.H., and 1928761 to A.A., as well as by VI EPSCoR (NSF numbers 0814417 and 1946412)

Unified Methods in Collecting, Preserving, and Archiving Coral Bleaching and Restoration Specimens to Increase Sample Utility and Interdisciplinary Collaboration

Coral reefs are declining worldwide primarily because of bleaching and subsequent mortality resulting from thermal stress. Currently, extensive efforts to engage in more holistic research and restoration endeavors have considerably expanded the techniques applied to examine coral samples. Despite such advances, coral bleaching and restoration studies are often conducted within a specific disciplinary focus, where specimens are collected, preserved, and archived in ways that are not always conducive to further downstream analyses by specialists in other disciplines. This approach may prevent the full utilization of unexpended specimens, leading to siloed research, duplicative efforts, unnecessary loss of additional corals to research endeavors, and overall increased costs. A recent US National Science Foundation-sponsored workshop set out to consolidate our collective knowledge across the disciplines of Omics, Physiology, and Microscopy and Imaging regarding the methods used for coral sample collection, preservation, and archiving. Here, we highlight knowledge gaps and propose some simple steps for collecting, preserving, and archiving coral-bleaching specimens that can increase the impact of individual coral bleaching and restoration studies, as well as foster additional analyses and future discoveries through collaboration. Rapid freezing of samples in liquid nitrogen or placing at −80 °C to −20 °C is optimal for most Omics and Physiology studies with a few exceptions; however, freezing samples removes the potential for many Microscopy and Imaging-based analyses due to the alteration of tissue integrity during freezing. For Microscopy and Imaging, samples are best stored in aldehydes. The use of sterile gloves and receptacles during collection supports the downstream analysis of host-associated bacterial and viral communities which are particularly germane to disease and restoration efforts. Across all disciplines, the use of aseptic techniques during collection, preservation, and archiving maximizes the research potential of coral specimens and allows for the greatest number of possible downstream analyses

RNAseq data used to identify Alphaflexivirus genomes in Stony Coral Tissue Loss Disease-affected, disease-exposed, and disease-unexposed coral colonies in the U.S. Virgin Islands (Multi-Species Coral Disease project)

Dataset: RNAseq data used to identify viral genomesRNA-seq data from healthy, SCTLD-exposed, and SCTLD-infected coral samples taken from a transmission experiment carried out in the US Virgin Islands. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/875583NSF Division of Ocean Sciences (NSF OCE) OCE-192877

An investigation of Symbiodiniaceae communities via ITS-2 rDNA amplicon sequencing in Acropora millepora corals from the Great Barrier Reef following exposure to stressors in October 2014

Dataset: Symbiodiniaceae communities in corals with ITS-2 rDNA amplicon sequencingSymbiodiniaceae communities were investigated at three locations on the Great Barrier Reef in October 2014. Acropora millepora samples from Davies Reef lagoon (18°30′3.96′′S, 147°22′48′′E), Rib Reef (18°28′53.4′′S, 146°52′24.96′′E), and Pandora Island (18°48′45′′S, 146°25′59.16′′E), were exposed to various stressors including pCO2, heat, bacteria, all of these, or none of these (control). This dataset lists accessions and collection information for ITS-2 rDNA amplicon data that are available at the National Center for Biotechnology Information (NCBI) under BioProject PRJNA596498. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/844431NSF Division of Ocean Sciences (NSF OCE) OCE-163579