skip to main content


Title: Microbial bioindicators of Stony Coral Tissue Loss Disease identified in corals and overlying waters using a rapid field‐based sequencing approach
Summary

Stony Coral Tissue Loss Disease (SCTLD) is a devastating disease. Since 2014, it has spread along the entire Florida Reef Tract and into the greater Caribbean. It was first detected in the United States Virgin Islands in January 2019. To more quickly identify microbial bioindicators of disease, we developed a rapid pipeline for microbiome sequencing. Over a span of 10 days we collected, processed and sequenced coral and near‐coral seawater microbiomes from diseased and apparently healthyColpophyllia natans,Montastraea cavernosa,Meandrina meandritesandOrbicella franksi. Analysis of bacterial and archaeal 16S ribosomal RNA gene sequences revealed 25 bioindicator amplicon sequence variants (ASVs) enriched in diseased corals. These bioindicator ASVs were additionally recovered in near‐coral seawater (<5 cm of coral surface), a potential reservoir for pathogens. Phylogenetic analysis of microbial bioindicators with sequences from the Coral Microbiome Database revealed thatVibrio,Arcobacter, Rhizobiaceae and Rhodobacteraceae sequences were related to disease‐associated coral bacteria and lineages novel to corals. Additionally, four ASVs (Algicola,Cohaesibacter,ThalassobiusandVibrio) were matches to microbes previously associated with SCTLD that should be targets for future research. Overall, this work suggests that a rapid sequencing framework paired with specialized databases facilitates identification of microbial disease bioindicators.

 
more » « less
Award ID(s):
1946412
NSF-PAR ID:
10379329
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Environmental Microbiology
Volume:
24
Issue:
3
ISSN:
1462-2912
Format(s):
Medium: X Size: p. 1166-1182
Size(s):
["p. 1166-1182"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    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.

     
    more » « less
  2. Abstract

    Coral diseases have increased in frequency and intensity around the tropics worldwide. However, in many cases, little is known about their etiology.Montiporawhite syndrome (MWS) is a common disease affecting the coralMontipora capitata, a major reef builder in Hawai'i. ChronicMontiporawhite syndrome (cMWS) is a slow‐moving form of the disease that affectsM. capitatathroughout the year. The effects of this chronic disease on coral immunology and microbiology are currently unknown. In this study, we use prophenoloxidase immune assays and 16S rRNA gene amplicon sequencing to characterize the microbiome and immunological response associated with cMWS. Our results show that immunological and microbiological responses are highly localized. Relative to diseased samples, apparently healthy portions of cMWS corals differed in immune activity and in the relative abundance of microbial taxa. Coral tissues with cMWS showed decreased tyrosinase‐type catecholase and tyrosinase‐type cresolase activity and increased laccase‐type activity. Catecholase and cresolase activity were negatively correlated across all tissue types with microbiome richness. The localized effect of cMWS on coral microbiology and immunology is probably an important reason for the slow progression of the disease. This local confinement may facilitate interventions that focus on localized treatments on tissue types. This study provides an important baseline to understand the interplay between the microbiome and immune system and the mechanisms used by corals to manage chronic microbial perturbations associated with white syndrome.

     
    more » « less
  3. null (Ed.)
    Corals from the northern Red Sea and Gulf of Aqaba exhibit extreme thermal tolerance. To examine the underlying gene expression dynamics, we exposed Stylophora pistillata from the Gulf of Aqaba to short-term (hours) and long-term (weeks) heat stress with peak seawater temperatures ranging from their maximum monthly mean of 27 °C (baseline) to 29.5 °C, 32 °C, and 34.5 °C. Corals were sampled at the end of the heat stress as well as after a recovery period at baseline temperature. Changes in coral host and symbiotic algal gene expression were determined via RNA-sequencing (RNA-Seq). Shifts in coral microbiome composition were detected by complementary DNA (cDNA)-based 16S ribosomal RNA (rRNA) gene sequencing. In all experiments up to 32 °C, RNA-Seq revealed fast and pervasive changes in gene expression, primarily in the coral host, followed by a return to baseline gene expression for the majority of coral (>94%) and algal (>71%) genes during recovery. At 34.5 °C, large differences in gene expression were observed with minimal recovery, high coral mortality, and a microbiome dominated by opportunistic bacteria (including Vibrio species), indicating that a lethal temperature threshold had been crossed. Our results show that the S. pistillata holobiont can mount a rapid and pervasive gene expression response contingent on the amplitude and duration of the thermal stress. We propose that the transcriptomic resilience and transcriptomic acclimation observed are key to the extraordinary thermal tolerance of this holobiont and, by inference, of other northern Red Sea coral holobionts, up to seawater temperatures of at least 32 °C, that is, 5 °C above their current maximum monthly mean. 
    more » « less
  4. Persistent bacterial presence is believed to play an important role in host adaptation to specific niches that would otherwise be unavailable, including the exclusive consumption of blood by invertebrate parasites. Nearly all blood-feeding animals examined so far host internal bacterial symbionts that aid in some essential aspect of their nutrition. Obligate blood-feeding (OBF) invertebrates exist in the oceans, yet symbiotic associations between them and beneficial bacteria have not yet been explored. This study describes the microbiome of 6 phylogenetically-diverse species of marine obligate blood-feeders, including leeches (both fish and elasmobranch specialists; e.g., Pterobdella, Ostreobdella, and Branchellion ), isopods (e.g., Elthusa and Nerocila ), and a copepod (e.g., Lernanthropus ). Amplicon sequencing analysis revealed the blood-feeding invertebrate microbiomes to be low in diversity, compared to host fish skin surfaces, seawater, and non-blood-feeding relatives, and dominated by only a few bacterial genera, including Vibrio (100% prevalence and comprising 39%–81% of the average total recovered 16S rRNA gene sequences per OBF taxa). Vibrio cells were localized to the digestive lumen in and among the blood meal for all taxa examined via fluorescence microscopy. For Elthusa and Branchellion, Vibrio cells also appeared intracellularly within possible hemocytes, suggesting an interaction with the immune system. Additionally, Vibrio cultivated from four of the obligate blood-feeding marine taxa matched the dominant amplicons recovered, and all but one was able to effectively lyse vertebrate blood cells. Bacteria from 2 additional phyla and 3 families were also regularly recovered, albeit in much lower abundances, including members of the Oceanospirillaceae, Flavobacteriacea, Porticoccaceae, and unidentified members of the gamma-and betaproteobacteria, depending on the invertebrate host. For the leech Pterobdella , the Oceanospirillaceae were also detected in the esophageal diverticula. For two crustacean taxa, Elthusa and Lernanthropus , the microbial communities associated with brooded eggs were very similar to the adults, indicating possible direct transmission. Virtually nothing is known about the influence of internal bacteria on the success of marine blood-feeders, but this evidence suggests their regular presence in marine parasites from several prominent groups. 
    more » « less
  5. Summary

    Coral‐associated microorganisms are thought to play a fundamental role in the health and ecology of corals, but understanding of specific coral–microbial interactions are lacking. In order to create a framework to examine coral–microbial specificity, we integrated and phylogenetically compared 21,100 SSU rRNA gene Sanger‐produced sequences from bacteria and archaea associated with corals from previous studies, and accompanying host, location and publication metadata, to produce the Coral Microbiome Database. From this database, we identified 39 described and candidate phyla of Bacteria and two Archaea phyla associated with corals, demonstrating that corals are one of the most phylogenetically diverse animal microbiomes. Secondly, this new phylogenetic resource shows that certain microorganisms are indeed specific to corals, including evolutionary distinct hosts. Specifically, we identified 2–37 putative monophyletic, coral‐specific sequence clusters within bacterial genera associated with the greatest number of coral species (Vibrio,EndozoicomonasandRuegeria) as well as functionally relevant microbial taxa (“CandidatusAmoebophilus”, “CandidatusNitrosopumilus” and under recognized cyanobacteria). This phylogenetic resource provides a framework for more targeted studies of corals and their specific microbial associates, which is timely given the escalated need to understand the role of the coral microbiome and its adaptability to changing ocean and reef conditions.

     
    more » « less