An official website of the United States government
Abstract Coral reefs are in global decline with coral diseases playing a significant role. This is especially true for Acroporid corals that represent ~25% of all Pacific coral species and generate much of the topographic complexity supporting reef biodiversity. Coral diseases are commonly sediment-associated and could be exacerbated by overharvest of sea cucumber detritivores that clean reef sediments and may suppress microbial pathogens as they feed. Here we show, via field manipulations in both French Polynesia and Palmyra Atoll, that historically overharvested sea cucumbers strongly suppress disease among corals in contact with benthic sediments. Sea cucumber removal increased tissue mortality ofAcropora pulchraby ~370% and colony mortality by ~1500%. Additionally, farmerfish that killAcropora pulchrabases to culture their algal gardens further suppress disease by separating corals from contact with the disease-causing sediment—functioning as mutualists rather than parasites despite killing coral bases. Historic overharvesting of sea cucumbers increases coral disease and threatens the persistence of tropical reefs. Enhancing sea cucumbers may enhance reef resilience by suppressing disease.
more »
« less
This content will become publicly available on May 3, 2026
Sea cucumber grazing linked to enrichment of anaerobic microbial metabolisms in coral reef sediments
Abstract Sea cucumbers have been overharvested world-wide, making assessments of their ecological effects challenging, but recent research demonstrated that sea cucumbers increase coral survival via disease suppression and were therefore important for facilitating reef health. The mechanisms underpinning the sea cucumber-coral interaction therefore are not well understood but are likely mediated through sea cucumber grazing of microbes from reef sediments. We explored how sea cucumber grazing alters the sediment microbiome by leveraging a healthy sea cucumber population on a reef in French Polynesia. We used quantitative PCR, 16S rRNA gene sequencing, and shotgun metagenomics to compare the sediment microbiome in cages placed in situ with or without sea cucumbers. We hypothesized that grazing would lower microbial biomass, change sediment microbiome composition, and deplete sediment metagenomes of anaerobic metabolisms, likely due to aeration of the sediments. Sea cucumber grazing resulted in a 75% reduction in 16S rRNA gene abundances and reshaped microbiome composition, causing a significant decrease of cyanobacteria and other phototrophs relative to ungrazed sediments. Grazing also resulted in a depletion of genes associated with cyanotoxin synthesis, suggesting a potential link to coral health. In contrast to expectations, grazed sediment metagenomes were enriched with marker genes of diverse anaerobic or microaerophilic metabolisms, including those encoding high oxygen affinity cytochrome oxidases. This enrichment differs from patterns linked to other bioturbating invertebrates. We hypothesize that grazing enriches anaerobic processes in sediment microbiomes through removal of oxygen-producing autotrophs, fecal deposition of sea cucumber gut-associated anaerobes, or modification of sediment diffusibility. These results suggest that sea cucumber harvesting influences biogeochemical processes in reef sediments, potentially mediating coral survival by altering the sediment microbiome and its production of coral-influencing metabolites.
more »
« less
- Award ID(s):
- 1947522
- PAR ID:
- 10596410
- Publisher / Repository:
- The ISME journal
- Date Published:
- Journal Name:
- The ISME Journal
- ISSN:
- 1751-7362
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
ABSTRACT Marine sediments harbour diverse microbial populations, but with increasing depth, these microbes are thought to have low activity due to depleted electron acceptors and lack of new organic matter after burial. However, physiochemical changes in environmental parameters could impact the metabolic activity of microbes in marine sediments. We performed seasonal sampling of shallow sediments to examine changes in population and abundance in relation to physiochemical changes over the year. We used amplicon sequencing, quantitative PCR and geochemistry to assess seasonal abundance of microbial populations at 3 depths (12–14, 38–40 and 48–50 cm) in shallow coastal sediments. 16S rRNA amplicon sequencing showed the sediment microbiome consists of common sediment taxa with minor seasonal variation. However, bacterial gene counts of 16S rRNA genes were highest in summer (2.50 × 1012 genes/g of sediment) and lowest in spring (1.64 × 1011 genes/g sediment). We observed differences in sediment temperature at depth across seasons (Summer 28°C–25.5°C; Winter 8.7°C–6.3°C) and correlated changes in dissolved organic matter composition that are not typically reported for this environment. We conclude deeper microbial populations in shallow sediments may experience seasonal abundance shifts resulting in a more variable subsurface community than initially presumed in the literature.more » « less
-
Biddle, Jennifer F. (Ed.)ABSTRACT Global climate change impacts marine ecosystems through rising surface temperatures, ocean acidification, and deoxygenation. While the response of the coral holobiont to the first two effects has been relatively well studied, less is known about the response of the coral microbiome to deoxygenation. In this study, we investigated the response of the microbiome to hypoxia in two coral species that differ in their tolerance to hypoxia. We conductedin situoxygen manipulations on a coral reef in Bahía Almirante on the Caribbean coast of Panama, which has previously experienced documented episodes of hypoxia. Naïve coral colonies (previously unexposed to hypoxia) ofSiderastrea sidereaandAgaricia lamarckiwere transplanted to a reef and either enclosed in chambers that created hypoxic conditions or left at ambient oxygen levels. We collected samples of surface mucus and tissue after 48 hours of exposure and characterized the microbiome by sequencing 16S rRNA genes. We found that the microbiomes of the two coral species were distinct from one another and remained so after exhibiting similar shifts in microbiome composition in response to hypoxia. There was an increase in both abundance and number of taxa of anaerobic microbes after exposure to hypoxia. Some of these taxa may play beneficial roles in the coral holobiont by detoxifying the surrounding environment during hypoxic stress or may represent opportunists exploiting host stress. This work describes the first characterization of the coral microbiome under hypoxia and is an initial step toward identifying potential beneficial bacteria for corals facing this environmental stressor. IMPORTANCEMarine hypoxia is a threat for corals but has remained understudied in tropical regions where coral reefs are abundant. Though microbial symbioses can alleviate the effects of ecological stress, we do not yet understand the taxonomic or functional response of the coral microbiome to hypoxia. In this study, we experimentally lowered oxygen levels aroundSiderastrea sidereaandAgaricia lamarckicoloniesin situto observe changes in the coral microbiome in response to deoxygenation. Our results show that hypoxia triggers a stochastic change of the microbiome overall, with some bacterial families changing deterministically after just 48 hours of exposure. These families represent an increase in anaerobic and opportunistic taxa in the microbiomes of both coral species. Thus, marine deoxygenation destabilizes the coral microbiome and increases bacterial opportunism. This work provides novel and fundamental knowledge of the microbial response in coral during hypoxia and may provide insight into holobiont function during stress.more » « less
-
The microbiomes of tropical corals are actively studied using 16S rRNA gene amplicons to understand microbial roles in coral health, metabolism, and disease resistance. However, due to the prokaryotic origins of mitochondria, primers targeting bacterial and archaeal 16S rRNA genes may also amplify homologous 12S mitochondrial rRNA genes from the host coral, associated microbial eukaryotes, and encrusting organisms. Standard microbial bioinformatics pipelines attempt to identify and remove these sequences by comparing them to reference taxonomies. However, commonly used tools have severely under-annotated mitochondrial sequences in 1440 coral microbiomes from the Global Coral Microbiome Project, preventing annotation of over 95% of reads in some samples. This issue persists when using Greengenes or SILVA prokaryotic reference taxonomies, and in other hosts, including 16S studies of vertebrates, and of marine sponges. Worse, mitochondrial under-annotation varies between coral families and across coral compartments, biasing comparisons of - and -diversity. By supplementing existing reference taxonomies with over 3000 animal mitochondrial rRNA gene sequences, we resolved roughly 97% of unique unclassified sequences as mitochondrial. These additional sequences did not cause a false elevation in mitochondrial annotations in mock communities with known compositions. We recommend using these extended taxonomies for coral microbiome analysis and whenever eukaryotic contamination may be a concern.more » « less
-
The microbiomes of tropical corals are actively studied using 16S rRNA gene amplicons to understand microbial roles in coral health, metabolism, and disease resistance. However, primers targeting bacterial and archaeal 16S rRNA genes may also amplify organelle rRNA genes from the coral, associated microbial eukaryotes, and encrusting organisms. In this manuscript, we demonstrate that standard workflows for annotating microbial taxonomy severely under-annotate mitochondrial sequences in 1272 coral microbiomes from the Earth Microbiome Project. This issue prevents annotation of >95% of reads in some samples and persists when using either Greengenes or SILVA taxonomies. Worse, mitochondrial under-annotation varies between species and across anatomy, biasing comparisons of α- and β-diversity. By supplementing existing taxonomies with diverse mitochondrial rRNA sequences, we resolve ~97% of unique unclassified sequences as mitochondrial, without increasing misannotation in mock communities. We recommend using these extended taxonomies for coral microbiome analysis and encourage vigilance regarding similar issues in other hosts.more » « less
