skip to main content

Explore Research Products in the NSF-PAR

  • NSF Public Access
  • Search Results
  • Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata

This content will become publicly available on May 25, 2024

Title: Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata
Reef-building corals contain a complex consortium of organisms, a holobiont, which responds dynamically to disease, making pathogen identification difficult. While coral transcriptomics and microbiome communities have previously been characterized, similarities and differences in their responses to different pathogenic sources has not yet been assessed. In this study, we inoculated four genets of the Caribbean branching coral Acropora palmata with a known coral pathogen ( Serratia marcescens ) and white band disease. We then characterized the coral’s transcriptomic and prokaryotic microbiomes’ (prokaryiome) responses to the disease inoculations, as well as how these responses were affected by a short-term heat stress prior to disease inoculation. We found strong commonality in both the transcriptomic and prokaryiomes responses, regardless of disease inoculation. Differences, however, were observed between inoculated corals that either remained healthy or developed active disease signs. Transcriptomic co-expression analysis identified that corals inoculated with disease increased gene expression of immune, wound healing, and fatty acid metabolic processes. Co-abundance analysis of the prokaryiome identified sets of both healthy-and-disease-state bacteria, while co-expression analysis of the prokaryiomes’ inferred metagenomic function revealed infected corals’ prokaryiomes shifted from free-living to biofilm states, as well as increasing metabolic processes. The short-term heat stress did not increase disease susceptibility for any of the four genets with any of the disease inoculations, and there was only a weak effect captured in the coral hosts’ transcriptomic and prokaryiomes response. Genet identity, however, was a major driver of the transcriptomic variance, primarily due to differences in baseline immune gene expression. Despite genotypic differences in baseline gene expression, we have identified a common response for components of the coral holobiont to different disease inoculations. This work has identified genes and prokaryiome members that can be focused on for future coral disease work, specifically, putative disease diagnostic tools.  more » « less
Award ID(s):
1951826
NSF-PAR ID:
10443641
Author(s) / Creator(s):
; ; ; ; ; ; ;
Editor(s):
Mapder, Tarunendu
Date Published:
Journal Name:
PLOS ONE
Volume:
18
Issue:
5
ISSN:
1932-6203
Page Range / eLocation ID:
e0286293
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ; ; ( , Proceedings of the National Academy of Sciences)
    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
  2. ; ; ( , Molecular Ecology)
    Abstract

    The mechanisms resulting in the breakdown of the coral symbiosis once the process of bleaching has been initiated remain unclear. Distinguishing the process of symbiont loss from the thermal stress response may shed light on the cellular and molecular pathways involved in each process. This study examined physiological changes and global gene expression patterns associated with white patch syndrome (WPS) inPorites lobata, which manifests in localized bleaching independent of thermal stress. In addition, a meta‐analysis of global gene expression studies in other corals and anemones was used to contrast differential regulation as a result of disease and thermal stress from patterns correlated with symbiotic state. Symbiont density, chlorophyllacontent, holobiont productivity, instant calcification rate, and total host protein content were uniformly reduced in WPS relative to healthy tissue. While expression patterns associated with WPS were secondary to fixed effects of source colony, specific functional enrichments combined with a lack of immune regulation suggest that the viral infection putatively giving rise to this condition affects symbiont rather than host cells. Expression in response to WPS also clustered independently of patterns in white syndrome impactedA. hyacinthus, further supporting a distinct aetiology of this syndrome. Expression patterns in WPS‐affected tissues were significantly correlated with prior studies that examined short‐term thermal stress responses independent of symbiotic state, suggesting that the majority of expression changes reflect a nonspecific stress response. Across studies, the magnitude and direction of expression change among particular functional enrichments suggests unique responses to stressor duration and highlights distinct responses to bleaching in an anemone model.

     
    more » « less
  3. ; ( , Molecular Ecology)
    Abstract

    Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations to boost the abundance of these symbionts in corals may increase resilience in warming oceans. However, the thermotolerant symbiontDurusdinium trenchiimay reduce growth and fecundity in Caribbean corals, and these tradeoffs need to be better understood as this symbiont spreads through the region. We sought to understand howD. trenchiimodulates coral gene expression by manipulating symbiont communities inMontastraea cavernosato produce replicate ramets containingD. trenchiitogether with paired ramets of these same genets (n = 3) containingCladocopiumC3 symbionts. We then examined differences in global gene expression between corals hostingDurusdiniumandCladocopiumunder control temperatures, and in response to short‐term heat stress. We identified numerous transcriptional differences associated with symbiont identity, which explained 2%–14% of the transcriptional variance. Corals withD. trenchiiupregulated genes related to translation, ribosomal structure and biogenesis, and downregulated genes related to extracellular structures, and carbohydrate and lipid transport and metabolism, relative to corals withCladocopium. Unexpectedly, these changes were similar to those observed inCladocopium‐dominated corals in response to heat stress, suggesting that thermotolerantD. trenchiimay cause corals to increase expression of heat stress‐responsive genes, explaining both the increased heat tolerance and the associated energetic tradeoffs in corals containingD. trenchii. These findings provide insight into the ecological changes occurring on contemporary coral reefs in response to climate change, and the diverse ways in which different symbionts modulate emergent phenotypes of their hosts.

     
    more » « less
  4. ; ; ; ; ; ( , Molecular Ecology)
    Abstract

    Coral reefs are experiencing unprecedented declines in health on a global scale leading to severe reductions in coral cover. One major cause of this decline is increasing sea surface temperature. However, conspecific colonies separated by even small spatial distances appear to show varying responses to this global stressor. One factor contributing to differential responses to heat stress is variability in the coral's micro‐environment, such as the amount of water flow a coral experiences. High flow provides corals with a variety of health benefits, including heat stress mitigation. Here, we investigate how water flow affects coral gene expression and provides resilience to increasing temperatures. We examined host and photosymbiont gene expression ofAcroporacf.pulchracolonies in discrete in situ flow environments during a natural bleaching event. In addition, we conducted controlled ex situ tank experiments where we exposedA. cf.pulchrato different flow regimes and acute heat stress. Notably, we observed distinct flow‐driven transcriptomic signatures related to energy expenditure, growth, heterotrophy and a healthy coral host–photosymbiont relationship. We also observed disparate transcriptomic responses during bleaching recovery between the high‐ and low‐flow sites. Additionally, corals exposed to high flow showed “frontloading” of specific heat‐stress‐related genes such as heat shock proteins, antioxidant enzymes, genes involved in apoptosis regulation, innate immunity and cell adhesion. We posit that frontloading is a result of increased oxidative metabolism generated by the increased water movement. Gene frontloading may at least partially explain the observation that colonies in high‐flow environments show higher survival and/or faster recovery in response to bleaching events.

     
    more » « less
  5. ; ( , Scientific Reports)
    Abstract Symbiosis with unicellular algae in the family Symbiodiniaceae is common across tropical marine invertebrates. Reef-building corals offer a clear example of cellular dysfunction leading to a dysbiosis that disrupts entire ecosystems in a process termed coral bleaching. Due to their obligate symbiotic relationship, understanding the molecular underpinnings that sustain this symbiosis in tropical reef-building corals is challenging, as any aposymbiotic state is inherently coupled with severe physiological stress. Here, we leverage the subtropical, facultatively symbiotic and calcifying coral Oculina arbuscula to investigate gene expression differences between aposymbiotic and symbiotic branches within the same colonies under baseline conditions. We further compare gene ontology (GO) and KOG enrichment in gene expression patterns from O. arbuscula with prior work in the sea anemone Exaiptasia pallida (Aiptasia) and the salamander Ambystoma maculatum —both of which exhibit endophotosymbiosis with unicellular algae. We identify nitrogen cycling, cell cycle control, and immune responses as key pathways involved in the maintenance of symbiosis under baseline conditions. Understanding the mechanisms that sustain a healthy symbiosis between corals and Symbiodiniaceae algae is of urgent importance given the vulnerability of these partnerships to changing environmental conditions and their role in the continued functioning of critical and highly diverse marine ecosystems. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email