On the importance of the microbiome and pathobiome in coral health and disease

The term “microbiome” was first coined in 1988 and given the definition of a characteristic microbial community occupying a reasonably well defined habitat which has distinct physio-chemical properties. A more recent term has also emerged, taking this one step further and focusing on diseases in host organisms. The “pathobiome” breaks down the concept of “one pathogen = one disease” and highlights the role of the microbiome, more specifically certain members within the microbiome, in causing pathogenesis. The development of next generation sequencing has allowed large data sets to be amassed describing the microbial communities of many organisms and the field of coral biology is no exception. However, the choices made in the analytical process and the interpretation of these data can significantly affect the outcome and the overall conclusions drawn. In this review we explore the implications of these difficulties, as well as highlighting analytical tools developed in other research fields (such as network analysis) which hold substantial potential in helping to develop a deeper understanding of the role of the microbiome in disease in corals. We also make the case that standardization of methods will substantially improve the collective gain in knowledge across research groups.N/

Distinct bacterial communities associated with the coral model Aiptasia in aposymbiotic and symbiotic states with Symbiodinium.

Coral reefs are in decline. The basic functional unit of coral reefs is the coral metaorganism or holobiont consisting of the cnidarian host animal, symbiotic algae of the genus Symbiodinium, and a specific consortium of bacteria (among others), but research is slow due to the difficulty of working with corals. Aiptasia has proven to be a tractable model system to elucidate the intricacies of cnidarian-dinoflagellate symbioses, but characterization of the associated bacterial microbiome is required to provide a complete and integrated understanding of holobiont function. In this work, we characterize and analyze the microbiome of aposymbiotic and symbiotic Aiptasia and show that bacterial associates are distinct in both conditions. We further show that key microbial associates can be cultured without their cnidarian host. Our results suggest that bacteria play an important role in the symbiosis of Aiptasia with Symbiodinium, a finding that underlines the power of the Aiptasia model system where cnidarian hosts can be analyzed in aposymbiotic and symbiotic states. The characterization of the native microbiome and the ability to retrieve culturable isolates contributes to the resources available for the Aiptasia model system. This provides an opportunity to comparatively analyze cnidarian metaorganisms as collective functional holobionts and as separated member species. We hope that this will accelerate research into understanding the intricacies of coral biology, which is urgently needed to develop strategies to mitigate the effects of environmental change.This work was supported by baseline funds to CRV by King Abdullah University of Science and Technology (KAUST) and by the Center Competitive Funding (CCF) Program FCC/1/1973- 18-01

The interaction between the proliferating macroalga Asparagopsis taxiformis and the coral Astroides calycularis induces changes in microbiome and metabolomic fingerprints

Mediterranean Sea ecosystems are considered as hotspots of biological introductions, exposed to possible negative effects of non-indigenous species. In such temperate marine ecosystems, macroalgae may be dominant, with a great percentage of their diversity represented by introduced species. Their interaction with temperate indigenous benthic organisms have been poorly investigated. To provide new insights, we performed an experimental study on the interaction between the introduced proliferative red alga Asparagopsis taxiformis and the indigenous Mediterranean coral Astroides calycularis. The biological response measurements included meta-barcoding of the associated microbial communities and metabolomic fingerprinting of both species. Significant changes were detected among both associated microbial communities, the interspecific differences decreasing with stronger host interaction. No short term effects of the macroalga on the coral health, neither on its polyp activity or its metabolism, were detected. In contrast, the contact interaction with the coral induced a change in the macroalgal metabolomic fingerprint with a significant increase of its bioactivity against the marine bacteria Aliivibrio fischeri. This induction was related to the expression of bioactive metabolites located on the macroalgal surface, a phenomenon which might represent an immediate defensive response of the macroalga or an allelopathic offense against coral.ERA-NET Biome project "SEAPROLIF"; CNRS; Provence Alpes Cote d'Azur Region; TOTAL Fundation; Fundacao para a Ciencia e a Tecnologia (FCT) [Netbiome/0002/2011]; FCT fellowships [SFRH/BPD/63703/2009, SFRH/BPD/107878/2015]info:eu-repo/semantics/publishedVersio

Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides

In this study, we examine microbial communities of early developmental stages of the coral Porites astreoides by sequence analysis of cloned 16S rRNA genes, terminal restriction fragment length polymorphism (TRFLP), and fluorescence in situ hybridization (FISH) imaging. Bacteria are associated with the ectoderm layer in newly released planula larvae, in 4-day-old planulae, and on the newly forming mesenteries surrounding developing septa in juvenile polyps after settlement. Roseobacter clade-associated (RCA) bacteria and Marinobacter sp. are consistently detected in specimens of P. astreoides spanning three early developmental stages, two locations in the Caribbean and 3 years of collection. Multi-response permutation procedures analysis on the TRFLP results do not support significant variation in the bacterial communities associated with P. astreoides larvae across collection location, collection year or developmental stage. The results are the first evidence of vertical transmission (from parent to offspring) of bacteria in corals. The results also show that at least two groups of bacterial taxa, the RCA bacteria and Marinobacter, are consistently associated with juvenile P. astreoides against a complex background of microbial associations, indicating that some components of the microbial community are long-term associates of the corals and may impact host health and survival

Abrolhos Bank Reef Health Evaluated by Means of Water Quality, Microbial Diversity, Benthic Cover, and Fish Biomass Data

The health of the coral reefs of the Abrolhos Bank (southwestern Atlantic) was characterized with a holistic approach using measurements of four ecosystem components: (i) inorganic and organic nutrient concentrations, [1] fish biomass, [1] macroalgal and coral cover and (iv) microbial community composition and abundance. The possible benefits of protection from fishing were particularly evaluated by comparing sites with varying levels of protection. Two reefs within the well-enforced no-take area of the National Marine Park of Abrolhos (Parcel dos Abrolhos and California) were compared with two unprotected coastal reefs (Sebastião Gomes and Pedra de Leste) and one legally protected but poorly enforced coastal reef (the “paper park” of Timbebas Reef). The fish biomass was lower and the fleshy macroalgal cover was higher in the unprotected reefs compared with the protected areas. The unprotected and protected reefs had similar seawater chemistry. Lower vibrio CFU counts were observed in the fully protected area of California Reef. Metagenome analysis showed that the unprotected reefs had a higher abundance of archaeal and viral sequences and more bacterial pathogens, while the protected reefs had a higher abundance of genes related to photosynthesis. Similar to other reef systems in the world, there was evidence that reductions in the biomass of herbivorous fishes and the consequent increase in macroalgal cover in the Abrolhos Bank may be affecting microbial diversity and abundance. Through the integration of different types of ecological data, the present study showed that protection from fishing may lead to greater reef health. The data presented herein suggest that protected coral reefs have higher microbial diversity, with the most degraded reef (Sebastião Gomes) showing a marked reduction in microbial species richness. It is concluded that ecological conditions in unprotected reefs may promote the growth and rapid evolution of opportunistic microbial pathogens

Microbial Friends And Foes: Characterizing The Cnidarian Response To Pathogenic And Mutualistic Microorganisms

The ecology and evolution of cnidarians is driven by symbiotic and pathogenic hostmicrobe relationships. Research regarding these relationships is especially timely given the recent decline of coral reef ecosystems, in part due to disruptions in cnidarian-microbe interactions. My dissertation is an experimental analysis of how cnidarians respond to both harmful and beneficial microorganisms and explores the interplay between these two types of interactions. Corals provide a multifaceted habitat that supports a rich bacterial assemblage, and in Chapter 1, I review our current knowledge regarding the diversity, specificity, development, and functions of these assemblages. With a meta-analysis of previous work, I quantitatively analyze what is known regarding the relationship between coral-associated microorganisms and disease. Finally, I examine evidence that these populations could be disrupted by climatic change. One of the most well-known mutualistic relationships is that between cnidarians and unicellular dinoflagellates. To evaluate the molecular mechanisms that underlie the persistence of this relationship, in Chapter 2, I identify differentially expressed transcripts between symbiotic and aposymbiotic individuals of the model sea anemone, Aiptasia pallida. These transcripts include those with potential functions in several metabolic pathways, transport of nutrients between the partners, and host tolerance of the dinoflagellate. To broaden our understanding of the cnidarian response to pathogenic microbes, in Chapter 3, I report the host transcriptome response of aposymbiotic Aiptasia to experimental inoculation with Serratia marcescens. My results suggest that Aiptasia responds to bacterial challenge via the regulation of tumor necrosis factor receptor-associated factor-mediated signaling, apoptosis, and ubiquitination, thus suggesting that lower metazoans respond to immune challenge via highly conserved mechanisms. To determine how the Aiptasia immune response is modulated via the presence of dinoflagellate symbionts, in Chapter 4, I compared gene expression and behavioral assays of S. marcescens-exposed anemones with and without their symbionts. The presence of dinoflagellates greatly alters the number and type of genes expressed in response to bacterial challenge. In addition, symbiotic anemones were less likely to recover from pathogen exposure and had lower survival rates than their aposymbiotic counterparts. These results are consistent with the hypothesis that symbiotic dinoflagellates suppress Aiptasia immunity, perhaps to promote symbiotic homeostasis