Disentangling causation: complex roles of coral‐associated microorganisms in disease

Mera, Hanaka; Bourne, David G.

doi:10.1111/1462-2920.13958

Cited by 64 publications

(58 citation statements)

References 232 publications

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“…However, in both cases, the sponge-associated microbiota shifted from a specific- to a generalist-dominated community in the unhealthy individuals. These findings indicate that, similar to corals [ 207 , 208 ], sponge diseases appear to start with an imbalance of the holobiont which is then followed by opportunistic or polymicrobial infections.…”

Section: Holobiont Responses: Stress Dysbiosis and Acclimatizationmentioning

confidence: 76%

The sponge holobiont in a changing ocean: from microbes to ecosystems

et al. 2018

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The recognition that all macroorganisms live in symbiotic association with microbial communities has opened up a new field in biology. Animals, plants, and algae are now considered holobionts, complex ecosystems consisting of the host, the microbiota, and the interactions among them. Accordingly, ecological concepts can be applied to understand the host-derived and microbial processes that govern the dynamics of the interactive networks within the holobiont. In marine systems, holobionts are further integrated into larger and more complex communities and ecosystems, a concept referred to as “nested ecosystems.” In this review, we discuss the concept of holobionts as dynamic ecosystems that interact at multiple scales and respond to environmental change. We focus on the symbiosis of sponges with their microbial communities—a symbiosis that has resulted in one of the most diverse and complex holobionts in the marine environment. In recent years, the field of sponge microbiology has remarkably advanced in terms of curated databases, standardized protocols, and information on the functions of the microbiota. Like a Russian doll, these microbial processes are translated into sponge holobiont functions that impact the surrounding ecosystem. For example, the sponge-associated microbial metabolisms, fueled by the high filtering capacity of the sponge host, substantially affect the biogeochemical cycling of key nutrients like carbon, nitrogen, and phosphorous. Since sponge holobionts are increasingly threatened by anthropogenic stressors that jeopardize the stability of the holobiont ecosystem, we discuss the link between environmental perturbations, dysbiosis, and sponge diseases. Experimental studies suggest that the microbial community composition is tightly linked to holobiont health, but whether dysbiosis is a cause or a consequence of holobiont collapse remains unresolved. Moreover, the potential role of the microbiome in mediating the capacity for holobionts to acclimate and adapt to environmental change is unknown. Future studies should aim to identify the mechanisms underlying holobiont dynamics at multiple scales, from the microbiome to the ecosystem, and develop management strategies to preserve the key functions provided by the sponge holobiont in our present and future oceans.

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Section: Holobiont Responses: Stress Dysbiosis and Acclimatizationmentioning

confidence: 76%

The sponge holobiont in a changing ocean: from microbes to ecosystems

et al. 2018

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“…Several studies have identified Vibrio spp. (⋎-Proteobacteria ) as causative agents of coral bleaching for multiple coral species and in multiple locations (Ushijima et al, 2014 ; reviewed in Mera and Bourne, 2018 ). Vibrio coralliilyticus ( V. coralliilyticus ) has emeregd as an important bacterial pathogen model for understanding the establishement and propagation of coral disease (Sussman et al, 2008 ; O'Santos et al, 2011 ; Garren et al, 2014 ; Pollock et al, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

Therapeutic Potential of a New Jumbo Phage That Infects Vibrio coralliilyticus, a Widespread Coral Pathogen

et al. 2018

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Biological control using bacteriophages is a promising approach for mitigating the devastating effects of coral diseases. Several phages that infect Vibrio coralliilyticus, a widespread coral pathogen, have been isolated, suggesting that this bacterium is permissive to viral infection and is, therefore, a suitable candidate for treatment by phage therapy. In this study, we combined functional and genomic approaches to evaluate the therapeutic potential of BONAISHI, a novel V. coralliilyticus phage, which was isolated from the coral reef in Van Phong Bay (Vietnam). BONAISHI appears to be strictly lytic for several pathogenic strains of V. coralliilyticus and remains infectious over a broad range of environmental conditions. This candidate has an unusually large dsDNA genome (303 kb), with no genes that encode known toxins or implicated in lysogeny control. We identified several proteins involved in host lysis, which may offer an interesting alternative to the use of whole bacteriophages for controlling V. coralliilyticus. A preliminary therapy test showed that adding BONAISHI to an infected culture of Symbiodinium sp. cells reduced the impact of V. coralliilyticus on Symbiodinium sp. photosynthetic activity. This study showed that BONAISHI is able to mitigate V. coralliilyticus infections, making it a good candidate for phage therapy for coral disease.

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“…Understanding coral disease causation remains challenging as complex interactions exist between causative agents, environment and host 1 , 15 . External factors such as infectious or opportunistic pathogens and environmental stressors may affect a compromised coral holobiont, potentially triggering diseases 15 . In particular, complex interactions have been identified within coral microbial communities driving disease processes 16 .…”

Section: Introductionmentioning

confidence: 99%

Local confinement of disease-related microbiome facilitates recovery of gorgonian sea fans from necrotic-patch disease

Quintanilla

Ramírez‐Portilla

Adu-Oppong

et al. 2018

Sci Rep

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Microbiome disruptions triggering disease outbreaks are increasingly threatening corals worldwide. In the Tropical Eastern Pacific, a necrotic-patch disease affecting gorgonian corals (sea fans, Pacifigorgia spp.) has been observed in recent years. However, the composition of the microbiome and its disease-related disruptions remain unknown in these gorgonian corals. Therefore, we analysed 16S rRNA gene amplicons from tissues of healthy colonies (n = 19) and from symptomatic-asymptomatic tissues of diseased colonies (n = 19) of Pacifigorgia cairnsi (Gorgoniidae: Octocorallia) in order to test for disease-related changes in the bacterial microbiome. We found that potential endosymbionts (mostly Endozoicomonas spp.) dominate the core microbiome in healthy colonies. Moreover, healthy tissues differed in community composition and functional profile from those of the symptomatic tissues but did not show differences to asymptomatic tissues of the diseased colonies. A more diverse set of bacteria was observed in symptomatic tissues, together with the decline in abundance of the potential endosymbionts from the healthy core microbiome. Furthermore, according to a comparative taxonomy-based functional profiling, these symptomatic tissues were characterized by the increase in heterotrophic, ammonia oxidizer and dehalogenating bacteria and by the depletion of nitrite and sulphate reducers. Overall, our results suggest that the bacterial microbiome associated with the disease behaves opportunistically and is likely in a state of microbial dysbiosis. We also conclude that the confinement of the disease-related consortium to symptomatic tissues may facilitate colony recovery.

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Disentangling causation: complex roles of coral‐associated microorganisms in disease

Cited by 64 publications

References 232 publications

The sponge holobiont in a changing ocean: from microbes to ecosystems

The sponge holobiont in a changing ocean: from microbes to ecosystems

Therapeutic Potential of a New Jumbo Phage That Infects Vibrio coralliilyticus, a Widespread Coral Pathogen

Local confinement of disease-related microbiome facilitates recovery of gorgonian sea fans from necrotic-patch disease

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