Modeling of the Coral Microbiome: the Influence of Temperature and Microbial Network

Lima, Laís Farias Oliveira; Weissman, Maya; Reed, Micheal; Papudeshi, Bhavya; Alker, Amanda T.; Morris, Megan M.; Edwards, Robert A.; Putron, Samantha J. de; Vaidya, Naveen K.; Dinsdale, Elizabeth A.

doi:10.1128/mbio.02691-19

Cited by 57 publications

(84 citation statements)

References 110 publications

(67 reference statements)

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“…The overall lower correlation may be attributable to site-speci c bacterial community composition differences. Corals from the GoA, however, exhibited a low correlation between replicate colonies at 30° and 33 °C that increased considerably at 36 °C, due to the substantial relative increase of Vibrionaceae and Rhodobacteraceae, driving the similarity between samples and indicating dysbiosis/loss of microbiome structure, as alluded earlier (Sweet and Bulling 2017;Boilard et al 2020;Lima et al 2020). Thus, the decreasing correlation coe cient(s) with increasing temperature observed in GoA corals is that of a population approaching a tipping point with subsequent systemic collapse: GoA corals ramp up their response to the increasing stressor until they reach a tipping point upon which the system collapses.…”

Section: Signatures Of Thermal Tolerance Across Regions and Coral Holmentioning

confidence: 78%

Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance

Voolstra

Valenzuela²,

Turkarslan³

et al. 2020

Preprint

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Corals from the northern Red Sea, in particular the Gulf of Aqaba (GoA), have exceptionally high bleaching thresholds approaching >5°C above their maximum monthly mean (MMM) temperatures. These elevated thresholds are thought to be due to historical selection, as corals passed through the warmer Southern Red Sea during re-colonization from the Arabian Sea. To test this hypothesis, we determined thermal tolerance thresholds of GoA versus Central Red Sea (CRS) Stylophora pistillata corals using the Coral Bleaching Automated Stress System (CBASS) to run a series of standardized acute thermal stress assays. Relative thermal thresholds of GoA and CRS corals were indeed similar and exceptionally high (~7°C above MMM). However, absolute thermal thresholds of CRS corals were on average 3°C above those of GoA corals. To explore the mechanistic underpinnings, we determined gene expression response and microbiome dynamics of coral holobiont compartments. Transcriptomic responses differed markedly, with a strong response to the thermal stress in GoA corals versus a remarkably muted response in corals from the CRS. This pattern was recapitulated in the algal symbionts that showed site-specific genetic differentiation. Concomitant to this, a subset of coral and algal genes showed temperature-induced expression in GoA corals, while exhibiting fixed high expression, i.e. front-loading, in CRS corals. Bacterial community composition of GoA corals changed dramatically under heat stress, whereas CRS corals displayed consistent assemblages, indicating distinct microbial response patterns. Our work demonstrates distinct patterns underlying thermal tolerance across spatial scales, even for the same species and ocean basin. We interpret the response of GoA corals as that of a resilient population approaching a tipping point in contrast to a pattern of consistently elevated thermal resistance in CRS corals that cannot further attune. Such response differences suggest distinct thermal tolerance mechanisms that affect the response of coral populations to ocean warming.

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Section: Signatures Of Thermal Tolerance Across Regions and Coral Holmentioning

confidence: 78%

Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance

Voolstra

Valenzuela²,

Turkarslan³

et al. 2020

Preprint

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“…Heat-stressed corals preferentially fed on Synechococcus to access the high nitrogen content in their cells and to compensate for the loss of nitrogen from algal endosymbiont Symbiodiniaceae during recovery from bleaching (71). The inner lagoon patch reefs in Bermuda are exposed to greater environmental fluctuations, particularly changes in temperature (45)(46)(47)51). Therefore, the high abundance of Synechococcus in the water column and in the SML of P. strigosa could be contributing to the energy transfer from pelagic to benthic trophic levels, and to the coral thermal tolerance in the inner lagoon reefs of Bermuda.…”

Section: The Coral Sml Microbiome From a Fluctuating Environment Provides More Services Related To Nutrient Cycling Stress Tolerance And mentioning

confidence: 99%

“…We selected P. strigosa as the coral host species because it is widely distributed across the Bermuda platform. The reef zones sampled were approximately 8 km apart (51) and P. strigosa is a broadcast spawner; therefore, there is a high likelihood that gene flow between the coral hosts colonizing inner and outer reefs is maintained and that the host genetics is not structured into different populations. Indeed, studies on other species have indicated high genetic exchange among reef sites in Bermuda (52,53).…”

Section: Introductionmentioning

confidence: 99%

“…Therefore, we selected this period to capture a potential long-term acclimatization of the coral holobiont to their reef zones, and not their immediate response to acute temperature fluctuations. Each reef zone was replicated across three reef sites (51). The SML of P. strigosa was collected from six colonies (diameter, 10 to 15 cm) from the inner and outer reef zones (n = 12 colonies total) using a two-way 50-ml syringe filled with 0.02-µmfiltered seawater (51).…”

Section: Introductionmentioning

confidence: 99%

“…Each reef zone was replicated across three reef sites (51). The SML of P. strigosa was collected from six colonies (diameter, 10 to 15 cm) from the inner and outer reef zones (n = 12 colonies total) using a two-way 50-ml syringe filled with 0.02-µmfiltered seawater (51). We collected 200 ml of coral mucus diluted in sterile seawater (four syringes applied to different parts of the colony's surface) per colony to increase DNA concentration per sample.…”

Section: Introductionmentioning

confidence: 99%

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Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale

Lima

Alker

Papudeshi

et al. 2021

Preprint

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Background The coral holobiont is comprised of a highly diverse microbial community that provides key services to corals such as protection against pathogens and nutrient cycling. The coral surface mucus layer (SML) microbiome is very sensitive to external changes and tied to ecosystem functioning, as it constitutes the direct interface between the coral host and the environment. The functional profile of microbial genes in the coral SML is underexplored and the use of shotgun metagenomics is relatively rare among coral microbiome studies. Here we investigate whether the bacterial taxonomic and functional profiles in the coral SML are shaped by the local reef zone and explore their role in coral health and ecosystem functioning. Results The analysis was conducted using metagenomes and metagenome assemble genomes (MAGs) associated with the coral Pseudodiploria strigosa and the water column from two naturally distinct reef environments in Bermuda: inner patch reefs exposed to a fluctuating thermal regime and the more stable outer reefs . Our results showed that the microbial community structure is simultaneously selected by the host medium (i.e., coral SML versus water) and the local environment (i.e., inner reefs versus outer reefs), both at taxonomic and functional levels. The coral SML microbiome from inner reefs provides more gene functions that are involved in nutrient cycling (e.g., photosynthesis, phosphorus metabolism, sulfur assimilation) and that are related to higher levels of microbial activity, competition, and stress response, such as dimethylsulfoniopropionate (DMSP) breakdown. In contrast, the coral SML microbiome from outer reefs contained genes indicative of a carbohydrate-rich mucus composition found in corals exposed to less stressful temperatures and showed high proportions of microbial gene functions that play a potential role in coral disease, such as degradation of lignin-derived compounds and sulfur oxidation. Conclusion The fluctuating environment in the inner patch reefs of Bermuda could be driving a more beneficial coral SML microbiome; potentially increasing holobiont resilience to environmental changes and disease. Our results reveal microbial taxa and functions selected at reef scale in the coral SML microbiome that can leverage disease management, microbiome engineering, and microbial eco-evolutionary theories.

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Physiological and microbiome adaptation of coral Turbinaria peltata in response to marine heatwaves

Zhai,

Zhang,

Zhou

et al. 2024

Ecology and Evolution

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Against the backdrop of global warming, marine heatwaves are projected to become increasingly intense and frequent. This trend poses a potential threat to the survival of corals and the maintenance of entire coral reef ecosystems. Despite extensive evidence for the resilience of corals to heat stress, their ability to withstand repeated heatwave events has not been determined. In this study, we examined the responses and resilience of Turbinaria peltata to repeated exposure to marine heatwaves, with a focus on physiological parameters and symbiotic microorganisms. In the first heatwave, from a physiological perspective, T. peltata showed decreases in the Chl a content and endosymbiont density and significant increases in GST, caspase‐3, CAT, and SOD levels (p < .05), while the effects of repeated exposure on heatwaves were weaker than those of the initial exposure. In terms of bacteria, the abundance of Leptospira, with the potential for pathogenicity and intracellular parasitism, increased significantly during the initial exposure. Beneficial bacteria, such as Achromobacter arsenitoxydans and Halomonas desiderata increased significantly during re‐exposure to the heatwave. Overall, these results indicate that T. peltata might adapt to marine heatwaves through physiological regulation and microbial community alterations.

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Modeling of the Coral Microbiome: the Influence of Temperature and Microbial Network

Cited by 57 publications

References 110 publications

Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance

Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance

Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale

Physiological and microbiome adaptation of coral Turbinaria peltata in response to marine heatwaves

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