Title: Modeling of the Coral Microbiome: the Influence of Temperature and Microbial Network
ABSTRACT Host-associated microbial communities are shaped by extrinsic and intrinsic factors to the holobiont organism. Environmental factors and microbe-microbe interactions act simultaneously on the microbial community structure, making the microbiome dynamics challenging to predict. The coral microbiome is essential to the health of coral reefs and sensitive to environmental changes. Here, we develop a dynamic model to determine the microbial community structure associated with the surface mucus layer (SML) of corals using temperature as an extrinsic factor and microbial network as an intrinsic factor. The model was validated by comparing the predicted relative abundances of microbial taxa to the relative abundances of microbial taxa from the sample data. The SML microbiome from Pseudodiploria strigosa was collected across reef zones in Bermuda, where inner and outer reefs are exposed to distinct thermal profiles. A shotgun metagenomics approach was used to describe the taxonomic composition and the microbial network of the coral SML microbiome. By simulating the annual temperature fluctuations at each reef zone, the model output is statistically identical to the observed data. The model was further applied to six scenarios that combined different profiles of temperature and microbial network to investigate the influence of each of these two factors on the model accuracy. The SML microbiome was best predicted by model scenarios with the temperature profile that was closest to the local thermal environment, regardless of the microbial network profile. Our model shows that the SML microbiome of P. strigosa in Bermuda is primarily structured by seasonal fluctuations in temperature at a reef scale, while the microbial network is a secondary driver. IMPORTANCE Coral microbiome dysbiosis (i.e., shifts in the microbial community structure or complete loss of microbial symbionts) caused by environmental changes is a key player in the decline of coral health worldwide. Multiple factors in the water column and the surrounding biological community influence the dynamics of the coral microbiome. However, by including only temperature as an external factor, our model proved to be successful in describing the microbial community associated with the surface mucus layer (SML) of the coral P. strigosa . The dynamic model developed and validated in this study is a potential tool to predict the coral microbiome under different temperature conditions. more »« less
Howard, Rachel D.; Schul, Monica D.; Rodriguez Bravo, Lucia M.; Altieri, Andrew H.; Meyer, Julie L.(
, Applied and Environmental Microbiology)
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.
IMPORTANCE
Marine 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.
In coral reefs and adjacent seagrass meadow and mangrove environments, short temporal scales (i.e. tidal, diurnal) may have important influences on ecosystem processes and community structure, but these scales are rarely investigated. This study examines how tidal and diurnal forcings influence pelagic microorganisms and nutrient dynamics in 3 important and adjacent coastal biomes: mangroves, coral reefs, and seagrass meadows. We sampled for microbial ( Bacteria and Archaea ) community composition, cell abundances and environmental parameters at 9 coastal sites on St. John, US Virgin Islands that spanned 4 km in distance (4 coral reefs, 2 seagrass meadows and 3 mangrove locations within 2 larger bays). Eight samplings occurred over a 48 h period, capturing day and night microbial dynamics over 2 tidal cycles. The seagrass and reef biomes exhibited relatively consistent environmental conditions and microbial community structure but were dominated by shifts in picocyanobacterial abundances that were most likely attributed to diel dynamics. In contrast, mangrove ecosystems exhibited substantial daily shifts in environmental parameters, heterotrophic cell abundances and microbial community structure that were consistent with the tidal cycle. Differential abundance analysis of mangrove-associated microorganisms revealed enrichment of pelagic oligotrophic taxa during high tide and enrichment of putative sediment-associated microbes during low tide. Our study underpins the importance of tidal and diurnal time scales in structuring coastal microbial and nutrient dynamics, with diel and tidal cycles contributing to a highly dynamic microbial environment in mangroves, and time of day likely contributing to microbial dynamics in seagrass and reef biomes.
Microorganisms are central to the functioning of coral reef ecosystems, but their dynamics are unstudied on most reefs. We examined the microbial ecology of shallow reefs within the Federated States of Micronesia. We surveyed 20 reefs surrounding 7 islands and atolls (Yap, Woleai, Olimarao, Kosrae, Kapingamarangi, Nukuoro, and Pohnpei), spanning 875053 km 2 . On the reefs, we found consistently higher coral coverage (mean ± SD = 36.9 ± 22.2%; max 77%) compared to macroalgae coverage (15.2 ± 15.5%; max 58%), and low abundances of fish. Reef waters had low inorganic nutrient concentrations and were dominated by Synechococcus, Prochlorococcus, and SAR11 bacteria. The richness of bacterial and archaeal communities was significantly related to interactions between island/atoll and depth. High coral coverage on reefs was linked to higher relative abundances of Flavobacteriaceae, Leisingera, Owenweeksia, Vibrio, and the OM27 clade, as well as other heterotrophic bacterial groups, consistent with communities residing in waters near corals and within coral mucus. Microbial community structure at reef depth was significantly correlated with geographic distance, suggesting that island biogeography influences reef microbial communities. Reefs at Kosrae Island, which hosted the highest coral abundance and diversity, were unique compared to other locations; seawater from Kosrae reefs had the lowest organic carbon (59.8-67.9 µM), highest organic nitrogen (4.5-5.3 µM), and harbored consistent microbial communities (>85% similar), which were dominated by heterotrophic cells. This study suggests that the reef-water microbial ecology on Micronesian reefs is influenced by the density and diversity of corals as well as other biogeographical features.
Mesophotic coral reef ecosystems (MCEs) are characterized by gradients in irradiance, temperature and trophic resources. As depth increases on Caribbean mesophotic reefs, particulate organic matter increases while dissolved organic matter decreases, and the increase in particulate organic matter is directly related to the increase in sponge abundances and growth rates on MCEs. To further understand the trophic ecology of sponges, changes in microbiome composition and function, stable isotopic composition and proximate biochemical composition of 4 Caribbean reef sponges ( Amphimedon compressa , Agelas tubulata , Plakortis angulospiculatus and Xestospongia muta) were quantified along a shallow to mesophotic depth gradient on Grand Cayman Island. Increases in δ 15 N for all sponges were observed as depth increased, indicating an increasing reliance on heterotrophic food resources. Species-specific changes in symbiotic microbial community composition were also observed as depth increased, and the predicted functional genes associated with nitrogen and carbon cycling showed species-specific changes between depths. Regardless of species-specific changes in microbiome community structure or function, or whether sponges were classified as high microbial or low microbial abundance, sponges increased their consumption of particulate organic matter with increasing depth into the lower mesophotic zone.
Seawater microorganisms play an important role in coral reef ecosystem functioning and can be influenced by biological, chemical, and physical features of reefs. As coral reefs continue to respond to environmental changes, the reef seawater microbiome has been proposed as a conservation tool for monitoring perturbations. However, the spatial variability of reef seawater microbial communities is not well studied, limiting our ability to make generalizable inferences across reefs. In order to better understand how microorganisms are distributed at multiple spatial scales, we examined seawater microbial communities in Florida Reef Tract and US Virgin Islands reef systems using a nested sampling design. On 3 reefs per reef system, we sampled seawater at regular spatial intervals close to the benthos. We assessed the microbial community composition of these waters using ribosomal RNA gene amplicon sequencing. Our analysis revealed that reef water microbial communities varied as a function of reef system and individual reefs, but communities did not differ within reefs and were not significantly influenced by benthic composition. For the reef system and inter-reef differences, abundant microbial taxa were found to be potentially useful indicators of environmental difference due to their high prevalence and variance. We further examined reef water microbial biogeography on a global scale using a secondary analysis of 5 studies, which revealed that microbial communities were more distinct with increasing geographic distance. These results suggest that biogeography is a distinguishing feature for reef water microbiomes, and that development of monitoring criteria may necessitate regionally specific sampling and analyses.
Lima, Laís F., Weissman, Maya, Reed, Micheal, Papudeshi, Bhavya, Alker, Amanda T., Morris, Megan M., Edwards, Robert A., de Putron, Samantha J., Vaidya, Naveen K., Dinsdale, Elizabeth A., Medina, Monica, and McFall-Ngai, Margaret J. Modeling of the Coral Microbiome: the Influence of Temperature and Microbial Network. Retrieved from https://par.nsf.gov/biblio/10190664. mBio 11.2 Web. doi:10.1128/mBio.02691-19.
Lima, Laís F., Weissman, Maya, Reed, Micheal, Papudeshi, Bhavya, Alker, Amanda T., Morris, Megan M., Edwards, Robert A., de Putron, Samantha J., Vaidya, Naveen K., Dinsdale, Elizabeth A., Medina, Monica, & McFall-Ngai, Margaret J. Modeling of the Coral Microbiome: the Influence of Temperature and Microbial Network. mBio, 11 (2). Retrieved from https://par.nsf.gov/biblio/10190664. https://doi.org/10.1128/mBio.02691-19
Lima, Laís F., Weissman, Maya, Reed, Micheal, Papudeshi, Bhavya, Alker, Amanda T., Morris, Megan M., Edwards, Robert A., de Putron, Samantha J., Vaidya, Naveen K., Dinsdale, Elizabeth A., Medina, Monica, and McFall-Ngai, Margaret J.
"Modeling of the Coral Microbiome: the Influence of Temperature and Microbial Network". mBio 11 (2). Country unknown/Code not available. https://doi.org/10.1128/mBio.02691-19.https://par.nsf.gov/biblio/10190664.
@article{osti_10190664,
place = {Country unknown/Code not available},
title = {Modeling of the Coral Microbiome: the Influence of Temperature and Microbial Network},
url = {https://par.nsf.gov/biblio/10190664},
DOI = {10.1128/mBio.02691-19},
abstractNote = {ABSTRACT Host-associated microbial communities are shaped by extrinsic and intrinsic factors to the holobiont organism. Environmental factors and microbe-microbe interactions act simultaneously on the microbial community structure, making the microbiome dynamics challenging to predict. The coral microbiome is essential to the health of coral reefs and sensitive to environmental changes. Here, we develop a dynamic model to determine the microbial community structure associated with the surface mucus layer (SML) of corals using temperature as an extrinsic factor and microbial network as an intrinsic factor. The model was validated by comparing the predicted relative abundances of microbial taxa to the relative abundances of microbial taxa from the sample data. The SML microbiome from Pseudodiploria strigosa was collected across reef zones in Bermuda, where inner and outer reefs are exposed to distinct thermal profiles. A shotgun metagenomics approach was used to describe the taxonomic composition and the microbial network of the coral SML microbiome. By simulating the annual temperature fluctuations at each reef zone, the model output is statistically identical to the observed data. The model was further applied to six scenarios that combined different profiles of temperature and microbial network to investigate the influence of each of these two factors on the model accuracy. The SML microbiome was best predicted by model scenarios with the temperature profile that was closest to the local thermal environment, regardless of the microbial network profile. Our model shows that the SML microbiome of P. strigosa in Bermuda is primarily structured by seasonal fluctuations in temperature at a reef scale, while the microbial network is a secondary driver. IMPORTANCE Coral microbiome dysbiosis (i.e., shifts in the microbial community structure or complete loss of microbial symbionts) caused by environmental changes is a key player in the decline of coral health worldwide. Multiple factors in the water column and the surrounding biological community influence the dynamics of the coral microbiome. However, by including only temperature as an external factor, our model proved to be successful in describing the microbial community associated with the surface mucus layer (SML) of the coral P. strigosa . The dynamic model developed and validated in this study is a potential tool to predict the coral microbiome under different temperature conditions.},
journal = {mBio},
volume = {11},
number = {2},
author = {Lima, Laís F. and Weissman, Maya and Reed, Micheal and Papudeshi, Bhavya and Alker, Amanda T. and Morris, Megan M. and Edwards, Robert A. and de Putron, Samantha J. and Vaidya, Naveen K. and Dinsdale, Elizabeth A. and Medina, Monica and McFall-Ngai, Margaret J.},
}
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