The Unseen Drivers of Coral Health; Coral Microbiome; The Hope for Effective Coral Restoration

ABSTRACT Microbial relationships are critical to coral health, and changes in microbiomes are often exhibited following environmental disturbance. However, the dynamics of coral-microbial composition and external factors that govern coral microbiome assembly and response to disturbance remain largely uncharacterized. Here, we investigated how antibiotic-induced disturbance affects the coral mucus microbiota in the facultatively symbiotic temperate coral Astrangia poculata, which occurs naturally with high (symbiotic) or low (aposymbiotic) densities of the endosymbiotic dinoflagellate Breviolum psygmophilum. We also explored how differences in the mucus microbiome of natural and disturbed A. poculata colonies affected levels of extracellular superoxide, a reactive oxygen species thought to have both beneficial and detrimental effects on coral health. Using a bacterial and archaeal small-subunit (SSU) rRNA gene sequencing approach, we found that antibiotic exposure significantly altered the composition of the mucus microbiota but that it did not influence superoxide levels, suggesting that superoxide production in A. poculata is not influenced by the mucus microbiota. In antibiotic-treated A. poculata exposed to ambient seawater, mucus microbiota recovered to its initial state within 2 weeks following exposure, and six bacterial taxa played a prominent role in this reassembly. Microbial composition among symbiotic colonies was more similar throughout the 2-week recovery period than that among aposymbiotic colonies, whose microbiota exhibited significantly more interindividual variability after antibiotic treatment and during recovery. This work suggests that the A. poculata mucus microbiome can rapidly reestablish itself and that the presence of B. psygmophilum, perhaps by supplying nutrients, photosynthate, or other signaling molecules, exerts influence on this process. IMPORTANCE Corals are animals whose health is often maintained by symbiotic microalgae and other microorganisms, yet they are highly susceptible to environmental-related disturbances. Here, we used a known disruptor, antibiotics, to understand how the coral mucus microbial community reassembles itself following disturbance. We show that the Astrangia poculata microbiome can recover from this disturbance and that individuals with algal symbionts reestablish their microbiomes in a more consistent manner compared to corals lacking symbionts. This work is important because it suggests that this coral may be able to recover its mucus microbiome following disturbance, it identifies specific microbes that may be important to reassembly, and it demonstrates that algal symbionts may play a previously undocumented role in microbial recovery and resilience to environmental change.

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

10.21203/rs.3.rs-600995/v1 ◽

2021 ◽

Author(s):

Laís Farias Oliveira Lima ◽

Amanda Alker ◽

Bhavya Papudeshi ◽

Megan Morris ◽

Robert Edwards ◽

...

Keyword(s):

Microbial Community ◽

Nutrient Cycling ◽

Ecosystem Functioning ◽

Environmental Changes ◽

Coral Host ◽

Shotgun Metagenomics ◽

Patch Reefs ◽

Coral Microbiome ◽

Gene Functions ◽

Coral Health

Abstract 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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The Organelle in the Room: Under-annotated Mitochondrial Reads Bias Coral Microbiome Analysis

10.1101/2021.02.23.431501 ◽

2021 ◽

Author(s):

Dylan Sonett ◽

Tanya Brown ◽

Johan Bengtsson-Palme ◽

Jacqueline L. Padilla-Gamiño ◽

Jesse R. Zaneveld

Keyword(s):

16S Rrna ◽

16S Rrna Genes ◽

Rrna Genes ◽

Rrna Gene ◽

Microbiome Analysis ◽

Coral Microbiome ◽

Β Diversity ◽

Microbial Eukaryotes ◽

Microbial Taxonomy ◽

Coral Health

AbstractThe microbiomes of tropical corals are actively studied using 16S rRNA gene amplicons to understand microbial roles in coral health, metabolism, and disease resistance. However, primers targeting bacterial and archaeal 16S rRNA genes may also amplify organelle rRNA genes from the coral, associated microbial eukaryotes, and encrusting organisms. In this manuscript, we demonstrate that standard workflows for annotating microbial taxonomy severely under-annotate mitochondrial sequences in 1272 coral microbiomes from the Earth Microbiome Project. This issue prevents annotation of >95% of reads in some samples and persists when using either Greengenes or SILVA taxonomies. Worse, mitochondrial under-annotation varies between species and across anatomy, biasing comparisons of α- and β-diversity. By supplementing existing taxonomies with diverse mitochondrial rRNA sequences, we resolve ~97% of unique unclassified sequences as mitochondrial, without increasing misannotation in mock communities. We recommend using these extended taxonomies for coral microbiome analysis and encourage vigilance regarding similar issues in other hosts.

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Adding insult to injury: Effects of chronic oxybenzone exposure and elevated temperature on two reef-building corals

10.1101/2019.12.19.882332 ◽

2019 ◽

Author(s):

Tim Wijgerde ◽

Mike van Ballegooijen ◽

Reindert Nijland ◽

Luna van der Loos ◽

Christiaan Kwadijk ◽

...

Keyword(s):

Global Warming ◽

Elevated Temperature ◽

Heat Wave ◽

Effect Study ◽

List Type ◽

Stylophora Pistillata ◽

Coral Microbiome ◽

The Face ◽

Acropora Tenuis ◽

Coral Health

AbstractWe studied the effect of chronic oxybenzone exposure and elevated temperature on coral health. Microcolonies of Stylophora pistillata and Acropora tenuis were cultured in 20 flow-through aquaria, of which 10 were exposed to oxybenzone at a field-relevant concentration of ~0.06 μg L−1 at 26 °C. After two weeks, half of the corals experienced a heat wave culminating at 33 °C. All S. pistillata colonies survived the heat wave, although heat reduced growth and zooxanthellae density, irrespective of oxybenzone. A. tenuis survival was reduced to 0% at 32 °C, and oxybenzone accelerated mortality. Oxybenzone and heat significantly reduced photosynthetic yield in both species, causing a 5% and 22−33% decrease, respectively. In addition, combined oxybenzone and temperature stress altered the abundance of five bacterial families in the microbiome of S. pistillata. Our results suggest that oxybenzone adds insult to injury by further weakening corals in the face of global warming.Highlights➢Chronic effect study on corals combining oxybenzone and elevated temperature➢Oxybenzone affected photosystem II of coral photosymbionts and altered coral microbiome➢Temperature effects were stronger than oxybenzone effects➢Sensitivities were species-dependent➢Oxybenzone adds insult to injury by weakening corals in the face of global warming

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Oceanographic habitat and the coral microbiomes of urban-impacted reefs

PeerJ ◽

10.7717/peerj.7552 ◽

2019 ◽

Vol 7 ◽

pp. e7552 ◽

Cited By ~ 2

Author(s):

Stephanie M. Rosales ◽

Christopher Sinigalliano ◽

Maribeth Gidley ◽

Paul R. Jones ◽

Lewis J. Gramer

Keyword(s):

Wave Height ◽

Relative Abundance ◽

Significant Wave Height ◽

High Throughput Sequencing ◽

Numerical Models ◽

Sea Temperature ◽

Significant Wave ◽

Coral Microbiome ◽

Coral Health

Coral reefs are in decline worldwide. In response to this habitat loss, there are efforts to grow, outplant, and restore corals in many regions. The physical oceanographic habitat of corals—such as sea temperature, waves, ocean currents, and available light—is spatially heterogeneous. We therefore hypothesize that outplant location may affect microbiomes, and ultimately, coral health and restoration success. We evaluated the influence of the physical oceanographic habitat on microbes in wild Porites astreoides and Siderastrea siderea. Tissue samples were collected at four Florida reefs in March, June, and September of 2015. We estimated oceanographic conditions from moored instruments, diver observations, remote sensing data, and numerical models. We analyzed microbiomes using amplicon 16S rRNA high-throughput sequencing data. We found microbial alpha-diversity negatively correlated with in situ sea temperature (which represented both the annual cycle and upwelling), as well as modeled alongshore currents, in situ sea-level, and modeled tide. Microbial beta-diversity correlated positively with significant wave height and alongshore currents from models, remotely-sensed relative turbidity, and in situ temperature. We found that archaea from the order Marine Group II decrease with increases in significant wave height, suggesting that this taxon may be influenced by waves. Also, during times of high wave activity, the relative abundance of bacteria from the order Flavobacteriales increases, which may be due to resuspension and cross-shelf transport of sediments. We also found that bacteria from the order SAR86 increase in relative abundance with increased temperature, which suggests that this taxon may play a role in the coral microbiome during periods of higher temperature. Overall, we find that physical oceanographic variability correlates with the structure of these coral microbiomes in ways that could be significant to coral health.

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A place for taxonomic profiling in the study of the coral prokaryotic microbiome

FEMS Microbiology Letters ◽

10.1093/femsle/fnz063 ◽

2019 ◽

Vol 366 (6) ◽

Cited By ~ 4

Author(s):

Alejandra Hernandez-Agreda ◽

William Leggat ◽

Tracy D Ainsworth

Keyword(s):

Temporal Dynamics ◽

Current Knowledge ◽

Amplicon Sequencing ◽

Taxonomic Profiling ◽

Coral Microbiome ◽

16S Amplicon Sequencing ◽

Coral Health ◽

Abundance And Diversity ◽

Physical And Chemical ◽

Healthy Coral

ABSTRACT The enormous variability in richness, abundance and diversity of unknown bacterial organisms inhabiting the coral microbiome have challenged our understanding of their functional contribution to coral health. Identifying the attributes of the healthy meta-organism is paramount for contemporary approaches aiming to manipulate dysbiotic stages of the coral microbiome. This review evaluates the current knowledge on the structure and mechanisms driving bacterial communities in the coral microbiome and discusses two topics requiring further research to define the healthy coral microbiome. (i) We examine the necessity to establish microbial baselines to understand the spatial and temporal dynamics of the healthy coral microbiome and summarise conceptual and logistic challenges to consider in the design of these baselines. (ii) We propose potential mechanical, physical and chemical mechanisms driving bacterial distribution within coral compartments and suggest experiments to test them. Finally, we highlight aspects of the use of 16S amplicon sequencing requiring standardization and discuss its contribution to other multi-omics approaches.

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Cold-water Coral Microbiome and Environmental Microbial Communities in a Remote NE Atlantic Submarine Canyon Setting: Microbial Diversity, Coral Health and Prospects

10.21203/rs.3.rs-192160/v1 ◽

2021 ◽

Author(s):

J. K. M. Appah ◽

E. Dillane ◽

A. Lim ◽

R. O ’Riordan ◽

L. O’Reilly ◽

...

Keyword(s):

Microbial Diversity ◽

Microbial Communities ◽

Cold Water ◽

Current Trend ◽

Benthic Fauna ◽

Lophelia Pertusa ◽

Coral Microbiome ◽

16S Rna ◽

Coral Health ◽

Bacterial Groups

Abstract In the Porcupine Bank Canyon, Lophelia pertusa and Madrepora oculata are the main framework-forming corals producing three dimensional structures which provide a home for a range of benthic fauna and microbial communities. To understand the roles and functions that microbes perform in coral health in the Porcupine Bank Canyon, three groups of samples (corals, sediment and water) were collected between 600–800 m depth. DNA was extracted from these samples and metabarcoding was performed on the V3-V4 region of the 16S RNA gene using Illumina technology. The coral microbiome showed greater microbial diversity than both the surrounding sediment and water communities. The genera Pseudomonas, Pseudoalteramonas and Photobacterium were the bacterial communities conserved at 100% coverage of coral samples whereas at the order-level classification Clostridiales, Bacteroidales, Flavobacteriales, Rhodobacterales and Rickettsiales were in high abundance in all the coral samples. A disproportionate distribution of probiotic and pathogenic bacterial groups at the different levels of classification was observed on the corals. Corals do not appear, at present, to be stressed by climate induced changing environmental conditions in the upper Porcupine Bank Canyon. Overall, the corals in the Porcupine Bank Canyon are in a healthy state despite the detection of pathogenic bacterial groups. However, the current trend of climate change and subsequent deep-sea warming could shift the bacterial composition towards a more dominant pathogenic bacterial community, with serious implications for coral health and stability of this important ecosystem.

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Microbiome restructuring: dominant coral bacterium Endozoicomonas species display differential adaptive capabilities to environmental changes

10.1101/2021.10.31.466697 ◽

2021 ◽

Author(s):

Kshitij Tandon ◽

Yu-Jing Chiou ◽

Sheng-Ping Yu ◽

Hernyi Justin Hsieh ◽

Chih-Ying Lu ◽

...

Keyword(s):

Environmental Changes ◽

Reciprocal Transplant ◽

Transplant Experiment ◽

Coral Host ◽

Reciprocal Transplant Experiment ◽

Microbiome Composition ◽

Coral Microbiome ◽

Adaptive Capabilities ◽

Differential Adaptation ◽

Coral Health

Bacteria in the coral microbiome play a crucial role in determining coral health and fitness, and the coral host often restructures its microbiome composition in response to external factors. An important but often neglected factor determining this microbiome restructuring is the capacity of microbiome members to adapt to a new environment. To address this issue, we examined how the microbiome structure of Acropora muricata corals changed over 9 months following a reciprocal transplant experiment. Using a combination of metabarcoding, genomics, and comparative genomics approaches, we found that coral colonies separated by a small distance harbored different dominant Endozoicomonas related phylotypes belonging to two different species, including a novel species, Candidatus Endozoicomonas penghunesis 4G, whose chromosome level (complete) genome was also sequenced in this study. Furthermore, the two dominant Endozoicomonas species showed varied adaptation capabilities when coral colonies were transplanted in a new environment. The differential adaptation capabilities of dominant members of the microbiome can a) provide distinct advantages to coral hosts when subjected to changing environmental conditions and b) have positive implications for future reefs.

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Multi-domain probiotic consortium as an alternative to chemical remediation of oil spills at coral reefs and adjacent sites

Microbiome ◽

10.1186/s40168-021-01041-w ◽

2021 ◽

Vol 9 (1) ◽

Author(s):

Denise P. Silva ◽

Helena D. M. Villela ◽

Henrique F. Santos ◽

Gustavo A. S. Duarte ◽

José Roberto Ribeiro ◽

...

Keyword(s):

Microbial Community ◽

Coral Reefs ◽

Environmental Changes ◽

Oil Spills ◽

Anthropogenic Activities ◽

Oil Contamination ◽

Negative Effects ◽

Corexit 9500 ◽

Coral Health ◽

The Impact

Abstract Background Beginning in the last century, coral reefs have suffered the consequences of anthropogenic activities, including oil contamination. Chemical remediation methods, such as dispersants, can cause substantial harm to corals and reduce their resilience to stressors. To evaluate the impacts of oil contamination and find potential alternative solutions to chemical dispersants, we conducted a mesocosm experiment with the fire coral Millepora alcicornis, which is sensitive to environmental changes. We exposed M. alcicornis to a realistic oil-spill scenario in which we applied an innovative multi-domain bioremediator consortium (bacteria, filamentous fungi, and yeast) and a chemical dispersant (Corexit® 9500, one of the most widely used dispersants), to assess the effects on host health and host-associated microbial communities. Results The selected multi-domain microbial consortium helped to mitigate the impacts of the oil, substantially degrading the polycyclic aromatic and n-alkane fractions and maintaining the physiological integrity of the corals. Exposure to Corexit 9500 negatively impacted the host physiology and altered the coral-associated microbial community. After exposure, the abundances of certain bacterial genera such as Rugeria and Roseovarius increased, as previously reported in stressed or diseased corals. We also identified several bioindicators of Corexit 9500 in the microbiome. The impact of Corexit 9500 on the coral health and microbial community was far greater than oil alone, killing corals after only 4 days of exposure in the flow-through system. In the treatments with Corexit 9500, the action of the bioremediator consortium could not be observed directly because of the extreme toxicity of the dispersant to M. alcicornis and its associated microbiome. Conclusions Our results emphasize the importance of investigating the host-associated microbiome in order to detect and mitigate the effects of oil contamination on corals and the potential role of microbial mitigation and bioindicators as conservation tools. Chemical dispersants were far more damaging to corals and their associated microbiome than oil, and should not be used close to coral reefs. This study can aid in decision-making to minimize the negative effects of oil and dispersants on coral reefs.

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Specificity of Associations between Bacteria and the Coral Pocillopora meandrina during Early Development

Applied and Environmental Microbiology ◽

10.1128/aem.01232-12 ◽

2012 ◽

Vol 78 (20) ◽

pp. 7467-7475 ◽

Cited By ~ 33

Author(s):

Amy Apprill ◽

Heather Q. Marlow ◽

Mark Q. Martindale ◽

Michael S. Rappé

Keyword(s):

Small Subunit ◽

Rrna Genes ◽

Polymorphism Analysis ◽

Roseobacter Clade ◽

Small Subunit Rrna ◽

Content Type ◽

Sterile Seawater ◽

Show Evidence ◽

Coral Health

ABSTRACTRelationships between corals and specific bacterial associates are thought to play an important role in coral health. In this study, the specificity of bacteria associating with the coralPocillopora meandrinawas investigated by exposing coral embryos to various strains of cultured marine bacteria, sterile seawater, or raw seawater and examining the identity, density, and location of incorporated cells. The isolates utilized in this experiment included members of the Roseobacter and SAR11 clades of theAlphaproteobacteria, aPseudoalteromonasspecies of theGammaproteobacteria, and aSynechococcusspecies of theCyanobacteriaphylum. Based on terminal restriction fragment length polymorphism analysis of small-subunit rRNA genes, similarities in bacterial communities associated with 170-h-old planulae were observed regardless of treatment, suggesting that bacteria may have been externally associated from the outset of the experiment. Microscopic examination ofP. meandrinaplanulae by fluorescencein situhybridization with bacterial and Roseobacter clade-specific oligonucleotide probes revealed differences in the densities and locations of planulae-associated cells. Planulae exposed to either raw seawater or strains ofPseudoalteromonasand Roseobacter harbored the highest densities of internally associated cells, of which 20 to 100% belonged to the Roseobacter clade. Planulae exposed to sterile seawater or strains of the SAR11 clade andSynechococcusdid not show evidence of prominent bacterial associations. Additional analysis of the raw-seawater-exposed planulae via electron microscopy confirmed the presence of internally associated prokaryotic cells, as well as virus-like particles. These results suggest that the availability of specific microorganisms may be an important factor in the establishment of coral-bacterial relationships.

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