The incredible world of coral-associated microorganisms.

Written by Sara Gagliardi

Coral reefs are critical to the conservation of marine ecosystems as they create 3-D habitat structures marine fauna use as refuge. Therefore, they directly influence many economically important species such as seabream, jack mackerel, catshark, and octopus. Despite their economic value, coral populations are extremely fragile and are subject to population declines by both the climatic changes (e.g., increasing seawater temperature and acidification) and the anthropogenic activities (e.g., fishing, pollution, and agriculture). Indeed, NASA reported that over the past 50 years almost 27% of monitored coral reefs have been lost worldwide, and another 32% will be lost in the next 32 years.

Chasing Coral review
Fig. 1 Image of living (left) and dead (right) stony corals from the Netflix documentary “Chasing Coral” by Jeff Orlowski (2012, source: https://lwlies.com/reviews/chasing-coral/).

A critical driver of coral health and survival is the composition of the microbial communities that interact with the coral host, called the microbiome. Indeed, corals live in symbiosis – i.e., a close and long-term relationship between different species – with viruses, bacteria, archaea, fungi, protists, and other invertebrates. The assemblage of the coral animal and its microbiome is termed the holobiont. Van de Water recovered that the association with microbes are present in the long-term history of coral evolution, as they play critical roles for the longevity of their host. It is therefore important for the survival of the holobiont to maintain these fragile relationships, although they are highly influenced by climatic changes and anthropogenic stressors.

Two subclasses of invertebrates include corals: the Hexacorallia (including sea anemones, black corals, scleractinian corals, or stony corals, corallimorpharians, tubular corals, and rugose corals) and the Octocorallia (including blue corals, soft corals, sea pens, and gorgonians). Extensive research has been conducted on the microbiome of stony corals, which has been described as diverse and variable on both spatial and temporal scales. Unlike stony corals, octocorals seem to maintain more stable microbial communities, although coral microbiome research seems to focus heavily on scleractinian corals and the bacterial fraction of the microbiome. Van de Water decided to study the bacterial composition of Antipathella subpinnata, a black coral of the Mediterranean Sea that provides critically important habitats in the mesophotic (40 to 150 m depth) by creating arborescent colonies. The author chose three sample locations, Portofino, Bordighera and Savona (Italy), during spring and autumn.

Antipathella subpinnata, Corallo nero, Antipataro ...
Fig. 2 Antipathella subpinnata, a black coral of Mediterranean Sea (source: http://www.biologiamarina.org/corallo-nero/).

Results of the analysis did not highlight a core microbiome – i.e., microbes that are ubiquitous in the coral specie, regardless of space and time – associated to A. subpinnata. Coral samples collected in Savona yielded a bacterial-associated community highly diverse from Portofino and Bordighera, with a major number of hydrocarbon-degrading gammaproteobacterial genera (Alcanivorax, Oleiphilus and Marinobacter). Van de Water suggested that this difference could be due to the presence of many commercial fishing vessels, cruises, and cargo ships in the port of Savona, while the Portofino and Bordighera ports are only frequented by yachts. The researcher speculates bacteria degrading hydrocarbons might have thrived because of the higher availability of resources in Savona. Moreover, he speculates the local currents (e.g., the anti-cyclonic currents) might play an important role as drivers of the microbial communities associated to A. subpinnata because of the induction of important upwellings of nutrient-rich waters from the depth that modifyrisut the balance of the holobiont functionalities. Finally, the environmental conditions might impact the planktonic communities that are a source of nutrients for corals, thus resulting in local and temporal differences in the microbiome composition and, potentially, in its functions.

Van de Water suggested that rather than having a core microbiome, black corals possess a microbiome with redundant functions to ensure the survival of the holobiont. These functions include the provisioning of important nutrients, the role in biogeochemical cycles (carbon, nitrogen, sulfur), the defence against pathogens, etc. Indeed, some bacteria can break down complex organic carbon compounds to digest prey (e.g., Bacteroidetes can degrade chitin, which composes the cell wall of fungi, the skeleton of black corals, the exoskeleton of arthropods, etc.). Others carry out important pathways in the cycles of nitrogen and sulphur to provide the coral molecules for the production of amino acids (e.g., Endozoicomonas) and/or antimicrobial compounds (e.g., Pseudovibrio sp.). However, it is thought that nitrogen and sulphur are overall lost by nutrient cycles among the holobiont, and therefore predation by the coral is required to overcome the depletion. Moreover, it is thought that some bacteria (e.g., Pseudoalteromonas) are present among the microbiome to regulate the composition of the microbial communities by secreting compounds with antibacterial, antifungal and alginolytic activities. This regulatory activity might be performed in the event of an environmental change to adjust the functionalities of the microbiome in the aim of maintaining survival of the host.

Antipathella subpinnata, Corallo nero, Antipataro ...
Fig. 3 Antipathella subpinnata in the deep Mediterranean Sea reefs (source: http://www.biologiamarina.org/corallo-nero/).

Due to their sedentary lifestyles, corals are unable to escape from suddenly unfavourable environments and require a mechanism to combat the disadvantages of this characteristic. The composition of the microbiome associated with the black coral A. subpinnata appears to be flexible and likely influenced by the local environmental conditions, yet the key functionalities for the prosperity of the holobiont are maintained as a likely result of redundancy within the microbiome. This microbiome plasticity is critical for the holobiont to adapt and/or rapidly acclimate in response to short and long-term environmental stressors.

References

van de Water, J. A. J. M., Coppari, M., Enrichetti, F., Ferrier-Pagès, C., & Bo, M. (2020). Local conditions influence the prokaryotic communities associated with the mesophotic black coral Antipathella subpinnata. Frontiers in Microbiology, 11, 1-20. DOI :10.3389/fmicb.2020.537813

https://en.wikipedia.org/wiki/Symbiosis

https://en.wikipedia.org/wiki/Hexacorallia

https://en.wikipedia.org/wiki/Octocorallia

https://earthobservatory.nasa.gov/features/Coral

https://en.wikipedia.org/wiki/Chitin

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