Written by Sara Gagliardi

Edited by Danielle Moloney

Introduction

The unprecedented mass coral bleaching events hitting coral reefs in recent decades,  causing researchers to question its causes and consequences, as well as the solutions that can be taken. Coral bleaching is described as the disruption of the symbiotic relationship between coral tissues and the endosymbiotic algae of the Symbiodiniaceae family, and is primarily due to the temperature-related damage of the photosystem apparatus of these algae. As these algae are expelled from the tissues due to water increase, the coral loses his primary food source and eventually dies.

Besides this important interaction, corals are associated with other microorganisms (bacteria, fungi, protistes, viruses, etc.), forming what is called the coral holobiont. As knowledge has increased about the beneficial role of bacteria in other organisms, such as the human body, the coral probiotic hypothesis has been presented. The coral probiotic hypothesis states that microbes support coral health through selection of advantageous configurations of the coral microbiome (i.e., the assemblage of the microorganisms associated with the coral tissues). This is done via mechanisms of antibiotic production, nutrient cycling, niche occupation, scavenge of reactive oxygen species (ROS), and microbial succession, and is based on the microbiome flexibility hypothesis (i.e., the potential and propensity for changes in the microbiome). Therefore, the research has increased its interest in finding, understanding and using these microbes that aid stress tolerance and resilience of corals, called beneficial microorganisms for corals (BMCs).

The experiment

In their study, Santoro and colleagues used a BMCs consortium of six bacterial strain with beneficial traits (e.g., nitrogen fixation or denitrification, dimethylsulfoniopropionate (DMSP) degradation, ROS scavenging potential, antagonistic activity against Vibrio coralliilyticus and/or Vibrio alginolyticus), no antagonistic activity against each other, and no records of harmful effects to humans or marine life. The study took place in mesocosms for 75 days, with four collection points: T0 at the beginning of the experiment, T1 at the peak of heat stress (30°C), T2 at the end of the 10-days peak stress, and T3 after a 15-day recovery period (end of the experiment). The BMCs consortium was applied to half of the coral fragments (BMC-treated and placebo) every three days during the simulated heat stress event and every 5 days during recovery. A control experiment ran with the same conditions but without inducement of heat stress.

Coral physiology was evaluated. The inoculation of the BMCs consortium allowed coral fragments to evade mortality during the experiment, with all coral fragments surviving at T3, compared to 60% survival of the placebo-treated corals due to bleaching. Furthermore, BMC-treated corals could recover from the decrease of the photosynthetic efficiency of the algae among their tissues. To explain the increased survival and recovery, analysis of the microbiome, the genetic expression(*) of each coral fragment (i.e., the transcriptome(**) of the holobiont), and the metabolic footprint were assessed at T2 and T3.

Results and discussion

The bacterial communities associated with coral tissues were different at the peak of heat stress (T2) between the BMCs and placebo-treated fragments, but became indistinguishable after the recovery period (T3), with most BMCs strains being lost after treatment. The role of BMCs in driving the structure of the microbiome was confirmed, but better understanding on their recruitment and incorporation under stress conditions should be ensured to improve the uptake and maintenance of these beneficial microbes.

The host transcriptome response to heat stress did not show significant differences between the BMC and placebo-treated fragments during the heat stress (T2), suggesting a similar holobiont response to the increasing temperature. However, the inoculation of BMCs helped the coral tissues to mitigate the post-heat stress disorder (PHSD), namely the effects of heat stress on the coral tissues after the period of recovery. The BMCs consortium showed a healing effect of PSHD, allowing coral tissues to attenuate the stress and increase their recovery by avoiding the expression of genes involved in apoptosis and inflammatory response. Indeed, placebo-treated coral survivors showed prolonged PHSD signs, with a higher expression of proteins involved in the response to thermal stress and apoptosis (e.g., production of kinases and receptors, signalling molecules, DNA methylation), triggering inflammatory and immune responses as well as cellular reconstruction (e.g., cytoskeleton organisation and anchoring, chromosome condensation, synthesis of membrane and secondary cell wall components, cellular adhesion proteins).

On the contrary, BMC-treated corals showed increased expression of genes associated with cellular homeostasis, biosynthesis of oestrogen and steroids, metabolic pathways, and cellular signalling and cycle, having a direct role in increasing the coral stress tolerance to heat. Furthermore, the metabolic profiles associated with BMC-treated corals highlighted the the maintenance of a lipidic reservoir and the exhibition of lower concentrations of dimethylsulfoniopropionate (DMSP) and dimethyl sulfoxide (DMSO) when compared to the placebo-treated fragments (even though DMSP was positively correlated to the presence of BMCs). Particularly, the presence of DMSP, produced by the algae, suggests the production of antimicrobial compounds by the microbiome that help the holobiont to control pathogens  (e.g., V. coralliilyticus), hence protecting the host from invasion.

Conclusion

The inoculation of selected BMCs consortium during heat stress induces changes in the holobiont at the level of the microbiome, the host gene expression and the metabolism, which coincide with an increase in the coral survival and improvement from recovery by the reconstruction of the host resilience and potential role of the BMCs in modulating pathogen infections. Hence, it is suggested that the inoculated consortium initiates a signal cascade within the holobiont that finally protects the host from thermal stress and blocks the PHSD symptoms, further corroborating the notion of the holobiont being a functional biological unit. More research is needed for the utilisation of such methods in the natural environment, however this study further highlights the potential of BMC treatments to improve coral resilience to the current climate crisis.

References

Santoro EP, Borges RM, Espinoza JL, Freire M, Messias CSMA, Villela HDM, et al. Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality. Science Advances. American Association for the Advancement of Science; 2021;7:eabg3088. 

Cover image: Mussismilia hispida colony, Flickr archive

(*) Gene expression: Process by which the information of a gene in the DNA is first converted into RNA and finally used to synthesise a functional product, such as a protein.

(**) Transcriptome: The collection of RNA sequences that a cell has transcribed from the DNA.