Restoring Earth’s Damaged Microbiomes
Raquel Peixoto
King Abdullah University of Science and Technology, Saudi Arabia
“Restoring microbiomes is a viable and imperative strategy to alleviating the impacts of breaching planetary boundaries on marine wildlife”
Six of the nine planetary boundaries have been breached. Climate change and other human-derived (anthropogenic) impacts are turning formerly pristine ecosystems, including microbiomes, into degraded ‘new normal’ states. These degraded ecosystems and organisms present a clear shift from native, and beneficial, microbiomes towards groups of disease-causing species – also called harmful microbiomes - that may affect the entire ecosystem functioning and is linked to biodiversity loss. Restoring microbiomes of degraded ecosystems is no longer a decision we need to make, but a reality we need to face. Coral reefs, for example, also referred to as the marine “canaries of the coal mine”, are threatened with functional extinction (i.e., the lack of their ecological services), by 2030, due to local and global impacts. Degraded corals and coral reefs have, as other degraded ecosystems, a harmful microbiome signature. The increasing seawater temperature linked with increases in greenhouse gas (GHG) emissions is the greatest threat to these ecosystems, causing the breakdown of key symbiotic interactions within the coral ecosystem (i.e., the coral and community of microorganisms associated with it) and consequent mass mortality that have already lead to a decline of 30% of the global coral population. The effects of climate change are further exacerbated by local stressors and disease outbreaks affecting these biodiversity hotspots that support approximately one-third of all marine species and support fisheries, tourism revenue, coastal protection, and carbon sequestration (i.e., the capture and long-term storage of carbon dioxide), through their connectivity with other marine ecosystems and One Health - which is the notion that the health of all living organisms and ecosystems are connected and part of the one planet’s health concept. Recent estimations predict that 70-90% of reef corals are at risk to be lost if the increase in the global average temperature exceeds 1.5°C above pre-industrial temperatures, which may have already happened or be imminent.
Active restoration efforts are mandatory to retain some coral reefs while achieving carbon neutrality. Modern restoration paradigms demand a multifaceted approach and customized medicine, integrating various rehabilitation and preventive methodologies to ensure efficacy amidst evolving environmental challenges. We, therefore, propose that microbiome restoration and rehabilitation is an easier and faster way to restore damaged wildlife and their ecosystems (Figure 1), compared to the restoration of their hosts and ecosystem conditions. Microbial therapies can regenerate functional/beneficial microbiomes following a disruption caused by different environmental impacts (e.g., pathogen infection, antibiotic treatment, changes in temperature and pollution). We highlight this tool as a powerful alternative to reduce biodiversity loss, due to the quick response and short generation times of microbial therapies. Our group pioneered the development and deployment of microbial therapies for corals and other marine organisms, generating the only customized medicine approach available that has been validated to enhance coral health and growth in tank experiments and increase coral resistance to thermal impacts in field trials.
After our seminal papers showing the protocols, framework and results of rehabilitating corals (and, considering all co-authors, other wildlife such as amphibians and bees), we founded the BMMO network to connect researchers working on probiotics for different hosts and therefore improve and accelerate the development of probiotics for marine life. In addition, many other groups, part of not of the BMMO network, have also started working on it. Even an specific call for projects on coral probiotics was launched by the Great Barrier Reef Foundation, where they highlighted our promising results as their inspiration for the call.
Figure 1. Microbiome restoration and rehabilitation and One Health: Healthy organisms and ecosystems rely on healthy microbiomes. Microbes are key members of the most living organisms and connect different entities across ecosystems. Anthropogenic effects can disturb these healthy microbiomes, causing harmful shifts in the microbial composition associated with organisms and ecosystems and mortality. Microbes respond rapidly to interventions with immediate effects and are easier to manipulate than macro-organisms (such as corals, amphibians, insects and bats and can, therefore, represent a promising target to mitigate biodiversity loss at scale and support a healthy planet (source: Peixoto et al., 2022, Nature Microbiology).
Building upon the groundbreaking results we obtained using probiotics for corals in tank trials, and the further literature on coral probiotics, we developed automated tools (i.e., an underwater irrigation system) and infrastructure (i.e., an underwater laboratory) to test microbial therapies in situ). We also developed a framework to manufacture coral probiotics at scale (in partnership with Merck) to advance the deployment of affordable microbial therapies in the real world. During a record heatwave event in the Red Sea in 2023, we could quickly deploy our automated dispenser and produce enough probiotics to test its efficiency during a mass bleaching event, when the symbiotic interactions between corals and their associated microbiome are affected leading some of the corals to die. Although Red Sea corals seem to be more resilient than most corals from other regions, the effects of climate change, including significant levels of mortality, have already started to also impact Red Sea corals. Our recent results indicate significant health improvements promoted by coral probiotics in situ, even under critical heatwave conditions.
Our research can have a tremendous impact on maintaining a safe operating space for humanity. In addition to probiotics, we are also testing other microbial therapies as alternatives to support coral restoration and rehabilitation efforts, such as the use of postbiotics (i.e., inanimate probiotics and/or their components that can still benefit their hosts) and vaccines to prevent marine wildlife loss due to disease outbreaks triggered by climate change and pollution. Our unpublished recent results prove the concept that postbiotics can also be used to increase coral resilience in their natural environment (in situ). Furthermore, our ongoing research indicates that "priming" corals with sub-lethal doses of pathogens enhances their resistance to subsequent infections, revealing promising avenues for disease prevention/vaccination in marine wildlife. This technological revolution aids the protection of wildlife while the desired future scenario of reaching carbon neutrality is attained – on top of also having the potential to directly contribute to mitigating the causes of biodiversity loss, as we are currently testing the use of probiotics to support restoration and accelerate the growth of foundation plant species forming mangroves (which are coastal ecosystems and biodiversity hotspots) and seagrass meadows, potentially contributing to increased capture and storage of carbon by coastal and marine ecosystems – also referred to as “blue carbon”. We are also exploring the use of microbial therapies to treat sick and threatened sea turtles.
Following our disruptive results proving several concepts in the field of microbiome restoration and rehabilitation (e.g., that we can restore the microbiome of corals, that this restoration correlates with health improvements, that these improvements can help them evade mortality, that postbiotics can also promote coral health enhancement, and that microbial therapies can be delivered in situ and protect corals in the real world), we have also proposed a science-based flexible framework and risk assessment steps that can guide the development and deployment of microbial therapies for wildlife and other ecosystems. Such potentially easier, stronger, and faster medicine for biodiversity (and consequently One Health -Figure 1) can, in addition, be applied to directly help restore or protect planetary boundaries, such as their use for removing or neutralizing pollutants from the environment using living organisms (also called pollution bioremediation), recovery of degraded land and water and carbon fixation.
Microbiome restoration breakthroughs can be used to protect wildlife and help mitigate impacts that affect all nine planetary boundaries, through restoring microbes - the key drivers of all biogeochemical cycles that shape our planet as we know it.
Photo 1. Prof. Raquel Peixoto applying coral probiotics in situ during a heatwave event in the Red Sea. Photo by KAUST/Morgan Bennett-Smith.
