Microbial solutions must be deployed against climate catastrophe

Microbial solutions must be deployed against climate catastrophe

Microbes and the climate crisis

Microorganisms have a pivotal but often overlooked role in the climate system1,2,3 — they drive the biogeochemical cycles of our planet, are responsible for the emission, capture and transformation of greenhouse gases, and control the fate of carbon in terrestrial and aquatic ecosystems. From humans to corals, most organisms rely on a microbiome that assists with nutrient acquisition, defence against pathogens and other functions. Climate change can shift this host–microbiome relationship from beneficial to harmful4. For example, ongoing global coral bleaching events, where symbiotic host–microbiome relationships are replaced by dysbiotic (that is, pathogenic) interactions (Fig. 1), and the consequent mass mortality mean the extinction of these ‘rainforests of the sea’ may be witnessed in this lifetime5. Specifically, a decline of 70–90% in coral reefs is expected with a global temperature rise of 1.5 °C (ref. 6). Although this example highlights how the microbiome is inextricably linked to climate problems, there is a wealth of evidence that microbes and the microbiome have untapped potential as viable climate solutions (Table 1). However, despite the promise of these approaches, they have yet to be embraced or deployed at scale in a safe and coordinated way that integrates the necessary but also feasible risk assessment and ethical considerations7.

Fig. 1: Corals and climate change.
Microbial solutions must be deployed against climate catastrophe

ad Examples of the same healthy (a, b), bleached (c) and dead (d) corals before (a, b) and after (c, d) being affected by heatwaves caused by climate change. Photos by Morgan Bennett-Smith.

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Mobilizing microbiome solutions to climate change

The multifaceted impacts of climate change on the environment, health and global economy demand a similar, if not more urgent and broad, mobilization of technologies as observed in response to the COVID-19 pandemic8,9. To facilitate the use of microbiome-based approaches and drawing from lessons learned during the COVID-19 pandemic9, we advocate for a decentralized yet globally coordinated strategy that cuts through bureaucratic red tape and considers local cultural and societal regulations, culture, expertise and needs. We are ready to work across sectors to deploy microbiome technologies at scale in the field.

We also propose that a global science-based climate task force comprising representatives from scientific societies and institutions should be formed to facilitate the deployment of these microbiome technologies. We volunteer ourselves to spearhead this, but we need your help too. Such a task force would provide stakeholders such as the Intergovernmental Panel on Climate Change (IPCC) committee and United Nations COP conference organizers, and global governments access to rigorous, rapid response solutions. Accompanied by an evidence-based framework, the task force will enable pilot tests to validate and scale up solutions, apply for dedicated funding, facilitate cross-sector collaboration and streamlined regulatory processes while ensuring rigorous safety and risk assessments. The effectiveness of this framework will be evaluated by key performance indicators, assessing the scope and impact of mitigation strategies on carbon reduction, ecosystem restoration and enhancement of resilience in affected communities, aiming to provide a diverse and adaptable response to the urgent climate challenges faced today. We must ensure that science is at the forefront of the global response to the climate crisis.

We encourage all relevant initiatives, governments and stakeholders to reach out to us at [email protected]. We are ready and willing to use our expertise, data, time and support for immediate action.

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Protein signatures predict coral resilience and survival to thermal bleaching events

Coral bleaching events from thermal stress are increasing globally in duration, frequency, and intensity. While bleaching can cause mortality, some corals survive, reacquire symbionts, and recover. We experimentally bleached Montipora capitata to examine molecular and physiological differences between corals that recover (resilient) and those that die (susceptible). Corals were collected and monitored for eight months post-bleaching to identify genets with long-term resilience. Using an integrated systems-biology approach that included quantitative proteomics, 16S rRNA sequencing to characterize the coral microbiome, total coral lipids, symbiont community composition and density, we explored molecular-level mechanisms of tolerance in corals pre- and post-bleaching. Prior to thermal stress, resilient corals have a more diverse microbiome and abundant proteins essential for carbon acquisition, symbiont retention, and pathogen resistance. Protein signatures of susceptible corals showed early symbiont rejection and utilized urea for carbon and nitrogen. Our results reveal molecular factors for surviving bleaching events and identify diagnostic protein biomarkers for reef management and restoration.

Filamentous virus-like particles are present in coral dinoflagellates across genera and ocean basins

Filamentous viruses are hypothesized to play a role in stony coral tissue loss disease (SCTLD) through infection of the endosymbiotic dinoflagellates (Family Symbiodiniaceae) of corals. To evaluate this hypothesis, it is critical to understand the global distribution of filamentous virus infections across the genetic diversity of Symbiodiniaceae hosts. Using transmission electron microscopy, we demonstrate that filamentous virus-like particles (VLPs) are present in over 60% of Symbiodiniaceae cells (genus Cladocopium) within Pacific corals (Acropora hyacinthus, Porites c.f. lobata); these VLPs are more prevalent in Symbiodiniaceae of in situ colonies experiencing heat stress. Symbiodiniaceae expelled from A. hyacinthus also contain filamentous VLPs, and these cells are more degraded than their in hospite counterparts. Similar to VLPs reported from SCTLD-affected Caribbean reefs, VLPs range from ~150 to 1500 nm in length and 16–37 nm in diameter and appear to constitute various stages in a replication cycle. Finally, we demonstrate that SCTLD-affected corals containing filamentous VLPs are dominated by diverse Symbiodiniaceae lineages from the genera Breviolum, Cladocopium, and Durusdinium. Although this study cannot definitively confirm or refute the role of filamentous VLPs in SCTLD, it demonstrates that filamentous VLPs are not solely observed in SCTLD-affected corals or reef regions, nor are they solely associated with corals dominated by members of a particular Symbiodiniaceae genus. We hypothesize that filamentous viruses are a widespread, common group that infects Symbiodiniaceae. Genomic characterization of these viruses and empirical tests of the impacts of filamentous virus infection on Symbiodiniaceae and coral colonies should be prioritized.

Genomic and transcriptomic insights into complex virus–prokaryote interactions in marine biofilms

Marine biofilms are complex communities of microorganisms that play a crucial ecological role in oceans. Although prokaryotes are the dominant members of these biofilms, little is known about their interactions with viruses. By analysing publicly available and newly sequenced metagenomic data, we identified 2446 virus–prokaryote connections in 84 marine biofilms. Most of these connections were between the bacteriophages in the Uroviricota phylum and the bacteria of Proteobacteria, Cyanobacteria and Bacteroidota. The network of virus–host pairs is complex; a single virus can infect multiple prokaryotic populations or a single prokaryote is susceptible to several viral populations. Analysis of genomes of paired prokaryotes and viruses revealed the presence of 425 putative auxiliary metabolic genes (AMGs), 239 viral genes related to restriction–modification (RM) systems and 38,538 prokaryotic anti-viral defence-related genes involved in 15 defence systems. Transcriptomic evidence from newly established biofilms revealed the expression of viral genes, including AMGs and RM, and prokaryotic defence systems, indicating the active interplay between viruses and prokaryotes. A comparison between biofilms and seawater showed that biofilm prokaryotes have more abundant defence genes than seawater prokaryotes, and the defence gene composition differs between biofilms and the surrounding seawater. Overall, our study unveiled active viruses in natural biofilms and their complex interplay with prokaryotes, which may result in the blooming of defence strategists in biofilms. The detachment of bloomed defence strategists may reduce the infectivity of viruses in seawater and result in the emergence of a novel role of marine biofilms.

Microbiome-based interventions to modulate gut ecology and the immune system

The gut microbiome lies at the intersection between the environment and the host, with the ability to modify host responses to disease-relevant exposures and stimuli. This is evident in how enteric microbes interact with the immune system, e.g., supporting immune maturation in early life, affecting drug efficacy via modulation of immune responses, or influencing development of immune cell populations and their mediators. Many factors modulate gut ecosystem dynamics during daily life and we are just beginning to realise the therapeutic and prophylactic potential of microbiome-based interventions. These approaches vary in application, goal, and mechanisms of action. Some modify the entire community, such as nutritional approaches or faecal microbiota transplantation, while others, such as phage therapy, probiotics, and prebiotics, target specific taxa or strains. In this review, we assessed the experimental evidence for microbiome-based interventions, with a particular focus on their clinical relevance, ecological effects, and modulation of the immune system.

Molecules-mediated bidirectional interactions between microbes and human cells

Complex molecules-mediated interactions, which are based on the bidirectional information exchange between microbes and human cells, enable the defense against diseases and health maintenance. Recently, diverse single-direction interactions based on active metabolites, immunity factors, and quorum sensing signals have largely been summarized separately. In this review, according to a simplified timeline, we proposed the framework of Molecules-mediated Bidirectional Interactions (MBI) between microbe and humans to decipher and understand their intricate interactions systematically. About the microbe-derived interactions, we summarized various molecules, such as short-chain fatty acids, bile acids, tryptophan catabolites, and quorum sensing molecules, and their corresponding human receptors. Concerning the human-derived interactions, we reviewed the effect of human molecules, including hormones, cytokines, and other circulatory metabolites on microbial characteristics and phenotypes. Finally, we discussed the challenges and trends for developing and deciphering molecule-mediated bidirectional interactions and their potential applications in the guard of human health.

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