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3 September 2024

Marine Microorganism Molecules as Potential Anti-Inflammatory Therapeutics

,
,
and
1
Group Bioactivities of Natural Compounds and Derivatives (BIONA), Institut Pasteur of New Caledonia, Member of the Pasteur Network, Noumea 98845, New Caledonia
2
Ifremer, Institut de Recherche pour le Développement (IRD), Centre Nationale de la Recherche Scientifique (CNRS), Université de la Réunion, Université de la Nouvelle-Calédonie, UMR 9220 ENTROPIE, 101 Promenade Roger Laroque, Noumea 98897, New Caledonia
3
Team Neuroimmunology and Peptide Therapy, Biotechnologie et Signalisation Cellulaire, UMR 7242, University of Strasbourg, 67085 Strasbourg, France
*
Author to whom correspondence should be addressed.
Mar. Drugs2024, 22(9), 405;https://doi.org/10.3390/md22090405
This article belongs to the Special Issue Pharmacological Potential of Marine Natural Products
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Abstract

The marine environment represents a formidable source of biodiversity, is still largely unexplored, and has high pharmacological potential. Indeed, several bioactive marine natural products (MNPs), including immunomodulators, have been identified in the past decades. Here, we review how this reservoir of bioactive molecules could be mobilized to develop novel anti-inflammatory compounds specially produced by or derived from marine microorganisms. After a detailed description of the MNPs exerting immunomodulatory potential and their biological target, we will briefly discuss the challenges associated with discovering anti-inflammatory compounds from marine microorganisms.

1. Introduction

Chronic inflammatory diseases (CIDs) have emerged as a significant global concern, with a prevalence of 5 to 7% of Western society in 2010 [1]. These illnesses, such as psoriasis, rheumatoid arthritis (RA), inflammatory bowel disease (IBD), Crohn’s disease (CD), or ulcerative colitis (UC), can be debilitating, leading to a reduced quality of life and, in the most severe cases, premature death [2].
Conventional treatments based on corticoids and non-steroidal anti-inflammatory drugs (NSAIDs) often lead to severe side effects, including gastrointestinal ulceration and bleeding, osteoporosis, hypertension, and glaucoma. Drug development more recently has focused on monoclonal antibodies targeting inflammatory cytokines such as tumor necrosis factor-α (TNF-α) or interleukins (e.g., IL-6) [3], or inhibitors of pathways activated by inflammatory cytokines, such as Janus Kinase inhibitors (Jakinibs) [4]. Although these therapies have shown considerable clinical efficacy, many patients remain unresponsive, and others may develop resistance to monoclonal antibody treatment. Furthermore, the use of such immunomodulatory molecules carries a limited but notable risk of developing opportunistic infections, such as Herpes Zoster Virus [5].
As life expectancy increases, there is an increased likelihood of developing CIDs, and therefore, managing these diseases has become more challenging. Hence, continuing to explore innovative treatment exploration and improving their response to these debilitating diseases is crucial. In this regard, the discovery of bioactive molecules from marine microorganisms represents a groundbreaking pharmaceutical development that could promote the identification of novel therapeutic compounds to treat CIDs.
Here, we aim to review marine microorganisms that produce molecules with potential pharmaceutical relevance, categorizing them based on producing genus and species, compounds’ molecular structures, and their mechanism of action on immune signaling pathways. Additionally, we will provide a brief overview of the difficulties related to identifying anti-inflammatory compounds derived from marine microorganisms.
While previous reviews have primarily centered on symbiotic bacteria, to the best of our knowledge, none have yet highlighted the anti-inflammatory properties of these microorganisms. For this review, we selected 208 articles published from 2000 to 2024. One anterior reference was retained for the historical aspect of a specific molecule. The search engines Google Scholar, Science Direct, PubMed, and MarinLit databases were used with the keywords “marine natural products” combined with “anti-inflammatory”, “macro-organisms”, “microorganisms”, “clinical pipeline”, “clinical use”, and “bioactivities.” The database Worms (https://www.marinespecies.org/, accessed on 17 January 2024) was used to identify the species of marine organisms.

3. Marine Microorganisms vs. Macro-Organisms: Who Are the Actual Producers of Metabolites?

Oceans are a vast and unexplored world, teeming with life and diversity. Recent advancements in bioprospecting and molecular technologies foster the identification of new marine organisms, from macroscopic to microscopic biota, in this fascinating ecosystem [168]. However, the number of unknown marine species is estimated between 60,000 and 1,950,000, depending on the literature [169]. In the early days, bioprospecting campaigns focused on larger species like cnidarians, sponges, or soft corals due to technical limitations [170]. Between the 1990s and the 2010s, marine invertebrates have been found to produce almost 10,000 new marine natural products (MNPs) [171]. These discoveries have revealed the immense potential of marine organisms for developing innovative compounds for therapeutic and industrial applications. Many metabolites produced by marine macro-organisms have shown promising biological properties, such as anti-inflammatory activity for 43.7% of compounds (Figure 1a). These metabolites belong to different classes of molecules like terpenes (26%), alkaloids (20%), lipids (20%), pigments (8%), polysaccharides (6%) as shown in Figure 1b. Among macro-organisms, those belonging to the phylum Echinodermata produce the most anti-inflammatory molecules (Table 1), inhibiting pro-inflammatory cytokines and the NF-κB pathway but also reducing inflammation in vivo (Table 1). Since then, the possibility of further exploring and leveraging marine ecosystems has been genuinely exciting as it could unlock countless benefits for human health.
Figure 1. Chemical classification of MNPs with anti-inflammatory activity as reported between 2000 and 2024. Percentage of known anti-inflammatory compounds produced by marine organisms (a), by marine macro-organisms (b), and microorganisms (c) according to the structure type.
An ongoing exploration of marine ecosystems has extended to extreme environments such as deep ocean trenches, geographical poles, or hydrothermal vents; furthermore, technological improvement of microorganisms conservation during collects prompted bioprospecting campaigns to focus on microorganisms such as microalgae, marine fungi, cyanobacteria, and other groups of marine microorganisms. These microscopic life forms represent over 90% of the marine biomass and play a critical role in geochemical processes necessary for terrestrial life [172]. They are also remarkable for their ability to thrive, even in the harshest environments, producing rare and unique compounds that cannot be found in terrestrial biotopes. Furthermore, marine microorganisms are highly metabolically efficient, producing large amounts of metabolites while consuming limited energy [173]. Over the past year, MNPs obtained from marine bacteria, fungi, and cyanobacteria increased by 22%, 85%, and 61%, respectively, between 2018 and 2020, underscoring the impact of marine microorganisms on scientific research [174]. Yet, macro-organisms such as sponges and cnidarians have also been shown to produce MNPs [175]. The identification of these sources has led to inquiries and discussions about the actual producers of these metabolites.
Recent studies have uncovered that certain compounds previously thought to be specifically produced by marine macro-organisms are actually the metabolic byproducts of associated microorganisms [176], as illustrated by bryostatin, which has been confirmed to originate from microbes. The discovery of this metabolite has been made through the identification of polyketide synthase genes involved in its biosynthesis and found in the genome of the bryozoan bacterial symbiont Candidatus Endobugula sertula [177]. Another striking example is the fungus Penicilium canescens found in the ascidian Styela plicata, which exhibited anti-inflammatory activity. Furthermore, the findings presented in Figure 1a indicate that 58.3% of common anti-inflammatory classes of molecules are produced by both marine macro-organisms and microorganisms. This suggests that microorganisms may play a crucial role in producing these compounds, as many microorganisms live in symbiosis with macro-organisms.
In comparison with macro-organisms, microorganisms represent a significant source of anti-inflammatory molecules, contributing a noteworthy 56% of these compounds (Figure 1a). Moreover, the diversity of their metabolites is astounding, including terpenes (27%), alkaloids (18%), peptides (4%), lipids (2%), and pigments (1%) as indicated in Figure 1C. However, the most intriguing aspect is the specific type of molecules, such as polyketides (32%) and phenazine derivatives (4%) produced by marine fungi that target pro-inflammatory cytokines like TNF-α or IL-6, as well as inflammatory markers like NO (Table 1, Figure 2). Given that these mediators are produced upon activation of the NF-kB pathway or are involved in the activation of the JAK-STAT pathway, it is plausible that the MNPs derived from fungi may inhibit these pathways. Additionally, marine microorganisms, particularly bacteria, can produce specific compounds that are not found in macro-organisms. These compounds, such as exopolysaccharides, macrolides, and azirine, can target inflammatory mediators such as cyclooxygenases, NO, TNF-α, and the NF-κB pathway (Table 1, Figure 2). It is worth noting that among microorganisms, most of the compounds are produced by fungi, particularly those belonging to the Ascomycota phylum (Table 1). In addition, they are the major producers of polyketides, one of the specific molecules mentioned above. Furthermore, although most specific molecules targeted the NF-κB pathway (Table 1), their structural characteristics prompt consideration of whether their modes of action could reveal new pathways and targets for modulating inflammation, thus extending our understanding of the interplay between marine compounds and the inflammatory process. These results suggest that fungi could potentially serve as valuable sources of anti-inflammatory molecules.
Figure 2. Chemical structure of specific molecules produced by marine microorganisms according to their classification. Regarding polyketides, only a few molecules were presented for each specific target involved in inflammation.
Considering the vast potential of microorganisms in the production of anti-inflammatory compounds, further research must be conducted to unlock their full potential and develop new treatments for inflammatory diseases.

4. Challenges and Future Directions

Exploring the potential of marine microorganisms as anti-inflammatory agents presents a myriad of challenges and promising future opportunities. One significant challenge lies in the development of anti-inflammatory drugs derived from marine sources, which may encounter barriers impacting the speed and efficiency of the process. Additionally, regulatory hurdles could potentially impede the approval and commercialization of marine-derived pharmaceuticals for anti-inflammatory purposes. Scaling up the production of bioactive compounds from marine microorganisms to meet demand poses a significant challenge, while ensuring the cost-effectiveness of extracting and utilizing these compounds for anti-inflammatory therapies is a critical consideration. The intricate complexity of marine ecosystems and the vast diversity of microorganisms further address the challenges in identifying and isolating effective anti-inflammatory compounds.
Looking towards the future, the quest for potent and effective anti-inflammatory natural products from marine organisms requires ongoing and rigorous research. It is essential to explore innovative approaches in marine drug discovery to uncover new and promising anti-inflammatory compounds. In the future, efforts should be focused on optimizing the drug development process from marine sources to enhance its efficacy and speed. Collaboration among researchers, industry members, and regulatory bodies is crucial for advancing marine-based anti-inflammatory therapies. Furthermore, emphasizing sustainable harvesting practices for marine microorganisms intended for anti-inflammatory purposes is vital for ensuring long-term viability.
By addressing these challenges and focusing on future directions, we can unlock marine microorganisms’ full potential as valuable sources of anti-inflammatory agents, leading to significant advancements in healthcare and therapeutic treatments.

5. Conclusions

The inter-relations between microorganisms and macro-organisms are complex, ranging from parasitic to symbiotic systems. In this regard, metagenomic analysis offers major insights to decipher the complexity of a micro-environment comprising a macro-organism and its hosts without providing any clues as to which among the various interacting, living species is actually responsible for the synthesis of the bioactive metabolites (Figure 3). On the other hand, microbiota identification and microbial isolation from a macro-organism is an attractive alternative, enabling the isolation and identification of specific bacterial species, their culture, and, ultimately, the demonstration of their ability to produce compounds of pharmaceutical interest. Indeed, microorganisms have emerged as a promising avenue for drug discovery, offering a solution to the challenges posed by low quantities of secondary metabolites and the difficulty of obtaining sufficient biomass necessary for pharmaceutical companies to perform clinical trials. Bacterial or microalgal cultures can provide a continuous source of biomass production within a subsequent purification of bioactive metabolites. These steps could revolutionize drug discovery by making it also more environmentally friendly by reducing the exploitation of marine resources.
Figure 3. Metagenomic approach to discover the metabolites produced by the microbiota of marine macro-organisms. Two strategies are illustrated. In the top figure, whole metagenomics sequencing enables the identification of most species present in a microenvironment without driving the determination of a species/activity relationship. In the bottom part, microbiota isolation from the environment or macro-organisms leads to bacterial identification, specific culture, and a possible link between a metabolite and bioactivity.

Author Contributions

Conceptualization, M.L., P.G. and M.M.; writing—original draft preparation, M.L.; writing—review and editing, M.L., P.G., T.J. and M.M; supervision, M.M. All authors have read and agreed to the published version of the manuscript.

Funding

This study is supported by the French National Research Agency (ANR; project CHARM N°ANR-21-CE43-0015-01). ML and MM positions are financed by the ANR and by the Government of New Caledonia, respectively.

Data Availability Statement

All data in this review are openly available without any restrictions.

Acknowledgments

We are thankful to Catherine Vonthron-Sénéchau and to Cyril Antheaume (University of Strasbourg) for a critical reading of the first version of the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

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