Reef Ecology and Marine Drug Discovery

A special issue of Marine Drugs (ISSN 1660-3397). This special issue belongs to the section "Marine Chemoecology for Drug Discovery".

Deadline for manuscript submissions: closed (31 December 2022) | Viewed by 30486

Special Issue Editors


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Guest Editor
Institute for Bioengineering and Biosciences (iBB), Instituto Superior Técnico (IST), Universidade de Lisboa, 1049-001 Lisbon, Portugal
Interests: bacterial evolution; blue bioeconomy; community and conservation ecology; comparative genomics; data science; host-microbiome interactions; secondary metabolism

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Guest Editor
Institute for Bioengineering and Biosciences (iBB), Instituto Superior Técnico (IST), Universidade de Lisboa, 1049-001 Lisbon, Portugal
Interests: microbial & chemical ecology; blue biotechnology; symbiosis; metagenomics; coral microbiomes

Special Issue Information

Dear Colleagues,

Marine reefs are among the most productive and diverse ecosystems on our planet, sustaining marine wildlife and hundreds of millions of people. Reef organisms such as cnidarians, sponges, bryozoans, tunicates, and echinoderms, together with an abundance of symbiotic and free-living algae, fungi, and prokaryotes, are amidst the most prolific producers of bioactive compounds of reefs and marine environments at large. Their natural products often show astounding structural novelty and chemical complexity, encompassing a large variety of terpenes, steroids, alkaloids, polyketides, and nonribosomal peptides. They facilitate chemically mediated behaviours and interspecies interactions from competition to cooperation. They also help to prevent overgrowth and predation of marine invertebrates, which play fundamental roles in nutrient cycling and community assembly in benthic ecosystems. There is indeed great potential for a minimally invasive and economically reliable retrieval of bioactive secondary metabolites from the highly diverse and chemically complex communities inhabiting reefs.

We cordially invite the scientific community to contribute original research or review articles on the chemical and microbial ecology of reef organisms and their potential for sustainable development of marine drugs. We welcome contributions on free-living or symbiotic macro- and microorganisms. Studies may be driven by bioactivity screenings, genomics, metabolomics, and/or structure elucidation. Ecological studies focussing on metabolic crosstalk in reefs and marine settings are also encouraged, as well as viewpoints on how the sustainable exploitation of natural products can promote the conservation and responsible stewardship of reef ecosystems.

Prof. Dr. Rodrigo Costa
Dr. Tina Keller-Costa
Guest Editors

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Keywords

  • reef organisms
  • chemical ecology
  • secondary metabolism
  • bioactive compounds
  • metabolomics
  • drug discovery
  • blue biotechnology
  • host-microbe interactions
  • cnidarians
  • marine sponges
  • sustainable reef exploitation

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Published Papers (8 papers)

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Research

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25 pages, 1714 KiB  
Article
Gambierone and Sodium Channel Specific Bioactivity Are Associated with the Extracellular Metabolite Pool of the Marine Dinoflagellate Coolia palmyrensis
by Alexander K. Leynse, Elizabeth M. Mudge, Andrew D. Turner, Benjamin H. Maskrey and Alison Robertson
Mar. Drugs 2023, 21(4), 244; https://doi.org/10.3390/md21040244 - 15 Apr 2023
Viewed by 2209
Abstract
Tropical epibenthic dinoflagellate communities produce a plethora of bioactive secondary metabolites, including the toxins ciguatoxins (CTXs) and potentially gambierones, that can contaminate fishes, leading to ciguatera poisoning (CP) when consumed by humans. Many studies have assessed the cellular toxicity of causative dinoflagellate species [...] Read more.
Tropical epibenthic dinoflagellate communities produce a plethora of bioactive secondary metabolites, including the toxins ciguatoxins (CTXs) and potentially gambierones, that can contaminate fishes, leading to ciguatera poisoning (CP) when consumed by humans. Many studies have assessed the cellular toxicity of causative dinoflagellate species to better understand the dynamics of CP outbreaks. However, few studies have explored extracellular toxin pools which may also enter the food web, including through alternative and unanticipated routes of exposure. Additionally, the extracellular exhibition of toxins would suggest an ecological function and may prove important to the ecology of the CP-associated dinoflagellate species. In this study, semi-purified extracts obtained from the media of a Coolia palmyrensis strain (DISL57) isolated from the U.S. Virgin Islands were assessed for bioactivity via a sodium channel specific mouse neuroblastoma cell viability assay and associated metabolites evaluated by targeted and non-targeted liquid chromatography tandem and high-resolution mass spectrometry. We found that extracts of C. palmyrensis media exhibit both veratrine enhancing bioactivity and non-specific bioactivity. LC-HR-MS analysis of the same extract fractions identified gambierone and multiple undescribed peaks with mass spectral characteristics suggestive of structural similarities to polyether compounds. These findings implicate C. palmyrensis as a potential contributor to CP and highlight extracellular toxin pools as a potentially significant source of toxins that may enter the food web through multiple exposure pathways. Full article
(This article belongs to the Special Issue Reef Ecology and Marine Drug Discovery)
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18 pages, 2998 KiB  
Article
Cryptic Diversity of Black Band Disease Cyanobacteria in Siderastrea siderea Corals Revealed by Chemical Ecology and Comparative Genome-Resolved Metagenomics
by Julie L. Meyer, Sarath P. Gunasekera, Anya L. Brown, Yousong Ding, Stephanie Miller, Max Teplitski and Valerie J. Paul
Mar. Drugs 2023, 21(2), 76; https://doi.org/10.3390/md21020076 - 22 Jan 2023
Cited by 7 | Viewed by 4853
Abstract
Black band disease is a globally distributed and easily recognizable coral disease. Despite years of study, the etiology of this coral disease, which impacts dozens of stony coral species, is not completely understood. Although black band disease mats are predominantly composed of the [...] Read more.
Black band disease is a globally distributed and easily recognizable coral disease. Despite years of study, the etiology of this coral disease, which impacts dozens of stony coral species, is not completely understood. Although black band disease mats are predominantly composed of the cyanobacterial species Roseofilum reptotaenium, other filamentous cyanobacterial strains and bacterial heterotrophs are readily detected. Through chemical ecology and metagenomic sequencing, we uncovered cryptic strains of Roseofilum species from Siderastrea siderea corals that differ from those on other corals in the Caribbean and Pacific. Isolation of metabolites from Siderastrea-derived Roseofilum revealed the prevalence of unique forms of looekeyolides, distinct from previously characterized Roseofilum reptotaenium strains. In addition, comparative genomics of Roseofilum strains showed that only Siderastrea-based Roseofilum strains have the genetic capacity to produce lasso peptides, a family of compounds with diverse biological activity. All nine Roseofilum strains examined here shared the genetic capacity to produce looekeyolides and malyngamides, suggesting these compounds support the ecology of this genus. Similar biosynthetic gene clusters are not found in other cyanobacterial genera associated with black band disease, which may suggest that looekeyolides and malyngamides contribute to disease etiology through yet unknown mechanisms. Full article
(This article belongs to the Special Issue Reef Ecology and Marine Drug Discovery)
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28 pages, 6086 KiB  
Article
Marine Sponge and Octocoral-Associated Bacteria Show Versatile Secondary Metabolite Biosynthesis Potential and Antimicrobial Activities against Human Pathogens
by João F. Almeida, Matilde Marques, Vanessa Oliveira, Conceição Egas, Dalila Mil-Homens, Romeu Viana, Daniel F. R. Cleary, Yusheng M. Huang, Arsénio M. Fialho, Miguel C. Teixeira, Newton C. M. Gomes, Rodrigo Costa and Tina Keller-Costa
Mar. Drugs 2023, 21(1), 34; https://doi.org/10.3390/md21010034 - 30 Dec 2022
Cited by 7 | Viewed by 5382
Abstract
Marine microbiomes are prolific sources of bioactive natural products of potential pharmaceutical value. This study inspected two culture collections comprising 919 host-associated marine bacteria belonging to 55 genera and several thus-far unclassified lineages to identify isolates with potentially rich secondary metabolism and antimicrobial [...] Read more.
Marine microbiomes are prolific sources of bioactive natural products of potential pharmaceutical value. This study inspected two culture collections comprising 919 host-associated marine bacteria belonging to 55 genera and several thus-far unclassified lineages to identify isolates with potentially rich secondary metabolism and antimicrobial activities. Seventy representative isolates had their genomes mined for secondary metabolite biosynthetic gene clusters (SM-BGCs) and were screened for antimicrobial activities against four pathogenic bacteria and five pathogenic Candida strains. In total, 466 SM-BGCs were identified, with antimicrobial peptide- and polyketide synthase-related SM-BGCs being frequently detected. Only 38 SM-BGCs had similarities greater than 70% to SM-BGCs encoding known compounds, highlighting the potential biosynthetic novelty encoded by these genomes. Cross-streak assays showed that 33 of the 70 genome-sequenced isolates were active against at least one Candida species, while 44 isolates showed activity against at least one bacterial pathogen. Taxon-specific differences in antimicrobial activity among isolates suggested distinct molecules involved in antagonism against bacterial versus Candida pathogens. The here reported culture collections and genome-sequenced isolates constitute a valuable resource of understudied marine bacteria displaying antimicrobial activities and potential for the biosynthesis of novel secondary metabolites, holding promise for a future sustainable production of marine drug leads. Full article
(This article belongs to the Special Issue Reef Ecology and Marine Drug Discovery)
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17 pages, 1919 KiB  
Article
Antimicrobial Biosynthetic Potential and Phylogenetic Analysis of Culturable Bacteria Associated with the Sponge Ophlitaspongia sp. from the Yellow Sea, China
by Lei Chen, Xue-Ning Wang, Hong-Yu Bi and Guang-Yu Wang
Mar. Drugs 2022, 20(10), 588; https://doi.org/10.3390/md20100588 - 21 Sep 2022
Cited by 3 | Viewed by 2495
Abstract
Sponge-derived bacteria are considered to be a promising source of novel drugs, owing to their abundant secondary metabolites that have diverse biological activities. In this study, we explored the antimicrobial biosynthetic potential and phylogenetics of culturable bacteria associated with the sponge Ophlitaspongia sp. [...] Read more.
Sponge-derived bacteria are considered to be a promising source of novel drugs, owing to their abundant secondary metabolites that have diverse biological activities. In this study, we explored the antimicrobial biosynthetic potential and phylogenetics of culturable bacteria associated with the sponge Ophlitaspongia sp. from the Yellow Sea, China. Using culture-dependent methods, we obtained 151 bacterial strains, which were then analysed for their antimicrobial activities against seven indicator strains. The results indicate that 94 (62.3%) of the 151 isolated strains exhibited antimicrobial activities and inhibited at least one of the indicator strains. Fifty-two strains were selected for further phylogenetic analysis using 16S rRNA gene sequencing, as well as for the presence of polyketide synthase (PKS) and non-ribosomal peptide synthetase (NRPS) genes. These 52 strains belonged to 20 genera from 18 families in 4 phyla, including Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria. Five strains with PKS genes and ten strains with NRPS genes were detected. Among them, two strains contained both PKS and NRPS genes. Notoacmeibacter sp. strain HMA008 (class Alphaproteobacteria) exhibited potent antimicrobial activity; thus, whole genome sequencing methods were used to analyse its secondary metabolite biosynthetic gene clusters. The genome of HMA008 contained 12 biosynthetic gene clusters that potentially encode secondary metabolites belonging to compound classes such as non-ribosomal peptides, prodigiosin, terpene, β-lactones, and siderophore, among others. This study indicates that the sponge Ophlitaspongia sp. harbours diverse bacterial strains with antimicrobial properties and may serve as a potential source of bioactive compounds. Full article
(This article belongs to the Special Issue Reef Ecology and Marine Drug Discovery)
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17 pages, 887 KiB  
Article
Coral Holobionts Possess Distinct Lipid Profiles That May Be Shaped by Symbiodiniaceae Taxonomy
by Tatyana V. Sikorskaya, Ekaterina V. Ermolenko, Kseniya V. Efimova and Ly T. P. Dang
Mar. Drugs 2022, 20(8), 485; https://doi.org/10.3390/md20080485 - 28 Jul 2022
Cited by 6 | Viewed by 2661
Abstract
Symbiotic relationships are very important for corals. Abiotic stressors cause the acclimatization of cell membranes in symbionts, which possess different membrane acclimatization strategies. Membrane stability is determined by a unique lipid composition and, thus, the profile of thylakoid lipids can depend on coral [...] Read more.
Symbiotic relationships are very important for corals. Abiotic stressors cause the acclimatization of cell membranes in symbionts, which possess different membrane acclimatization strategies. Membrane stability is determined by a unique lipid composition and, thus, the profile of thylakoid lipids can depend on coral symbiont species. We have analyzed and compared thylakoid lipidomes (mono- and digalactosyldiacylglycerols (MGDG and DGDG), sulfoquinovosyldiacylglycerols (SQDG), and phosphatidylglycerols (PG)) of crude extracts from symbiotic reef-building coral Acropora sp., the hydrocoral Millepora platyphylla, and the octocoral Sinularia flexibilis. S. flexibilis crude extracts were characterized by a very high SQDG/PG ratio, a DGDG/MGDG ratio < 1, a lower degree of galactolipid unsaturation, a higher content of SQDG with polyunsaturated fatty acids, and a thinner thylakoid membrane which may be explained by the presence of thermosensitive dinoflagellates Cladocopium C3. In contrast, crude extracts of M. platyphylla and Acropora sp. exhibited the lipidome features of thermotolerant Symbiodiniaceae. M. platyphylla and Acropora sp. colonies contained Cladocopium C3u and Cladocopium C71/C71a symbionts, respectively, and their lipidome profiles showed features that indicate thermotolerance. We suggest that an association with symbionts that exhibit the thermotolerant thylakoid lipidome features, combined with a high Symbiodiniaceae diversity, may facilitate further acclimatization/adaptation of M. platyphylla and Acropora sp. holobionts in the South China Sea. Full article
(This article belongs to the Special Issue Reef Ecology and Marine Drug Discovery)
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27 pages, 4173 KiB  
Article
Insights into the Antimicrobial Activities and Metabolomes of Aquimarina (Flavobacteriaceae, Bacteroidetes) Species from the Rare Marine Biosphere
by Sandra Godinho Silva, Patrícia Paula, José Paulo da Silva, Dalila Mil-Homens, Miguel Cacho Teixeira, Arsénio Mendes Fialho, Rodrigo Costa and Tina Keller-Costa
Mar. Drugs 2022, 20(7), 423; https://doi.org/10.3390/md20070423 - 28 Jun 2022
Cited by 16 | Viewed by 4422
Abstract
Two novel natural products, the polyketide cuniculene and the peptide antibiotic aquimarin, were recently discovered from the marine bacterial genus Aquimarina. However, the diversity of the secondary metabolite biosynthetic gene clusters (SM-BGCs) in Aquimarina genomes indicates a far greater biosynthetic potential. In [...] Read more.
Two novel natural products, the polyketide cuniculene and the peptide antibiotic aquimarin, were recently discovered from the marine bacterial genus Aquimarina. However, the diversity of the secondary metabolite biosynthetic gene clusters (SM-BGCs) in Aquimarina genomes indicates a far greater biosynthetic potential. In this study, nine representative Aquimarina strains were tested for antimicrobial activity against diverse human-pathogenic and marine microorganisms and subjected to metabolomic and genomic profiling. We found an inhibitory activity of most Aquimarina strains against Candida glabrata and marine Vibrio and Alphaproteobacteria species. Aquimarina sp. Aq135 and Aquimarina muelleri crude extracts showed particularly promising antimicrobial activities, amongst others against methicillin-resistant Staphylococcus aureus. The metabolomic and functional genomic profiles of Aquimarina spp. followed similar patterns and were shaped by phylogeny. SM-BGC and metabolomics networks suggest the presence of novel polyketides and peptides, including cyclic depsipeptide-related compounds. Moreover, exploration of the ‘Sponge Microbiome Project’ dataset revealed that Aquimarina spp. possess low-abundance distributions worldwide across multiple marine biotopes. Our study emphasizes the relevance of this member of the microbial rare biosphere as a promising source of novel natural products. We predict that future metabologenomics studies of Aquimarina species will expand the spectrum of known secondary metabolites and bioactivities from marine ecosystems. Full article
(This article belongs to the Special Issue Reef Ecology and Marine Drug Discovery)
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15 pages, 1465 KiB  
Article
Not Drug-like, but Like Drugs: Cnidaria Natural Products
by Claire Laguionie-Marchais, A. Louise Allcock, Bill J. Baker, Ellie-Ann Conneely, Sarah G. Dietrick, Fiona Kearns, Kate McKeever, Ryan M. Young, Connor A. Sierra, Sylvia Soldatou, H. Lee Woodcock and Mark P. Johnson
Mar. Drugs 2022, 20(1), 42; https://doi.org/10.3390/md20010042 - 30 Dec 2021
Cited by 6 | Viewed by 3969
Abstract
Phylum Cnidaria has been an excellent source of natural products, with thousands of metabolites identified. Many of these have not been screened in bioassays. The aim of this study was to explore the potential of 5600 Cnidaria natural products (after excluding those known [...] Read more.
Phylum Cnidaria has been an excellent source of natural products, with thousands of metabolites identified. Many of these have not been screened in bioassays. The aim of this study was to explore the potential of 5600 Cnidaria natural products (after excluding those known to derive from microbial symbionts), using a systematic approach based on chemical space, drug-likeness, predicted toxicity, and virtual screens. Previous drug-likeness measures: the rule-of-five, quantitative estimate of drug-likeness (QED), and relative drug likelihoods (RDL) are based on a relatively small number of molecular properties. We augmented this approach using reference drug and toxin data sets defined for 51 predicted molecular properties. Cnidaria natural products overlap with drugs and toxins in this chemical space, although a multivariate test suggests that there are some differences between the groups. In terms of the established drug-likeness measures, Cnidaria natural products have generally lower QED and RDL scores than drugs, with a higher prevalence of metabolites that exceed at least one rule-of-five threshold. An index of drug-likeness that includes predicted toxicity (ADMET-score), however, found that Cnidaria natural products were more favourable than drugs. A measure of the distance of individual Cnidaria natural products to the centre of the drug distribution in multivariate chemical space was related to RDL, ADMET-score, and the number of rule-of-five exceptions. This multivariate similarity measure was negatively correlated with the QED score for the same metabolite, suggesting that the different approaches capture different aspects of the drug-likeness of individual metabolites. The contrasting of different drug similarity measures can help summarise the range of drug potential in the Cnidaria natural product data set. The most favourable metabolites were around 210–265 Da, quite often sesquiterpenes, with a moderate degree of complexity. Virtual screening against cancer-relevant targets found wide evidence of affinities, with Glide scores <−7 in 19% of the Cnidaria natural products. Full article
(This article belongs to the Special Issue Reef Ecology and Marine Drug Discovery)
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Review

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19 pages, 3125 KiB  
Review
The Soft Coral Sarcophyton trocheliophorum: A Warehouse of Terpenoids with Structural and Pharmacological Diversity
by Qi-Bin Yang, Qihao Wu, Jun-Kun Chen and Lin-Fu Liang
Mar. Drugs 2023, 21(1), 30; https://doi.org/10.3390/md21010030 - 29 Dec 2022
Cited by 4 | Viewed by 2418
Abstract
The soft coral Sarcophyton trocheliophorum, which was frequently encountered on Indo-Pacific and Red Sea coral reefs, furnished a wealth of secondary metabolites. Notably, terpenoids dominated the chemical profile of this species. In this review, we summarized the discovery of 156 terpenoids from [...] Read more.
The soft coral Sarcophyton trocheliophorum, which was frequently encountered on Indo-Pacific and Red Sea coral reefs, furnished a wealth of secondary metabolites. Notably, terpenoids dominated the chemical profile of this species. In this review, we summarized the discovery of 156 terpenoids from the soft coral S. trocheliophorum specimens in different geographical areas. The structures comprised 13 terpenoidal classes with various functionalities. We covered the era from the first report of S. trocheliophorum-derived metabolites in 1976 up to October 2022. The biological effects of these chemical compositions on a vast array of potential pharmacological activities such as protein tyrosine phosphatase 1B (PTP1B) inhibitory, neuroprotective, cytotoxic, anti-inflammatory, antibacterial, antivirus, and immunomodulatory activities were also presented. This review also revealed an immense demand to explore the terpene biosynthetic gene clusters of this species besides the chemo- and bio-investigations. Full article
(This article belongs to the Special Issue Reef Ecology and Marine Drug Discovery)
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