Microbial Bioactives
Microbial Bioactives | Online ISSN 2209-2161
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Marine Sponge Microbiomes in Drug Discovery: Bioactive Secondary Metabolites, Symbiosis, Biosynthetic Gene Clusters, and Biotechnological Opportunities
V Vasanthabharathi 1 *, S Jayalakshmi 1
Microbial Bioactives 4 (1) 1-8 https://doi.org/10.25163/microbbioacts.4110712
Submitted: 22 March 2021 Revised: 18 May 2021 Accepted: 25 May 2021 Published: 27 May 2021
Abstract
Marine sponges harbor some of the most ancient and complex microbial symbioses known in the marine biosphere, and over time these partnerships appear to have evolved into remarkably productive biochemical systems. This review synthesizes current evidence regarding sponge-associated microbial diversity, biosynthetic potential, and the growing pharmaceutical relevance of marine sponge holobionts. Following PRISMA 2020-guided systematic screening and proportion-based meta-synthesis, the study integrates ecological, microbiological, and biochemical findings from studies investigating sponge-associated bacteria and fungi involved in secondary metabolite production. The compiled evidence demonstrates that sponge microbiomes consistently contain metabolically active microbial consortia dominated by Actinobacteria, Proteobacteria, and fungal Ascomycota, all of which contribute substantially to antimicrobial, antiviral, antitumor, and cytotoxic compound discovery. Comparative analyses revealed considerable variability in bioactive screening success across sponge hosts and microbial groups, yet positive biosynthetic activity remained consistently detectable throughout most studies. Forest and funnel plot interpretations further suggested biologically meaningful trends despite methodological heterogeneity. Advances in metagenomics, genome mining, and synthetic biology are gradually overcoming long-standing limitations associated with unculturable symbionts and limited compound supply. Collectively, the findings suggest that marine sponge–microbe symbioses function as evolutionarily stable reservoirs of chemically diverse natural products with major implications for future biotechnology and therapeutic development. At the same time, the review highlights unresolved ecological and translational challenges that continue to shape marine natural product research.
Keywords: Marine sponges; microbial symbiosis; sponge microbiome; secondary metabolites; natural products; drug discovery; biosynthetic gene clusters; marine biotechnology
References
Ang, K. K. H., Holmes, M. J., Higa, T., Hamann, M. T., & Kara, U. A. K. (2000). In vivo antimalarial activity of the beta-carboline alkaloid manzamine A. Antimicrobial Agents and Chemotherapy, 44(6), 1645–1649. https://pubmed.ncbi.nlm.nih.gov/10817722/ (PMC)
Baltz, R. H. (2008).Renaissance in antibacterial discovery from actinomycetes. Current Opinion in Pharmacology, 8(5), 557–563. https://pubmed.ncbi.nlm.nih.gov/18524678/ (PubMed)
Bérdy, J. (2005). Bioactive microbial metabolites: A personal view. The Journal of Antibiotics, 58(1), 1–26. https://doi.org/10.1038/ja.2005.1
Bergmann, W., & Burke, D. C. (1955). Contributions to the study of marine products. XXXIX. The nucleosides of sponges. III. Spongothymidine and spongouridine. The Journal of Organic Chemistry, 20(11), 1501–1507. https://doi.org/10.1021/jo01128a007
Borenstein, M., Hedges, L. V., Higgins, J. P. T., & Rothstein, H. R. (2009). Introduction to meta-analysis. Wiley. https://doi.org/10.1002/9780470743386
Bringmann, G., Lang, G., Gulder, T. A. M., Tsuruta, H., Mühlbacher, J., Maksimenka, K., & Müller, W. E. G. (2005). The first sorbicillinoid alkaloids from a sponge-derived Penicillium chrysogenum strain. Tetrahedron, 61(30), 7252–7265. https://doi.org/10.1016/j.tet.2005.05.026
Brinkmann, C. M., Marker, A., & Kurtböke, D. I. (2010). Biodiversity of marine sponges and associated microbes which have been reported to produce therapeutically important compounds. Marine Drugs, 8(4), 1417–1459.
DerSimonian, R., & Laird, N. (1986). Meta-analysis in clinical trials. Controlled Clinical Trials, 7(3), 177–188. https://doi.org/10.1016/0197-2456(86)90046-2
Duckworth, A. R., Battershill, C. N., & Bergquist, P. R. (1997).Influence of explant procedures and environmental factors on culture success of three sponges. Aquaculture, 156(3–4), 251–267. https://doi.org/10.1016/S0044-8486(97)00131-2
Egger, M., Davey Smith, G., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315(7109), 629–634. https://doi.org/10.1136/bmj.315.7109.629
Erwin, P. M., López-Legentil, S., González-Pech, R., & Turon, X. (2012).A specific mix of generalists: Bacterial symbionts in Mediterranean Ircinia spp. FEMS Microbiology Ecology, 79(3), 619–637. https://doi.org/10.1111/j.1574-6941.2011.01243.x
Esteves, A. I. S., Hardoim, C. C. P., Xavier, J. R., Gonçalves, J. M. S., & Costa, R. (2013). Molecular richness and biotechnological potential of bacteria cultured from Irciniidae sponges in the north-east Atlantic. FEMS Microbiology Ecology, 85(3), 519–536. https://doi.org/10.1111/1574-6941.12140
Feling, R. H., Buchanan, G. O., Mincer, T. J., Kauffman, C. A., Jensen, P. R., & Fenical, W. (2003).
Salinosporamide A: A highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus Salinispora. Angewandte Chemie International Edition, 42(3), 355–357. https://doi.org/10.1002/anie.200390115
Fieseler, L., Horn, M., Wagner, M., & Hentschel, U. (2004).Discovery of the candidate phylum “Poribacteria” in marine sponges. Applied and Environmental Microbiology, 70(6), 3724–3732. https://doi.org/10.1128/AEM.70.6.3724-3732.2004
Grasso, L. L., Martino, D. C., & Alduina, R. (2021). Production of antibacterial compounds from actinomycetes. Antibiotics, 10(4), 483.
Hardoim, C. C. P., & Costa, R. (2014). Microbial communities and bioactive compounds in marine sponges of the family Irciniidae—A review. Marine Drugs, 12(10), 5089–5122. https://doi.org/10.3390/md12105089
Hentschel, U., Usher, K. M., & Taylor, M. W. (2002).Marine sponges as microbial fermenters. FEMS Microbiology Ecology, 40(3), 191–203. https://doi.org/10.1111/j.1574-6941.2005.00046.x
Higgins, J. P. T., Thomas, J., Chandler, J., Cumpston, M., Li, T., Page, M. J., & Welch, V. A. (2022). Cochrane handbook for systematic reviews of interventions (Version 6.3). Cochrane. http://www.training.cochrane.org/handbook
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003). Measuring inconsistency in meta-analyses. BMJ, 327(7414), 557–560. https://doi.org/10.1136/bmj.327.7414.557
Jagannathan, P., Manemann, S. M., Rowe, M. P., Callender, G. G., & Soto, W. (2021).Marine actinomycetes: New sources of biotechnological products. Marine Drugs, 19(2), 1–18. https://doi.org/10.3390/md19070365
Li, C. W., Chen, J. Y., & Hua, T. E. (1998).Precambrian sponges with cellular structures. Science, 279(5352), 879–882. https://doi.org/10.1126/science.279.5352.879
Love, G. D., Grosjean, E., Stalvies, C., Fike, D. A., Grotzinger, J. P., Bradley, A. S., … & Summons, R. E. (2009).Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature, 457(7230), 718–721. https://doi.org/10.1038/nature07673
Osinga, R., Tramper, J., & Wijffels, R. H. (1999). Cultivation of marine sponges. Marine Biotechnology, 1(6), 509–532.https://doi.org/10.1007/PL00011807
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., et al. (2021). The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 372, n71. https://doi.org/10.1136/bmj.n71
Paz, Z., Komon-Zelazowska, M., Druzhinina, I. S., Aveskamp, M. M., Shnaiderman, A., Aluma, Y., Carmeli, S., Ilan, M., & Yarden, O. (2010). Diversity and potential antifungal properties of fungi associated with a Mediterranean sponge. Fungal Diversity, 42(1), 17–26. https://doi.org/10.1007/s13225-010-0020-x
Proksch, P., Edrada, R. A., & Ebel, R. (2002).Drugs from the seas: Current status and microbiological implications. Applied Microbiology and Biotechnology, 59(2–3), 125–134. https://doi.org/10.1007/s00253-002-1006-8
Rego, A., Raio, F., Martins, T. P., Ribeiro, H., Sousa, A. G. G., Séneca, J., Baptista, M. S., Lee, C. K., Cary, S. C., Ramos, V., et al. (2020). Metagenomic analysis of polyketide synthase and nonribosomal peptide synthetase genes in Antarctic soils. Microorganisms, 8(2), 279. https://doi.org/10.3390/microorganisms8020279
Rinkevich, B. (2005).Marine invertebrate cell cultures: New millennium trends. Marine Biotechnology, 7(5), 429–439. https://doi.org/10.1007/s10126-004-0108-y
Santos-Aberturas, J., & Vior, N. M. (2022). Beyond soil-dwelling Actinobacteria: Fantastic antibiotics and where to find them. Antibiotics, 11(2), 195. https://doi.org/10.3390/antibiotics11020195
Schmitt, S., Weisz, J. B., Lindquist, N., & Hentschel, U. (2007).Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Applied and Environmental Microbiology, 73(7), 2067–2078. https://doi.org/10.1128/AEM.01944-06
Siegl, A., & Hentschel, U. (2010). PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environmental Microbiology Reports, 2(4), 507–513. https://doi.org/10.1111/j.1758-2229.2009.00057.x
Sipkema, D., Osinga, R., Schatton, W., Mendola, D., Tramper, J., & Wijffels, R. H. (2005). Large-scale production of pharmaceuticals by marine sponges: Sea, cell, or synthesis? Marine Biotechnology, 7(2), 142-162. https://doi.org/10.1007/s10126-004-0405-5
Spalding, M. D., Fox, H. E., Allen, G. R., Davidson, N., Ferdaña, Z. A., Finlayson, M., … & Robertson, J. (2007). Marine ecoregions of the world: A bioregionalization of coastal and shelf areas. BioScience, 57(7), 573-583. https://doi.org/10.1641/B570707
Taylor, M. W., Radax, R., Steger, D., & Wagner, M. (2007). Sponge associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiology and Molecular Biology Reviews, 71(2), 295-347. https://doi.org/10.1128/MMBR.00040-06
Thakur, N., Anil, A., & Müller, W. (2004). Culturable epibacteria of the marine sponge Ircinia fusca: Temporal variations and their possible role in the epibacterial defense of the host. Aquatic Microbial Ecology, 37(3), 295–304. https://doi.org/10.3354/ame037295
Thomas, T., Kavlekar, D. P., & LokaBharathi, P. A. (2010). Marine drugs from sponge-microbe association-a review. Marine Drugs, 8(4), 1417-1468. https://doi.org/10.3390/md8041417
Tong, Y., Charusanti, P., Zhang, L., Weber, T., & Lee, S. Y. (2015). CRISPR-Cas9 based engineering of actinomycetal genomes. ACS Synthetic Biology, 4(9), 1020-1029. https://doi.org/10.1021/acssynbio.5b00038
Van Soest, R. W. M., Boury-Esnault, N., Hooper, J. N. A., Rützler, K., de Voogd, N. J., Alvarez, B., … & Dohrmann, M. (2012). Global diversity of sponges (Porifera). PLoS ONE, 7(4), e35105. https://doi.org/10.1371/journal.pone.0035105
Wang, G. (2006). Diversity and biotechnological potential of sponge associated microbial consortia. Journal of Industrial Microbiology & Biotechnology, 33(7), 545-551. https://doi.org/10.1007/s10295-006-0123-2
Webster, N. S., & Taylor, M. W. (2012). Marine sponges and their microbial symbionts: Love and other relationships. Environmental Microbiology, 14(2), 335-346. https://doi.org/10.1111/j.1462-2920.2011.02460.x
Wilkinson, C. R. (1978). Microbial associations in sponges. II. Numerical-analysis of sponge and water bacterial populations. Marine Biology, 49(2), 169–176.
Zan, J. D., Fuqua, C., & Hill, R. T. (2011). Diversity and functional analysis of luxS genes in vibrios from marine sponges Mycale laxissima and Ircinia strobilina. The ISME Journal, 5(9), 1505–1516. https://doi.org/10.1038/ismej.2011.31
Zhang, Y., Mu, J., Feng, Y., Kang, Y., Zhang, J., Gu, P., Wang, Y., Ma, L., & Zhu, Y. (2005). Broad-spectrum antimicrobial activity of marine bacteria associated with the sponge Hymeniacidon perleve. World Journal of Microbiology and Biotechnology, 21(2), 201–206. https://doi.org/10.1007/s11274-004-3318-6
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