First Record on Microbial Colonies in Freshwater Sponges in East Java, Indonesia, and Their Estimated Pollutant Degradation Genes

  • Edwin Setiawan Department of Biology, Institut Teknologi Sepuluh Nopember, Kampus ITS Sukolilo, Surabaya, Indonesia, 60111 https://orcid.org/0000-0003-3947-3334
  • Michael Einstein Hermanto Postgraduate Alumni of Biology Department, Institut Teknologi Sepuluh Nopember, Kampus ITS Sukolilo, Surabaya, Indonesia, 60111
  • Ahmad Yanuar PT. Milieu Elang Abadi, Pondok Wage Indah II Waru, Sidoarjo 61257, Indonesia
  • Catur Riani School of Pharmacy, Institut Teknologi Bandung, Jl. Ganesa No.10 Bandung, Indonesia, 40132
  • Wuttichai Mhuanthong National Center for Genetic Engineering and Biotechnology (BIOTEC) | BioTec. Bioresources Technology Unit, Thailand
  • Fitra Adi Prayogo Biomedical Sciences Study Program, Karya Husada University, Jl. R. Kompol Soekanto No.46, Semarang, Indonesia, 50276 https://orcid.org/0000-0003-4354-2654
  • Dyah Wulandari Food Technology Department, Faculty of Agricultural Technology, Soegijapranata Catholic University (SCU), UNIKA Semarang, Indonesia, 50219 https://orcid.org/0000-0003-0923-8317
  • Anto Budiharjo Molecular and Applied Microbiology Laboratory, Central Laboratory of Research and Service, Diponegoro University, Jl. Prof. Sudharto SH, Semarang, Indonesia, 58275; Biotechnology Study Program, Faculty of Science and Mathematics, Diponegoro University, Jl. Prof. Soedarto, SH, Semarang, Indonesia, 50275 https://orcid.org/0000-0002-4815-5138
  • Laurensius M. Jackie Department of Biology, Faculty of Science and Mathematics, Diponegoro University, Jl. Prof. Soedarto, SH, Semarang, Indonesia, 50275
Keywords: East Java Indonesia, Eunapius carteri, Oncosclera asiatica, Freshwater sponges, Microbial colonies

Abstract

Sponges are known to harbor diverse and abundant microbial colonies. Nevertheless, studies on the diversity and abundance of microbial colonies in freshwater sponges have not been as extensive as those of marine sponges. This study investigates the microbial colonies of two freshwater sponge species, Eunapius carteri and Oncosclera asiatica, from the Kaliporong River in Indonesia. High microbial diversity was observed, with E. carteri harboring over 1,400 unique microbial species (Operational Taxonomic Units or OTUs) and O. asiatica hosting over 400. Proteobacteria were the dominant bacterial group in both sponges, comprising over 90 % of O. asiatica and over 50 % in E. carteri colonies. Functional profiling revealed a high potential for xenobiotic degradation in both sponge species, particularly through pathways involving Cytochrome P450 and the degradation of benzoate, caprolactam, and aminobenzoate. O. asiatica shows more of these degradation pathways than E. carteri. For example, benzoate degradation, involving over 60 genes or enzymes, was more pervasive in O. asiatica (5.81 %) than in E. carteri (5.03 %). These findings highlight the significant role of freshwater sponges in supporting diverse microbial populations with potential for bioremediation, particularly in polluted environments like the Kaliporong River. Further research is needed to understand the specific functions of these microbial colonies in freshwater sponges and their impact on the ecosystem.

References

Adamska, M., 2016. Sponges as models to study emergence of complex animals. Current Opinion in Genetics & Development, 39, pp.21-28. doi: 10.1016/j.gde.2016.05.026.

Aisami, A. & Gusmanizar, N., 2019. Characterization of an acrylamide-degrading bacterium isolated from hydrocarbon sludge. Bioremediation Science and Technology Research, 7(2), pp.15-19. doi: 10.54987/bstr.v7i2.487

Allocati, N. et al., 2018. Glutathione transferases: substrates, inihibitors and pro-drugs in cancer and neurodegenerative diseases. Oncogenesis, 7, 8. doi: 10.1038/s41389-017-0025-3.

Alviz-Gazitua, P. et al., 2022. Cupriavidus metallidurans CH34 possesses aromatic catabolic versatility and degrades benzene in the presence of mercury and cadmium. Microorganisms, 10(2), 484. doi: 10.3390/microorganisms10020484

Anayo, O.F. et al., 2019. The Beneficial Roles of Pseudomonas in Medicine, Industries, and Environment: A Review. In Pseudomonas Aeruginosa - An Armory Within. IntechOpen. doi: 10.5772/intechopen.85996.

Arora, P.K., 2015. Bacterial degradation of monocyclic aromatic amines. Frontiers in Microbiology, 6, 820. doi: 10.3389/fmicb.2015.00820.

Baker, B.J. et al., 2015. Genomic resolution of linkages in carbon, nitrogen, and sulfur cycling among widespread estuary sediment bacteria. Microbiome, 3, 14. doi: 10.1186/s40168-015-0077-6.

Cassier-Chauvat, C. et al., 2023. The Glutathione System: A Journey from Cyanobacteria to Higher Eukaryotes. Antioxidants, 12, 1199. doi: 10.3390/antiox12061199

Chaix, G. et al., 2017. Distinct Aeromonas Populations in Water Column and Associated with Copepods from Estuarine Environment (Seine, France). Frontiers in Microbiology, 8, 1259. doi: 10.3389/fmicb.2017.01259.

de Voogd, N.J. et al., 2024. World Porifera Database, viewed 5 January 2025, from https://www.marinespecies.org/porifera.

Douglas, G.M. et al., 2020. PICRUSt2 for prediction of metagenome functions. Nature Biotechnology, 38(6), pp.685-688. doi: 10.1038/s41587-020-0548-6.

Edgar, R.C., 2016. UCHIME2: improved chimera prediction for amplicon sequencing. BioRxiv, 12, 074252. doi: 10.1101/074252

Ferreira, M.R.S. et al., 2020. Geographical location and habitat predict variation in prokaryotic community composition of Suberites diversicolor. Annals of Microbiology, 70, 14. doi: 10.1186/s13213-020-01546-z.

Feuda, R. et al., 2017. Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals. Current Biology, 27, pp.3864-3870. doi: 10.1016/j.cub.2017.11.008.

Francis, B. et al., 2021. North Sea spring bloom-associated Gammaproteobacteria fill diverse heterotrophic niches. Environmental Microbiome, 16, 15. doi: 10.1186/s40793-021-00385-y.

Gaikwad, S., Shouche, Y.S. & Gade, W.N., 2016. Microbial community structure of two freshwater sponges using Illumina MiSeq sequencing revealed high microbial diversity. AMB Express, 6, 40. doi: 10.1186/s13568-016-0211-2.

Gloeckner, V. et al., 2014. The HMA-LMA dichotomy revisited: an electron microscopical survey of 56 sponge species. The Biological Bulletin, 227, pp.78-88. doi: 10.1086/BBLv227n1p78.

Greule, A. et al., 2018. Unrivalled diversity: the many roles and reactions of bacterial cytochromes P450 in secondary metabolism. Natural Product Reports, 35, pp.757-791. doi: 10.1039/c7np00063d.

Gugliandolo, C. et al., 2008. Pathogenic Vibrio, Aeromonas and Arcobacter spp. associated with copepods in the Straits of Messina (Italy). Marine Pollution Bulletin, 56, pp.600-606. doi: 10.1016/j.marpolbul.2007.12.001

Hall, C. et al., 2021. Freshwater sponge hosts and their green algae symbionts: a tractable model to understand intracellular symbiosis. PeerJ, 9, e10654. doi: 10.7717/peerj.10654.

Hill, M.S. & Sacristán-Soriano, O., 2017. Molecular and Functional Ecology of Sponges and Their Microbial Symbionts. In Climate Change, Ocean Acidification and Sponges: Impacts Across Multiple Levels of Organization. Cham: Springer, pp.105-142. doi: 10.1007/978-3-319-59008-0_5.

Keller-Costa, T. et al., 2014. The freshwater sponge Ephydatia fluviatilis harbours diverse Pseudomonas species (Gammaproteobacteria, Pseudomonadales) with broad-spectrum antimicrobial activity. PLoS ONE, 9, e88429. doi: 10.1371/journal.pone.0088429

Kelly, S.L. & Kelly, D.E., 2013. Microbial cytochromes P450: biodiversity and biotechnology. Where do cytochromes P450 come from, what do they do and what can they do for us? Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1612), 20120476. doi: 10.1098/rstb.2012.0476.

Kenny, N.J. et al., 2019. Symbiosis, Selection, and Novelty: Freshwater Adaptation in the Unique Sponges of Lake Baikal. Molecular Biology and Evolution, 36, pp.2462-2480. doi: 10.1093/molbev/msz151.

Kunakom, S. et al., 2023. Cytochromes P450 involved in bacterial RiPP biosyntheses. Journal of Industrial Mirobiology and Biotechnology, 50(1), kuad005. doi: 10.1093/jimb/kuad005.

Laport, M.S., Pinheiro, U. & Rachid, C.T.C.D.C., 2019. Freshwater Sponge Tubella variabilis Presents Richer Microbiota Than Marine Sponge Species. Frontiers in Microbiology, 10, 2799. doi: 10.3389/fmicb.2019.02799.

Lo Giudice, A. & Rizzo, C., 2024. Freshwater Sponges as a Neglected Reservoir of Bacterial Biodiversity. Microorganisms, 12(1), 25 doi: 10.3390/microorganisms12010025.

Manconi, R. & Pronzato, R., 2016. How to survive and persist in temporary freshwater? Adaptive traits of sponges (Porifera: Spongillida): A review. Hydrobiologia, 782, pp. 11-22. doi: 10.1007/s10750-016-2714-x.

Moitinho-Silva, L. et al., 2017. Predicting the HMA-LMA Status in Marine Sponges by Machine Learning. Frontiers in Microbiology, 8, 752. doi: 10.3389/fmicb.2017.00752.

Muñoz-García, A. et al., 2019. Influence of salinity on the degradation of xenobiotic compounds in rhizospheric mangrove soil. Environmental Pollution, 249, pp.750-757. doi: 10.1016/j.envpol.2019.03.056.

Nanjani, S. et al., 2022. Transcriptome profiling reveals upregulation of benzoate degradation and related genes in Pseudomonas aeruginosa D6 during textile dye degradation. Environmental Research, 212, 113288. doi: 10.1016/j.envres.2022.113288.

Narainsamy, K. et al., 2016. Oxidative‐stress detoxification and signalling in cyanobacteria: The crucial glutathione synthesis pathway supports the production of ergothioneine and ophthalmate. Molecular Microbiology, 100(1), pp.15-24. doi: 10.1111/mmi.13296

Nikrad, M.P., Cottrell, M.T. & Kirchman, D.L., 2014. Uptake of Dissolved Organic Carbon by Gammaproteobacterial Subgroups in Coastal Waters of the West Antarctic Peninsula. Applied and Environmental Microbiology, 80, pp.3362-3368. doi: 10.1128/aem.00121-14.

Pawlik, J.R. & McMurray, S.E., 2020. The Emerging Ecological and Biogeochemical Importance of Sponges on Coral Reefs. Annual Review of Marine Science, 12, pp.315-337. doi: 10.1146/annurev-marine-010419-010807.

Pisani, D. et al., 2015. Genomic data do not support comb jellies as the sister group to all other animals. Proceedings of the National Academy of Sciences, 112, pp.15402-15407. doi: 10.1073/pnas.1518127112.

Poppell, E. et al., 2014. Sponge heterotrophic capacity and bacterial community structure in high‐and low‐microbial abundance sponges. Marine Ecology, 35, pp.414-424. doi: 10.1111/maec.12098.

Priyadarshi, S., Shukla, A. & Borse, B.B., 2014. Polyhydroxyalkanoates: role of Ralstonia eutropha. International Journal of Biomedical and Advance Research, 5(2), pp.68-76. doi: 10.7439/ijbar.v5i2.639

Putra, S. et al., 2023. Two centuries of sponges (phylum Porifera) taxonomic studies in Indonesia (1820–2021): checklist and bibliography. Zootaxa, 5298, pp.1-74. doi: 10.11646/zootaxa.5298.1.1.

Rai, R. et al., 2021. Regulation of antioxidant defense and glyoxalase systems in cyanobacteria. Plant Physiology and Biochemistry, 168, pp.353-372. doi: 10.1016/j.plaphy.2021.09.037.

Rajendran, I., 2016. Typification of Chemical Compounds of Marine Sponge Metabolites. In Marine Sponges: Chemicobiological and Biomedical Applications. New Delhi: Springer India, pp.167-256. doi: 10.1007/978-81-322-2794-6_11.

Ruengsawang, N., Sangpradub, N. & Manconi, R., 2022. Aquatic Insects in Habitat-Forming Sponges: The Case of the Lower Mekong and Conservation Perspectives in a Global Context. Diversity, 14(11), 911. doi: 10.3390/d14110911

Senate, L.M. et al., 2019. Similarities, variations, and evolution of cytochrome P450s in Streptomyces versus Mycobacterium. Scintific Reports, 9, 3962. doi: 10.1038/s41598-019-40646-y.

Setiawan, E. et al., 2023. Revisit Study of Freshwater Sponges Eunapius carteri (Bowerbank, 1863) and a New Record of Oncosclera asiatica Manconi and Ruengsawang, 2012 (Porifera: Spongillida) in Porong River, East Java, Indonesia. HAYATI Journal of Biosciences, 30, pp.232-245. doi: 10.4308/hjb.30.2.232-245.

Setiawan, E. et al., 2024. A Mini Review on Analysis of Potential Antibacterial Activity of Symbiotic Bacteria from Indonesian Freshwater Sponge: An Unexplored and A Hidden Potency. Journal of Tropical Biodiversity and Biotechnology, 9(1), jtbb82682. doi: 10.22146/jtbb.82682.

Tooker, B.C. et al., 2022. Pseudomonas aeruginosa cytochrome P450 CYP168A1 is a fatty acid hydroxylase that metabolizes arachidonic acid to the vasodilator 19-HETE. Journal of Biological Chemistry, 298, 101629. doi: 10.1016/j.jbc.2022.101629.

Varijakzhan, D. et al., 2021. Bioactive compounds from marine sponges: Fundamentals and applications. Marine Drugs, 19(5), 246. doi: 10.3390/md19050246.

Vesty, A. et al., 2017. Evaluating the impact of DNA extraction method on the representation of human oral bacterial and fungal communities. PLoS ONE, 12(1), e0169877. doi: 10.1371/journal.pone.0169877

Walters, W. et al., 2016. Improved Bacterial 16S rRNA Gene (V4 and V4-5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys. mSystems, 1, e00009-15. doi: 10.1128/mSystems.00009-15.

Wang, Q. & Cole, J.R., 2024. Updated RDP taxonomy and RDP Classifier for more accurate taxonomic classification. Microbiology Resource Announcements, 13(4), e01063-23. doi: 10.1128/mra.01063-23.

Webster, N.S. & Thomas, T., 2016. The sponge hologenome. ASM Journals MBio, 7(2), pp.10-1128. doi: 10.1128/mbio.00135-16.

Weigel, B.L. & Erwin, P.M., 2016. Intraspecific Variation in Microbial Symbiont Communities of the Sun Sponge, Hymeniacidon heliophila, from Intertidal and Subtidal Habitats. Applied and Environmental Microbiology, 82, pp.650-658. doi: 10.1128/aem.02980-15.

Yadav, R., Rajput, V. & Dharne, M., 2021. Functional metagenomic landscape of polluted river reveals potential genes involved in degradation of xenobiotic pollutants. Environmental Research, 192, 110332. doi: 10.1016/j.envres.2020.110332.

Yilmaz, P. et al., 2014. The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucleic Acids Research, 42(D1), pp.D643-D648. doi: 10.1093/nar/gkt1209.

Zhang, W. et al., 2021. Intracellular GSH/GST antioxidants system change as an earlier biomarker for toxicity evaluation of iron oxide nanoparticles. NanoImpact, 23, 100338. doi: 10.1016/j.impact.2021.100338.

Published
2025-10-24
How to Cite
Setiawan, E., Hermanto, M. E., Yanuar, A., Riani, C., Mhuanthong, W., Prayogo, F. A., Wulandari, D., Budiharjo, A. and Jackie, L. M. (2025) “First Record on Microbial Colonies in Freshwater Sponges in East Java, Indonesia, and Their Estimated Pollutant Degradation Genes ”, Journal of Tropical Biodiversity and Biotechnology, 10(4), p. jtbb19647. doi: 10.22146/jtbb.19647.
Section
Research Articles