Bioremediation Performance of Marine Sponge Symbiont Bacteria against Nickel and Mercury Heavy Metal Pollutants

Ismail Marzuki, Ruzkiah Asaf, Admi Athirah


Heavy metals, mercury, and nickel are toxic contaminants, forming positive ions when concentrated and dissolved, and can accumulate in a specific object, including water. The activity and performance of bacterial bioremediation against toxic heavy metals vary due to bacterial characteristics and internal contaminant factors. This research aims to analyze the activity, performance, and efficiency of bioremediation of nickel and mercury pollutants using marine sponge symbiont bacteria. The bioremediation analysis procedure, suspension of bacteria Alcaligenes faecalis strain Cu4-1 (AF), and Acinetobacter calcoaceticus strain PHCDB14 (AC) interacted with heavy metal pollutants as contaminants for 15 days. Bioremediation performance and efficiency were measured using AAS. The analysis parameters consisted of the performance, efficiency, and mechanism of bacterial bioremediation against nickel and mercury pollutants. The research results show that the bioremediation performance of AF and AC bacteria can carry out the bioremediation function against Ni+2 and Hg+2 contaminants. The bioremediation performance of AF bacteria against Ni+2 pollutant is, on average 167.64±0.9 mg/L, equivalent to 66.85% bioremediation efficiency, and against Hg+2 an average 171.55±0.7 equivalent to the efficiency of 65.47%. The performance of bioremediation of AC bacteria on Ni+2 pollutant was 168.92±0.7 or efficiency reached 66.97%, and 145.87±0.8 for Hg+2, equivalent to 58.35% efficiency. The bioremediation performance of AF ˂ AC bacteria against Ni+2 pollutants, but against Hg+2 pollutants, the bioremediation performance of AF ˃ AC bacteria. The symbiotic bacteria of marine sponges are thought to have bioremediation performance against toxic metal pollutants are bacteria isolated from sponges whose body surface is covered with mucus substances.


Bioremediation; bacterial; marine sponges; pollutants; nickel, mercury

Full Text:



E. Ziss, W.H. Friesl,C. Noller, A. Watzinger, and R.N. Hood, “Heavy Metal City-Zen. Exploring the potential risk of heavy metal contamination of food crop plants in urban gardening contexts using a citizen science approachâ€. Sustainability, vol. 13, no. 15, p.8626, 2021.

I. Marzuki, R. Ahmad, M. Kamaruddin, R. Asaf, R. Armus, and I. Siswanty, “Performance of cultured marine sponges-symbiotic bacteria as a heavy metal bio-adsorption,†Biodiversitas, vol. 22, no. 12, pp. 5536–5543, 2021.

A. Canaza, L. Pozo, E. F-. Guardia, and V. A. Vargas. “Biosorption Of Lead(Ii) Ions By Dead Bacterial Biomass Isolated From Mine Waterâ€. Revista Boliviana de Química, vol. 38, no. 3, pp. 119-125, 2021.

K. Dutta and S. Shityakov, “New Trends in Bioremediation Technologies Toward Environment-Friendly Society: A Mini-Review,†Front. Bioeng. Biotechnol., vol. 9, no. August, p. 666858, 2021.

A. M. Jibran, O. A. Ovewole, J. G. Yakubu, A. Hussaini and E. C. Egwim. “Heavy metals biosorption by urease producing Lysinibacillus fusiformis 5Bâ€. European J. of Bio. Res., vol 10 no 4, pp.326-335, 2020.

I. Marzuki, M. Y. Ali, H. U. Syarif, Erniati, S. Gusty, L. Daris and K. Nisaa. “Investigation of Biodegradable Bacteria as Bio indicators of the Presence of PAHs Contaminants in Marine Waters in the Marine Tourism Area of Makassar City,†in The 6th International Conference on Tropical and Coastal Region Eco-Development, 27-28 October 2020, Indonesia, IOP Conf. Series: Earth and Env. Sci. vol. 750, 2021, pp. 012006.

A. Bianchini and J. Rossi, “An integrated industry-based methodology to unlock full-scale implementation of phosphorus recovery technology,†sustainability., vol. 12, no. 24, pp. 1–17, 2020.

I. Marzuki, R. S. Alwi, Erniati, Mudyawati, Sinardi, and A. S. Iryani, “Chitosan Performance of Shrimp Shells in The Biosorption Ion Metal of Cadmium, Lead and Nickel Based on Variations pH Interaction,†in the First Int. Conf. on Materials Eng. and Manag. (Engineering Section) (ICMEMe), 1-2 August, 2019, Makassar, Indonesia, Atlantik Press, vol. 165, no. 1, 2019, pp. 6–11.

A. D. M. Ibrahim, S. Hamdona, M. E-. Naggar, H.A.E-. Hassayeb, O. Hassan, H. Tadros and M. M. A. E-. Naggar. “Heavy metal removal using a fixed bed bioreac. J. of Basic and App. Sci., vol. 8, no. 1, 7p., 2019.

S. S. Abdel Gawad, “Acute toxicity of some heavy metals to the fresh water snail, Theodoxus niloticus (Reeve, 1856),†Egypt. J. Aquat. Res., vol. 44, no. 2, pp. 83–87, 2018.

A. M. Hamdan, H.A. El‑Mageed and N. Ghanem. “Biological treatment of hazardous heavy metals by Streptomyces rochei ANH for sustainable water management in agricultureâ€. Scientific Reports, vol. 11, p.9314, 2021.

A. E. Rodríguez, S. C. Hernández, and L. D. Jiménez. “Evidence of Resistance of Heavy Metals from Bacteria Isolated from Natural Waters of a Mining Area in Mexicoâ€. Water, vol. 13, no. 10, p. 2766, 2021.

K. A. Alaboudi, B. Ahmed, and G. Brodie, “Annals of Agricultural Sciences Phytoremediation of Pb and Cd contaminated soils by using sun fl ower ( Helianthus annuus ) plant,†Ann. Agric. Sci., vol. 63, no. 1, pp. 123–127, 2018.

S. Selvam, K. Jesuraja, S. Venkatramanan, P. D. Roy, and V. Jeyanthi Kumari, “Hazardous microplastic characteristics and its role as a vector of heavy metal in groundwater and surface water of coastal south India,†J. Hazard. Mater., vol. 402, no. September, p. 123786, 2021.

I. Lawal. “Nitrogen Fixing Bacteria and Their Application for Heavy Metal Removal: A Mini Reviewâ€. J. of Bioc. Micr. and Biotec. vol. 9, no.2, pp. 43–47, 2021.

H. Kinoshita. “Biosorption of Heavy Metals by Lactic Acid Bacteria for Detoxificationâ€. Methods in Molecular Biology, vol. 1887, pp.145-157, 2019.

I. Marzuki, K. Nisaa, R. Asaf, R. Armus, M. Kamaruddin, A. Sapar and A. Emelda. “Biodegradation mechanism of naphthalene using marine sponge symbiotic bacteria,†In 2nd International Conference on Fisheries and Marine, 15 July 2021, Khairun University, Ternate, Indonesia (Virtual), IOP Conf. Ser. Earth Env. Sci., vol. 890, no. 1, p. 012020, 2021.

W. Irawati, R. Pinontoan, and T. Yuwono. “Indigenous copper resistant bacteria isolated from activated sludge of water treatment plant in Surabaya, Indonesiaâ€. Biodiversitas, vol. 21, no. 11, pp.5077-5084, 2020.

M. Z. A. Zaimee, M.S. Sarjadi, and M.L. Rahman, “Heavy metals removal from water by efficient adsorbentsâ€. Water (Switzerland). vol. 13, no.19, p. 2659, 2021.

J. F. Silva, B. F., G. R. Dias, M. M. de-Carvalho, and M. S. Laport, “Unravelling the sponge microbiome as a promising source of biosurfactantsâ€. Critical Reviews in Micr., Taylor & Francis. Vol 28, no. 1, p.324, 2022.

Y. Wei, W. Chen, C. Liu, and H. Wang, “Facial synthesis of adsorbent from hemicelluloses for Cr(VI) adsorption,†Molecules, vol. 26, no. 5, p. 1443, 2021.

X. X. Liu, X. Hu, Y. Cao, W. J. Pang, J. Y. Huang, P. Guo and L. Huang. “Biodegradation of Phenanthrene and Heavy Metal Removal by Acid-Tolerant Burkholderia fungorum FM-2,†Front. Microbiol., vol. 10, no. MAR, pp. 1–13, 2019.

I. Marzuki, R. Asaf, M. Paena, A. Athirah, K. Nisaa, R. Ahmad and M. Kamaruddin. “Anthracene and Pyrene Biodegradation Performance of Marine Sponge Symbiont Bacteria Consortium,†Molecules, vol. 26, no. 22, p. 6851, 2021.

I. Marzuki, M. Kamaruddin, and R. Ahmad, “Identification of marine sponges-symbiotic bacteria and their application in degrading polycyclic aromatic hydrocarbons,†Biodiversitas, vol. 22, no. 3, pp. 1481–1488, 2021.

J. I. P. Baquiran, M. A. L. Nada, N. Posadas, D. P. Manogan, P. C. Cabaitan, and C. Conaco, “Population structure and microbial community diversity of two common tetillid sponges in a tropical reef lagoon,†PeerJ, vol. 2020, no. 4, pp. 1–25, 2020.

J. H. Kim, H. Choi, G. H. Sung, S. A. Seo, K. I. Kim, Y. J. Kang and J.C Kang. “Toxic effects on hematological parameters and oxidative stress in juvenile olive flounder, Paralichthys olivaceus exposed to waterborne zinc,†Aquac. Reports, vol. 15, no. October, p. 100225, 2019.

I. Marzuki, E.Septiningsih, E. S. Kaseng, H. Herlinah, A. Sahrijanna, S. Sahabuddin, R. Asaf, A. Athirah, B. H. Isnawan,,G. S. Samidjo, F. Rumagia, E. Hamidah, I. S. Santi and K. Nisaa. “Investigation of Global Trends of Pollutants in Marine Ecosystems around Barrang Caddi Island, Spermonde Archipelago Cluster: An Ecological Approachâ€. Toxics, vo. 10, no. 6, p.301, 2022.

I. Marzuki, S. Sinardi, I. Pratama, M. Chaerul, I. Paserangi, M. Kamaruddin and R. Asaf. “Performance of sea sponges micro symbionts as a biomaterial in biodegradation naphthalene waste of modified,†in The 5th Int.Seminar on Sust. Urban Dev., 5 August 2020, Jakarta, Indonesia, IOP Conf. Ser: Earth and Env. Sci. vol. 737, no. 1, 2021, pp. 012016.

I. Marzuki, I. Pratama, H. E. Ismail, I. Paserangi, M. Kamaruddin, M. Chaerul and R. Ahmad. “The Identification and Distribution Components of Polycyclic Aromatic Hydrocarbon Contaminants at the Port of Paotere, Makassar, South Sulawesi,†in The 1st Int. Conf. on Biotechnology and Food Sciences, 11 Sept. 2020, Surabaya, Indonesia IOP Conf. Series: Earth and Env. Sci. IOP Publishing, vol. 679, 2021, pp. 012017.

M. C. Bart, M. Hudspith, H. T. Rapp, P. F. M. Verdonschot, and J. M. de Goeij, “A Deep-Sea Sponge Loop? Sponges Transfer Dissolved and Particulate Organic Carbon and Nitrogen to Associated Fauna,†Front. Mar. Sci., vol. 8, no. March, pp. 1–12, 2021.

L. Cepoi, I. Zinicovscaia, A. Valuta, L. Codreanu, L. Rudi, T. Chiriac, N. Yushin, D. Grozdov and A. Peshkova. “Peculiarities of the Edaphic Cyanobacterium Nostoc linckia Culture Response and Heavy Metal Accumulation from Copper-Containing Multimetal Systemsâ€. Toxics, vo. 10, no. 3, p.113, 2022.

L. I. F. Salih, R.O. Rashed, and S.M. Muhammed. “Evaluation of heavy metal content in water and removal of metals using native isolated bacterial strainsâ€. Biodiversitas, vol. 22, no. 8, pp. 3163-3174, 2021.

M. Haque, K. A. Haque, Z. H. Tanvir and K. Alam. “Biofilm Formation, Production of Matrix Compounds and Biosorption of Copper, Nickel and Lead by Different Bacterial Strainsâ€. Front. Microbiol. vol. 10, p. 615113, 2021.

J. S. Evans, S. L-. Legentil, J. R. Pawlik, I. G. Turnbull, and P. M. Erwin, “Molecular detection and microbiome differentiation of two cryptic lineages of giant barrel sponges from Conch Reef, Florida Keys,†Coral Reefs, vol. 40, no. 3, pp. 853–865, 2021.

A. G. Tenea, G. G. Vasile, C. Dinu, S. Gheorghe, L. F. Pascu, M. Mureseanu and C. Ene. “Behavior of Cd accumulation in sinapis alba L. In the presence of essential elements (Ca, Mg, Fe, Zn, Mn, Cu, Ni),†Rev. Chim., vol. 71, no. 6, pp. 378–389, 2020.

A. M. Orani, A. Barats, E. Vassileva, and O. P. Thomas, “Marine sponges as a powerful tool for trace elements biomonitoring studies in coastal environment,†Mar. Pollut. Bull., vol. 131, no. April, pp. 633–645, 2018.

M. Priyadarshanee, and S. Das. “Biosorption and removal of toxic heavy metals by metal tolerating bacteria for bioremediation of metal contamination: A comprehensive reviewâ€. J. of Environmental Chem. Eng. vol. 9, no.1, p. 104686, 2021.

S. S. El-Hawary, A. M. Sayed, R. Mohammed, H. M. Hassan, M. E Rateb, E. Amin, T. A. Mohammed, M. El-Mosery, A. B. muhsinah, A. Alsayari, H. Wajant, M. A. Anany and U. R. Abdelmohsen. “Bioactive brominated oxindole alkaloids from the red sea sponge callyspongia siphonella,†Mar. Drugs, vol. 17, no. 8, pp. 1–13, 2019.

X. Zou, X. Liu, M. Liu, M. Liu, and B. Zhang, “A framework for rice heavy metal stress monitoring based on phenological phase space and temporal profile analysis,†Int. J. Environ. Res. Public Health, vol. 16, no. 3, p. 350, 2019.

L. A. Tziveleka, E. Ioannou, D. Tsiourvas, P. Berillis, E. Foufa, and V. Roussis, “Collagen from the marine sponges Axinella cannabina and Suberites carnosus: Isolation and morphological, biochemical, and biophysical characterization,†Mar. Drugs, vol. 15, no. 6, p. 152, 2017.

P. Ziarati, V. Vambol, and S. Vambol, “Use of inductively coupled plasma optical emission spectrometry detection in determination of arsenic bioaccumulation in Trifolium pratense L. from contaminated soil,†Ecol. Quest., vol. 31, no. 1, p. 1, 2019.

F. Fahruddin, M. F. Samawi, M. Tuwo, and R. E. Tanjung, “The Effect of Heavy Metal Lead (Pb) on the Growth of Ammonia- Degrading Bacteria and Physical Changes of Eichhornia crassipes in Groundwater Phytoremediation,†Int. J. Adv. Sci. Eng. Inf. Technol., vol. 11, no. 3, pp. 994–1000, 2021.

M. T. Sibero, Y. Igarashi, O. K. Radjasa, A. Sabdono, A. Trianto, D. S. Zilda and Y. J. Wijaya. “Sponge-associated fungi from a mangrove habitat in Indonesia: species composition, antimicrobial activity, enzyme screening and bioactive profiling,†Int. Aquat. Res., vol. 11, no. 2, pp. 173–186, 2019.

T. Kamal, A. M. Asiri, and N. Ali, “Catalytic reduction of 4-nitrophenol and methylene blue pollutants in water by copper and nickel nanoparticles decorated polymer sponges,†Spectrochim. Acta Part A Mol. Biomol. Spectrosc., vol. 261, p. 120019, Nov. 2021.

A. Bossery, F. Shoukr, M. Komy, H. Rady, and M. ElArab, “Sponges from Elphinstone Reef, Northern Red Sea, Egypt,†Egypt. J. Exp. Biol., vol. 13, no. January, pp. 79–89, 2017.

F. Gaiti, W. L. Hatleberg, M. Tanurdžić, and B. M. Degnan, “Sponge long non-coding RNAs are expressed in specific cell types and conserved networks,†Non-coding RNA, vol. 4, no. 1, pp. 27–41, 2018.

I. Marzuki, S. Gusty, R. Armus, A. Sapar, R. Asaf, A. Athirah and Jaya. “Secondary Metabolite Analysis and Anti-Bacteria and Fungal Activities of Marine Sponge Methanol Extract Based on Coral Cover,†in The 6th Int. Conf. on Basic Sciences, 4–5 November 2020, Ambon, Indonesia, (IAP Conf. Proc.), vol. 2360, 2021, pp. 040007.

X. M. Su, A. M. Bamba, S. Zhang, Y. G. Zhang, M. Z. Hashmi, H. J. Lin, and L. X. Ding. “Revealing potential functions of VBNC bacteria in polycyclic aromatic hydrocarbons biodegradation,†Lett. Appl. Microbiol., vol. 66, no. 4, pp. 277–283, 2018.

E. Muszyńska, M. Labudda, I. Kamińska, M. Górecka, and M. Bederska-Błaszczyk, “Evaluation of heavy metal-induced responses in Silene vulgaris ecotypes,†Protoplasma, no. May, 2019.

A. Gran, Z.J. Ramos, E. Fuentes, D. Bravo, and D.J.M. Pérez. “Effect of co-contamination by PAHs and heavy metals on bacterial communities of diesel contaminated soils of south shetland islands, Antarcticaâ€. Microorganisms. vol. 8, no.11, pp. 1–17, 2020.

M. Mostafidi, F. Shirkhan, and M. T. Zahedi, “Bioaccumulation of the Heavy Metals Contents in Green Leafy Vegetables,†J. Nutr. Food Sci. Technol., vol. 2, no. 1, pp. 1–7, 2021.

M. Mostafidi, F. Shirkhan, M. T. Zahedi, P. Ziarati, and B. Hochwimmer, “Risk Assessment of the Heavy Metals Contents in Ready-to-eat Vegetables in Distributed Brands at the Supply Level of Sales Centers in Tehran , Iran,†Res. Line, no. February 2020, pp. 1–12, 2019.

S. Campana, K. Busch, U. Hentschel, G. Muyzer, and J. M. de Goeij, “DNA â€stable isotope probing DNAâ€stable isotope probing (DNAâ€SIP) identifies marine spongeâ€associated bacteria actively utilizing dissolved organic matter (DOM),†Environ. Microbiol., vol. 00, no. 00, pp. 1–16, 2021.

S. A. Jokinen, T. Jilbert, R. Tiihonen-Filppula, and K. Koho, “Terrestrial organic matter input drives sedimentary trace metal sequestration in a human-impacted boreal estuary,†Sci. Total Environ., vol. 717, p. 137047, 2020.

Y-.N. Xu, and Y. Chen. “Advances in heavy metal removal by sulfate-reducing bacteriaâ€. Water Sci Technol. Vol. 81, no. 9, pp. 1797–1827, 2020.

H. Handajani, W. Widanarni, T. Budiardi, and M. Setiawati, “Phytoremediation by Echinodorus palaefolius to Reduce Nitrogen and Phosphate Waste of Intensive Culture Anguilla bicolor in Recirculation Aquaculture Systems,†Int. J. Adv. Sci. Eng. Inf. Technol., vol. 11, no. 2, pp. 783–790, 2021.

V. H. T. Pham, J. Kim, S. Chang, and W. Chung. “Bacterial Biosorbents, an Efficient Heavy Metals Green Clean-Up Strategy: Prospects, Challenges, and Opportunitiesâ€. Microorganisms, vol. 10, no. 3, p. 610, 2022.

V. Zammuto, M. G. Rizzo, L. M De-Plano, D. Franco, S. Guglielmino, M. T. Caccamo, S. Magazu, A. Fujimori, A. L. Guidice, M. Guglielmin, K. R. McAlpin, R. Moeller and C. Gugliandolo. “Effects of heavy ion particle irradiation on spore germination of bacillus spp. From extremely hot and cold environments,†life, vol. 10, no. 11, pp. 1–20, 2020.

P. Sharma and S. Kumar. “Bioremediation of heavy metals from industrial effluents by endophytes and their metabolic activity: Recent advancesâ€. Bioresource Technology, vol. 339, p. 125589, 2021.

Q. Zhang, G. Han, M. Liu, X. Li, L. Wang, and B. Liang, “Distribution and contamination assessment of soil heavy metals in the jiulongjiang river catchment, southeast China,†Int. J. Environ. Res. Public Health, vol. 16, no. 23, p. 4674, 2019.

M. Arienzo, L. Ferrara, and M. Trifuoggi, “The dual role of microplastics in marine environment: Sink and vectors of pollutants,†J. Mar. Sci. Eng., vol. 9, no. 6, p. 642, 2021.

R. Armus, C. Selry, I. Marzuki, H. Hasan, Syamsia, and A. Sapar, “Investigation of Potential Marine Bacterial Isolates in Biodegradation Methods on Hydrocarbon Contamination,†J. Phys. Conf. Ser., vol. 1899, no. 1, 2021, pp. 012006.

I. Marzuki, L. Daris, S. Yunus, and A. D. Riana, “Selection and characterization of potential bacteria for polycyclic aromatic biodegradation of hydrocarbons in sea sponges from Spermonde Islands , Indonesia,†AACL Bioflux, vol. 13, no. 6, pp. 3493–3506, 2020.

K. A. Alaboudi, B. Ahmed, and G. Brodie, “Annals of Agricultural Sciences Phytoremediation of Pb and Cd contaminated soils by using sun fl ower (Helianthus annuus) plant,†Ann. Agric. Sci., vol. 63, no. 1, pp. 123–127, 2018.

I. V. Dotsenko and A. V. Mikhailenko, “Phytoplankton and Its Role in Accumulation of Microelements in Bottom Deposits of Azov Sea,†Sci. World J., vol. 2019, p. p.7, 2019.

W. M.K. Nakashima, S. Kawasaki, A. Arabelo, K. Banda, I. Nyambe, M. Chirwa, M. Ito, T. Sato, T. Igarashi, H. Nakata, S. Nakayama and M. Ishizuka. “Biosorption of Pb (II) and Zn (II) from aqueous solution by Oceanobacillus profundus isolated from an abandoned mineâ€. Scientific Reports, vol 10. p. 21189, 2020.

X. Liu, X. Hu, Y. Cao, W.P. Jing, H.J. Yu, P. Guo, and P, L. Huang. “Biodegradation of Phenanthrene and Heavy Metal Removal by Acid-Tolerant Burkholderia fungorum FM-2â€. Front Microbiol. vol. 10, pp. 1–13, 2019.

C. J. Freeman, C. G. Easson, C. L. Fiore, and R. W. Thacker, “Sponge–Microbe Interactions on Coral Reefs: Multiple Evolutionary Solutions to a Complex Environment,†Front. Mar. Sci., vol. 8, no. July, pp. 1–24, 2021.

T. Topal and C. Onac, “Determination of Heavy Metals and Pesticides in Different Types of Fish Samples Collected from Four Different Locations of Aegean and Marmara Sea,†J. Food Qual., vol. 2020, p. p.12, 2020.

R. Qu, G. Han, M. Liu, and X. Li, “The mercury behavior and contamination in soil profiles in mun river basin, Northeast Thailand,†Int. J. Environ. Res. Public Health, vol. 16, no. 21, p. 4131, 2019.

P. Ziarati, F. Mirmohammad Makki, S. Vambol, and V. Vambol, “Determination of toxic metals content iranian and Italian flavoured olive oil,†Acta Technol. Agric., vol. 22, no. 2, pp. 64–69, 2019.



  • There are currently no refbacks.

Published by INSIGHT - Indonesian Society for Knowledge and Human Development