First identification of marine anammox bacteria in Indonesia under tropical aquaculture conditions
Article Sidebar
Abstract Views: 290
File Views: 213
Main Article Content
Abstract
Abstract. Zainuddin EN, Gumelar G, Ismail S, Rustama MM, Zulkarnaini Z. 2025. First identification of marine anammox in Indonesia under tropical aquaculture conditions. Biodiversitas 26: 6469-6479. Marine anaerobic ammonium oxidation (anammox) bacteria offer a promising and sustainable pathway for nitrogen removal from aquatic environments, particularly in shrimp aquaculture, where nitrogen-rich waste can cause environmental problems. This study aimed to identify marine anammox bacteria (MAB) under tropical conditions in two filter bioreactors (FtBRs) operated at tropical ambient temperatures with seawater salinity of 32-33 ppt. FtBR 1 was inoculated with intensive shrimp pond sludge, while FtBR 2 received a mixture of sludge and freshwater anammox granules (Candidatus Brocadia fulgida). Microbial community profiling was performed using Illumina HiSeq sequencing targeting the V3-V4 regions of the 16S rRNA gene. Both reactors successfully enriched the marine anammox species Candidatus Scalindua wagneri, accounting for 7% (FtBR 1) and 21% (FtBR 2) of the phylum Planctomycetota. In contrast, Candidatus Brocadia fulgida failed to survive under high salinity. Notably, Xanthomarina gelatinilytica emerged as the dominant genus in both systems, suggesting its important role in the hydrolysis and mineralization of organic nitrogen originating from shrimp aquaculture sludge. MAB were successfully identified and enriched despite their low relative abundance, suggesting potential interactions with co-occurring denitrifying communities. This study represents the first documented identification of MAB in Indonesia. These findings represent the first documented presence of MAB in Indonesia from aquaculture sludge. This work provides a foundation for developing localized, low-energy nitrogen removal technologies for sustainable shrimp aquaculture in coastal regions.
Article Details
Issue
Section
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
References
Alqahtani MF, Bajracharya S, Katuri KP, Ali M, Ragab A, Michoud G, Daffonchio D, Saikaly PE. 2019. Enrichment of Marinobacter sp. and halophilic homoacetogens at the biocathode of microbial electrosynthesis system inoculated with Red Sea brine pool. Front Microbiol 10: 2563. DOI: 10.3389/fmicb.2019.02563.
Amano T, Yoshinaga I, Yamagishi T, van Thuoc C, Thu PT, Ueda S, Kato K, Sako Y, Suwa Y. 2011. Contribution of anammox bacteria to benthic nitrogen cycling in a mangrove forest and shrimp ponds, Haiphong, Vietnam. Microbes Environ 26 (1): 1-6. DOI: 10.1264/jsme2.me10150.
Awata T, Kindaichi T, Ozaki N, Ohashi A. 2015. Biomass yield efficiency of the marine anammox bacterium, “Candidatus Scalindua sp.,” is affected by salinity. Microbes Environ 30 (1): 86-91. DOI: 10.1264/jsme2.me14088.
Brettar I, Labrenz M, Flavier S, Bötel J, Kuosa H, Christen R, Höfle MG. 2006. Identification of a Thiomicrospira denitrificans-like epsilonproteobacterium as a catalyst for autotrophic denitrification in the central Baltic Sea. Appl Environ Microbiol 72 (2): 1364-1372. DOI: 10.1128/aem.72.2.1364-1372.2006.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7 (5): 335-336. DOI: 10.1038/nmeth.f.303.
Dalsgaard T, Thamdrup B, Canfield DE. 2005. Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156 (4): 457-464. DOI: 10.1016/j.resmic.2005.01.011.
Edgar RC. 2013. UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10 (10): 996-998. DOI: 10.1038/nmeth.2604.
Foesel BU, Gieseke A, Schwermer C, Stief P, Koch L, Cytryn E, De La Torré JR, Van Rijn J, Minz D, Drake HL, Schramm A. 2008. Nitrosomonas Nm143-like ammonia oxidizers and Nitrospira marina-like nitrite oxidizers dominate the nitrifier community in a marine aquaculture biofilm. FEMS Microbiol Ecol 63 (2): 192-204. DOI: 10.1111/j.1574-6941.2007.00418.x.
Gonzalez-Martinez A, Muñoz-Palazon B, Rodriguez-Sanchez A, Gonzalez-Lopez J. 2018. New concepts in anammox processes for wastewater nitrogen removal: Recent advances and future prospects. FEMS Microbiol Lett 365 (6): fny031. DOI: 10.1093/femsle/fny031.
Gonzalez-Silva BM, Rønning AJ, Andreassen IK, Bakke I, Cervantes FJ, Østgaard K, Vadstein O. 2017. Changes in the microbial community of an anammox consortium during adaptation to marine conditions revealed by 454 pyrosequencing. Appl Microbiol Biotechnol 101 (12): 5149-5162. DOI: 10.1007/s00253-017-8160-5.
Gumelar G, Zainuddin E, Zulkarnaini Z. 2022. Anaerobic ammonium oxidation performance in shrimp pond wastewater treatment. And Intl J Appl Sci Eng Technol 2 (2): 51-56. DOI: 10.25077/aijaset.v2i1.41.
Gumelar G, Zainuddin EN, Zulkarnaini Z. 2024. Fast start-up marine anammox process using intensive shrimp pond solid waste as inoculum in filter bioreactor. J Sustain Sci Manag 19 (1): 55-62. DOI: 10.46754/jssm.2024.01.005.
Harwati TU, Kasai Y, Kodama Y, Susilaningsih D, Watanabe K. 2009. Tropicibacter naphthalenivorans gen. nov., sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from Semarang Port in Indonesia. Intl J Syst Evol Microbiol 59 (Pt 2): 392-396. DOI: 10.1099/ijs.0.65821-0.
Huang F, Pan L, He Z, Zhang M, Zhang M. 2020. Identification, interactions, nitrogen removal pathways and performances of culturable heterotrophic nitrification-aerobic denitrification bacteria from mariculture water by using cell culture and metagenomics. Sci Total Environ 732: 139268. DOI: 10.1016/j.scitotenv.2020.139268.
Hukom V, Nielsen R, Asmild M, Nielsen M. 2020. Do aquaculture farmers have an incentive to maintain good water quality? The case of small-scale shrimp farming in Indonesia. Ecol Econ 176: 106717. DOI: 10.1016/j.ecolecon.2020.106717.
Ismail IN, Taufik M, Umor NA, Norulhuda MR, Zulkarnaini Z, Ismail S. 2022. Anammox process for aquaculture wastewater treatment: Operational condition, mechanism, and future prospective. Water Sci Technol 86 (12): 3093-3112. DOI: 10.2166/wst.2022.403.
Kawagoshi Y, Nakamura Y, Kawashima H, Fujisaki K, Fujimoto A, Furukawa K. 2009. Enrichment culture of marine anaerobic ammonium oxidation (anammox) bacteria from sediment of sea-based waste disposal site. J Biosci Bioeng 107: 61-63. DOI: 10.1016/j.jbiosc.2008.10.003.
Kawagoshi Y, Nakamura Y, Kawashima H, Fujisaki K, Furukawa K, Fujimoto A. 2010. Enrichment of marine anammox bacteria from seawater-related samples and bacterial community study. Water Sci Technol 61 (1): 119-126. DOI: 10.2166/wst.2010.796.
Kindaichi T, Awata T, Tanabe K, Ozaki N, Ohashi A. 2011. Enrichment of marine anammox bacteria in Hiroshima Bay sediments. Water Sci Technol 63 (5): 964-969. DOI: 10.2166/wst.2011.277.
Labbé N, Parent S, Villemur R. 2004. Nitratireductor aquibiodomus gen. nov., sp. nov., a novel alpha-proteobacterium from the marine denitrification system of the Montreal Biodome (Canada). Intl J Syst Evol Microbiol 54: 269-273. DOI: 10.1099/ijs.0.02793-0.
Li M, Wang Y, Qin Z, Tian Z, Luan Y, Lu D. 2019. System for startup of Partial Nitritation-Anammox-Denitrification (PNAD) reaction. IOP Conf Ser: Earth Environ Sci 300: 032087. DOI: 10.1088/1755-1315/300/3/032087.
Lücker S, Nowka B, Rattei T, Spieck E, Daims H. 2013. The genome of Nitrospina gracilis illuminates the metabolism and evolution of the major marine nitrite oxidizer. Front Microbiol 4: 27. DOI: 10.3389/fmicb.2013.00027.
Magoč T, Salzberg SL. 2011. FLASH: Fast Length Adjustment of Short reads to improve genome assemblies. Bioinformatics 27 (21): 2957-2963. DOI: 10.1093/bioinformatics/btr507.
Micolucci F, Roques JAC, Ziccardi GS, Fujii N, Sundell K, Kindaichi T. 2023. Candidatus Scalindua, a biological solution to treat saline recirculating aquaculture system wastewater. Processes 11 (3): 690. DOI: 10.3390/pr11030690.
Okabe S, Kamizono A, Zhang L, Kawasaki S, Kobayashi K, Oshiki M. 2024. Salinity tolerance and osmoadaptation strategies in four genera of anammox bacteria: Brocadia, Jettenia, Kuenenia, and Scalindua. Environ Sci Technol 58: 5357-5371. DOI: 10.1021/acs.est.3c07324.
Pan C, Zhao Y-G, Mupindu P, Zhao S. 2024. The denitrification ability and nitrogen metabolism pathway of aerobic denitrifier Marinobacter alkaliphilus SBY-1 under low C/N ratios. Sci Total Environ 957: 177651. DOI: 10.1016/j.scitotenv.2024.177651.
Pereira AD, Cabezas A, Etchebehere C, de Lemos Chernicharo CA, de Araújo JC. 2017. Microbial communities in anammox reactors: A review. Environ Technol Rev 6 (1): 74-93. DOI: 10.1080/21622515.2017.1304457.
Rahayu T, Tyastuti EM, Ambarwati A, Agustina L, Setiyadi NA, Jamil N, Sidiq Y. 2024. Metagenomic data of bacterial 16S rRNA in the cemetery soil samples in Surakarta City, Indonesia. Data Brief 52: 109963. DOI: 10.1016/j.dib.2023.109963.
Russ L, Speth DR, Jetten MSM, Op den Camp HJM, Kartal B. 2014. Interactions between anaerobic ammonium and sulfur-oxidizing bacteria in a laboratory scale model system. Environ Microbiol 16 (11): 3487-3498. DOI: 10.1111/1462-2920.12487.
Smith KS, Ingram-Smith C. 2007. Methanosaeta, the forgotten methanogen? Trends Microbiol 15 (4): 150-155. DOI: 10.1016/j.tim.2007.02.002.
Tal Y, Watts JEM, Schreier HJ. 2006. Anaerobic ammonium-oxidizing (anammox) bacteria and associated activity in fixed-film biofilters of a marine recirculating aquaculture system. Appl Environ Microbiol 72 (4): 2896-2904. DOI: 10.1128/aem.72.4.2896-2904.2006.
Vaidya B, Kumar R, Sharma G, Srinivas TNR, Kumar PA. 2015. Xanthomarina gelatinilytica gen. nov., sp. nov., isolated from seawater. Intl J Syst Evol Microbiol 65 (11): 3926-3932. DOI: 10.1099/ijsem.0.000515.
van de Vossenberg J, Rattray JE, Geerts W, Kartal B, van Niftrik L, van Donselaar EG, Damsté JSS, Strous M, Jetten MSM. 2008. Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ Microbiol 10 (11): 3120-3129. DOI: 10.1111/j.1462-2920.2008.01643.x.
Wang T, Li J, Zhang LH, Yu Y, Zhu YM. 2017. Simultaneous heterotrophic nitrification and aerobic denitrification at high concentrations of NaCl and ammonia nitrogen by Halomonas bacteria. Water Sci Technol 76 (2): 386-395. DOI: 10.2166/wst.2017.214.
Yi M, Wang H, Ma X, Wang C, Wang M, Liu Z, Lu M, Cao J, Ke X. 2023. Efficient nitrogen removal of a novel Pseudomonas chengduensis strain BF6 mainly through assimilation in the recirculating aquaculture systems. Bioresour Technol 379: 129036. DOI: 10.1016/j.biortech.2023.129036.
Yokota N, Watanabe Y, Tokutomi T, Kiyokawa T, Hori T, Ikeda D, Song K, Hosomi M, Terada A. 2018a. High-rate nitrogen removal from waste brine by marine anammox bacteria in a pilot-scale UASB reactor. Appl Microbiol Biotechnol 102 (3): 1501-1512. DOI: 10.1007/s00253-017-8663-0.
Yokota N, Watanabe Y, Tokutomi T, Kiyokawa T, Hori T, Ikeda D, Song K, Hosomi M, Terada A. 2018b. High-rate nitrogen removal from waste brine by marine anammox bacteria in a pilot-scale UASB reactor. Appl Microbiol Biotechnol 102 (3): 1501-1512. DOI: 10.1007/s00253-017-8663-0.
Zhang L, Okabe S. 2020. Ecological niche differentiation among anammox bacteria. Water Res 171: 115468. DOI: 10.1016/j.watres.2020.115468.
Zhang M, Zhang T, Shao MF, Fang HHP. 2009. Autotrophic denitrification in nitrate-induced marine sediment remediation and Sulfurimonas denitrificans-like bacteria. Chemosphere 76 (5): 677-682. DOI: 10.1016/j.chemosphere.2009.03.066.
Zulkarnaini Z, Atsil N, Aribah HC, Komala PS, Silvia S, Matsuura N. 2024a. Diversity of anammox bacteria from landfill treatment plant sludge in tropical area. Appl Sci Eng Prog 17 (2): 7299. DOI: 10.14416/j.asep.2024.01.003.
Zulkarnaini Z, Komala PS, Putra RP, Ali M, Matsuura N, Koike K, Wang J, Mawarda PC, Yamamoto-Ikemoto R. 2025. Cultivation of anammox bacteria from a tropical lake in Indonesia using a novel filter bioreactor to enhance nitrogen removal efficiency. Water Sci Technol 91 (7): 811-826. DOI: 10.2166/wst.2025.050.
Zulkarnaini Z, Matsuura N, Kanazawa S, Honda R, Yamamoto-Ikemoto R. 2024b. Optimizing start-up strategies for the two-inflow nitritation/ anammox process: Influence on biofilm microbial community composition. Water Sci Technol 89 (6): 1583-1594. DOI: 10.2166/wst.2024.065.