Bioactivity of carotenoid produced by soft coral symbiotic microorganisms from Panjang and Karimunjawa Island, Central Java, Indonesia
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Abstract. Kusmita L, Nuryadi H, Widyananto PA, Muchlissin S, Sabdono A, Trianto A, Radjasa OK. 2021. Bioactivity of carotenoid produced by soft coral symbiotic microorganisms from Panjang and Karimunjawa Island, Central Java, Indonesia. Biodiversitas 22: 732-740. The diversity of soft corals is more varied in waters. One of the characteristics of soft corals is the production of secondary metabolites, i. i.e. carotenoids. Carotenoids are phytonutrients found in the cells of a wide variety of plants, algae, and bacteria as secondary metabolic compounds with antioxidant functions. Carotenoid biosynthesis is strongly influenced by the environment in which the producing organism grows. This study was aimed to uncover the antioxidant and anti-ultraviolet activities of carotenoids produced by soft coral symbiotic microorganisms in the waters surrounding the Panjang and Karimunjawa Islands in the North Java Sea, Indonesia. The parameters observed included water quality, antioxidant activity, and anti-ultraviolet activity. The results indicated that the water quality at Panjang Island did not meet quality standards (including salinity, visibility, dissolved oxygen, ammonia, and nitrate) while that at Karimunjawa did. The diversity of soft corals was more varied at Karimunjawa Island than at Panjang Island. In contrast to the bioactivity, the carotenoid extracts from the Panjang Island soft coral symbiotic microorganisms showed higher activity than those from Karimunjawa Island microorganisms. The highest antioxidant activity was found in the bacterial isolate 19.PP.Sc1.6 from Panjang Island and was identified based on the 16S rRNA gene as Virgibacillus salarius, with 99% similarity.
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References
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Burgess JG, Armstrong E, Jiang Z, Berggren M. 2003. The Development of a Marine Natural Product-based Antifouling Paint The Development of a Marine Natural Product-based Antifouling Paint. DOI: 10.1080/0892701031000061778
Casali JR, Gimenez J, Diez J, Alvarez-Mazos J, de Lersundi DV, Goni M, Campo MA, Chahor Y, Gastesi R, and Lopez J. 2010. Sediment production and water quality of waterheds with contrasting land use in Navarre (Spain). Agricultural Water Management. 97, 1683-1694. https://doi:10.1016/j.agwat.2010.05.024
Dahuri R, Rais J, Ginting SP, dan Sitepu MJ. 1996. Pengelolaan Sumberdaya Wilayah Pesisir dan Lautan Secara Terpadu. Jakarta: Pradnya Paramita.
Decree of the State Minister for the Environment Number 51 Year 2004 about Sea Water Quality Standart.
Dutta D, Chaudhuri U, Chakraborty R. 2005. Structure, health benefits, antioxidant property and processing and storage of carotenoids. African J Food, Agric Nutr Dev. 4,1510–1520. doi: 10.4314/ajfand.v4i13.71773
Edreva A, Velikova V, Tsonev T, Dagnon S, Gürel E, Aktas L, Gesheva E. 2008. Stress-protective role of secondary metabolites: diversity of functions and mechanisms. Gen Appl Plant Physiol. 34(1–2), 67–78
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Fibricius K, and Alderslade P. 2001. Soft Corals and Sea Fans: A Comprehensive guide to the Tropical Shallow-Water Genera Of The Central West Pasific, The Indian Ocean and Red Sea. Published by the Australian Institute of Marine Science PMB 3 Townsville MC, Queensland: Australia.
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Hamuna B, Tanjung, Suwito RHR, Maury HK, Alianto. 2018. Kajian Kualitas Air Laut dan Indeks Pencemaran Berdasarkan Parameter Fisika-Kimia di Perairan Distrik Depapre Jayapura. Jurnal Ilmu Kelautan. 16 (1), 35-43. https://doi.org/10.14710/jil.16.1.35-43
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Ibrahim HAH. 2012. Antibacterial carotenoids of three Holothuria species in Hurghada, Egypt. Egyptian Journal of Aquatic Research 38, 185–194. https://doi.org/10.1016/j.ejar.2013.01.004
Indarjo A, Wijadmoko M, Munasik. 2004. Kondisi Terumbu Karang di Perairan Pulau Panjang Jepara. Ilmu Kelautan. 9 (4), 217 – 224. DOI: https://doi.org/10.14710/ik.ijms.9.4.217-224
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Kjer J, Debbab A, Aly AH, and Proksch P. 2010. Methods for isolation of marine-derived endophytic fungi and their bioactive secondary products. Nat. Protoc. 5(3), 479–90. DOI: 10.1038/nprot.2009.223.
Khoo HE, Prasad KN, Kong KW, Jiang Y, Ismail A. 2011. Carotenoids and their isomers: Color pigments in fruits and vegetables. Molecules. 16,1710–1738. doi: 10.3390/molecules16021710
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 33,1870-1874. DOI: 10.1093/molbev/msw054
Kumar SA, Chaudhuri S, Dutta D. 2016. Antioxidant efficacy of carotenoid extract from bacterial strain Kocuria marina DAGII. Mater Today Proc. 3,3427–3433. doi: 10.1016/j.matpr.2016.10.023
Kusmita L, Mutiara EV, Nuryadi H, Pratama PA, Wiguna AS, Radjasa OK. 2017. Characterization of carotenoid pigments from bacterial symbionts of soft-coral Sarcophyton sp. from North Java Sea. Int Aquat Res. 9,61–69. doi: 10.1007/s40071-017-0157-2.
Mansur JS, Breder MNR, Mansur MCA, Azulay RD. 1986. Determinação do fator de proteção solar por espectrofotometria. An. Bras. Dermatol., Rio de Janeiro, v. 61, p. 121-124.
Manuputty AEW. 2016. The Common Soft Corals (Octocorallia: Alcyonacea) in East Biak Waters. Oseanologi dan Limnologi in Indonesia. 1 (2), 47 – 59.
Maoka T., 2011. Carotenoids in Marine Animals. Mar. Drugs. 9, 278 – 293. doi:10.3390/md9020278
Murniasih T. 2005. Subtansi Kimia Untuk Pertahanan Diri dari Hewan Laut Tak Bertulang Belakang. Oseana. 30(2), 19 – 27.
Murti DB, Susanto A, Radjasa OK, Rondonuwu FS. 2016. Pigments Characterization and Molecular Identification of Bacterial Symbionts of Brown Algae Padina sp . Collected from Karimunjawa Island. 21,59–64. doi: 10.14710/ik.ijms.21.2.59-64
Nugraheni SA, Khoeri MM, Kusmita L, Widyastuti Y, and Radjasa OK. 2010 Charakterization Of Carotenoid Pigments From Bacterial Symbionts Of Seagrass Thalassia hemprichii. J Coast Dev. 14,51-60.
Odum EP. 1993. Dasar-dasar Ekologi. Edisi ketiga. Gadjah Mada Press Yogyakarta. p. 134–162.
Puspasari F, Nurachman Z, Noer AA, Radjasa OK,van der Maarel MJEC, and Natalia D. 2011. Characteristics of Raw starch Degrading ?-amylase from Bacillus aquimaris MKSC 6.2 associated with soft coral Sinularia sp. Strarch. 63, 462 – 467. https://doi.org/10.1002/star.201000127
Radjasa OK, Sabdono A, Zocchi J, Zocchi E. 2007a. Richness of secondary metabolite-producing marine bacteria associated with sponge Haliclona sp. Int J Pharmacol. 3,275–279. doi: 10.3923/ijp.2007.275.279.
Radjasa OK, Salasia SIO, Sabdono A, Weise J, Johannes F, Imhoff, Lammler C, and Risk M. 2007b. Antibacterial Activity of Marine Bacterium Pseudomonas sp. Associated with Soft Coral Sinularia polydacta against Streptococcus equi Subsp. zooepidemicus. Int J Pharmacol 3:170–174. doi: 10.3923/ijp.2007.170.174
Radjasa OK, Vaske YM, Navarro G, Vervoort HC, Tenney K, Linington RG, Crews P. 2011. Highlights of marine invertebrate-derived biosynthetic products: their biomedical potential and possible production by microbial associants. Bioorg Med Chem. 19,6658–6674. https://doi.org/10.1016/j.bmc.2011.07.017.
Radjasa OK, Khoeri MM, Darusallam CC, Trimasanto H, Sudoyo H. 2013. Bacterial symbionts of reef invertebrates: screening for anti-pathogenic bacteria activity. Biodiversity. 14,80–86. https://doi.org/10.1080/14888386.2013.774937
Radušiene J, Karpaviciene B, Stanius Ž. 2012. Effect of external and Internal factors on secondary metabolites accumulation in St. John’s worth. Bot. Lith. 18. http://dx.doi.org/10.2478/v10279-012-0012-8.
Ramakrishna A, and Ravishankar GA. 2011. Influence of abiotic stress signals on secondary metabolite in plants. Plant Signaling & Behavior. 6:11, 1720-1731. DOI: 10.4161/psb.6.11.17613
Riccioni G, D’Orazio N, Franceschelli S, and Speranza L. 2011. Marine Carotenoids and Cardiovascular Risk Markers. Marine Drugs. 9, 1166-1175. doi: 10.3390/md9071166.
Riley PA. 1994. Free radicals in biology: oxidative stress and effects of ionizing radiation. Int J Rad Biol. 65, 27-33. DOI: 10.1080/09553009414550041
Rodriguez-Amaya DB, and Kimura M. 2004. HarvestPlus Handbook for Carotenoid Analysis. Washington, DC and Cali: International Food Policy Reasearch Institute (IFPRI) and International Center for Tropical Agliculture (CIAT)
Sabdono A, Sawonua PH, Kartika AGD, Amelia JM, Radjasa OK. 2015. Coral diseases in Panjang Island, Java Sea: diversity of anti–pathogenic bacterial coral symbionts. Procedia Chemistry. 14,15–21 DOI 10.1016/J.PROCHE.2015.03.004.
Salmin. 2015. Oksigen terlarut (DO) dan Kebutuhan Oksigen Biologi (BOD) sebagai Salah Satu Indikator untuk Menentukan Kualitas Perairan. Oseana. 30 (3), 21-26
Sibero MT, Bachtiarini TU, Trianto A, Lupita AH, Sari DP, Igarashi Y, Harunari E, Sharma AR, Radjasa OK, Sabdono A. 2019. Characterization of a yellow pigmented coral-associated bacterium exhibiting anti-Bacterial Activity Against Multidrug Resistant (MDR) Organism. Egyptian Journal of Aquatic Research. 45, 81–87.https://doi.org/10.1016/j.ejar.2018.11.007
Stahl W, and Sies H. 2003. Antioxidant activity of carotenoids. Mol Aspects Med. 24,345–351. doi: 10.1016/S0098-2997(03)00030-X
Sudha G. Ravishankar GA. 2003. Elicitation of anthocyanin production in callus cultures of Daucus carota and involvement of calcium channel modulators. Curr Sci. 84(6),775-779.
Suparmi, Radjasa OK, Limantara L. 2007. Mikroorganisme yang Berasosiasi Dengan Sponge: Potensinya Sebagai Sumber Biopigmen dan Upaya Budidayanya. Aquacultura Indonesiana. 8(2), 121-133
Verma N, Shukla S. 2015. Impact of various factors responsible for fluctuation in plant secondary metabolites. J. Appl. Res. Med. Aromatic Plants. 2(4), 105–113. http://dx.doi.org/10.1016/j.jarmap.2015.09.002.
Vilchez C, Forjan E, Cuaresma M, Bédmar F, Garbayo I, and Vega JM. 2011. Marine Carotenoids: Biological Functions and Commercial Aplications. Mar. Drugs. 9(3), 319-333. doi: 10.3390/md9030319.
Vershinin A. 1999. Biological Functions of Carotenoid—diversity and evolution. Biofactor. 10(2-3), 99 – 105. DOI: 10.1002/biof.5520100203.
Wardoyo STH. 1982. Water Analysis Manual Tropical Aquatic Biology Program. Biotrop SEAMEO. Bogor. p 81.
Widiadmoko W. 2013. Pemantauan Kualitas Air secara Fisika dan Kimia di Perairan Teluk Hurun. Bandar Lampung: Balai Besar Pengembangan Budidaya Laut (BBPBL) Lampung.
Zainudin M, Ambariyanto, Widowati I. 2013. Kajian Kualitas Perairan Jepara terhadap Kelimpahan dan Senyawa Bioaktif Antimikrobia Ekstrak Seaweed Spesies Sargassaceae (Phaeophyta, Fucales), Prosiding Seminar Nasional III. Fakultas Perikanan dan Ilmu Kelautan Universitas Diponegoro.
Atschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, and Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs. Nucleid Acid Res. 25, 3389–3402. Doi: 10.1093/nar/25.17.3389
Britton W. 2004. Worked Example of Isolation and Analysis. In: George B, Synnove L, Hanspeter P, editors. Carotenoids volume 1A: Isolation and analysis. Basel: Birkhäuser Verlag.p. 201–214.
Burgess JG, Armstrong E, Jiang Z, Berggren M. 2003. The Development of a Marine Natural Product-based Antifouling Paint The Development of a Marine Natural Product-based Antifouling Paint. DOI: 10.1080/0892701031000061778
Casali JR, Gimenez J, Diez J, Alvarez-Mazos J, de Lersundi DV, Goni M, Campo MA, Chahor Y, Gastesi R, and Lopez J. 2010. Sediment production and water quality of waterheds with contrasting land use in Navarre (Spain). Agricultural Water Management. 97, 1683-1694. https://doi:10.1016/j.agwat.2010.05.024
Dahuri R, Rais J, Ginting SP, dan Sitepu MJ. 1996. Pengelolaan Sumberdaya Wilayah Pesisir dan Lautan Secara Terpadu. Jakarta: Pradnya Paramita.
Decree of the State Minister for the Environment Number 51 Year 2004 about Sea Water Quality Standart.
Dutta D, Chaudhuri U, Chakraborty R. 2005. Structure, health benefits, antioxidant property and processing and storage of carotenoids. African J Food, Agric Nutr Dev. 4,1510–1520. doi: 10.4314/ajfand.v4i13.71773
Edreva A, Velikova V, Tsonev T, Dagnon S, Gürel E, Aktas L, Gesheva E. 2008. Stress-protective role of secondary metabolites: diversity of functions and mechanisms. Gen Appl Plant Physiol. 34(1–2), 67–78
Effendi H. 2003. Telaah Kualitas Air bagi Pengelolaan Sumberdaya dan Lingkungan Perairan. Cetakan Kelima. Yogjakarta: Kanisius
Fibricius K, and Alderslade P. 2001. Soft Corals and Sea Fans: A Comprehensive guide to the Tropical Shallow-Water Genera Of The Central West Pasific, The Indian Ocean and Red Sea. Published by the Australian Institute of Marine Science PMB 3 Townsville MC, Queensland: Australia.
Galasso C, Corinaldesi C, and Sansone C. 2017. Carotenoids from Marine Organisms: Biological Functions and Industrial Applications. Antioxidants. 6, 96. doi:10.3390/antiox6040096
Gross J. 1991. Pigmen in Vegetables. Van Nastrand Reinhold, New York, 351 pp.
Haila K. 1999. Effects of Carotenoids and Carotenoid- Tocopherol Interaction on Lipid Oxidation In Vitro. University of Helsinki, Department of Applied Chemistry and Microbiology Helsinki.
Hamuna B, Tanjung, Suwito RHR, Maury HK, Alianto. 2018. Kajian Kualitas Air Laut dan Indeks Pencemaran Berdasarkan Parameter Fisika-Kimia di Perairan Distrik Depapre Jayapura. Jurnal Ilmu Kelautan. 16 (1), 35-43. https://doi.org/10.14710/jil.16.1.35-43
Hua NP, Hamza-Chaffai A, Vreeland RH, Isoda H, Naganuma T. 2008. Virgibacillus salarius sp. nov., a halophilic bacterium isolated from a Saharan salt lake. International Journal of Systematic and Evolutionary Microbiology. 58 (Pt 10), 2409–14. https://doi.org/10.1099/ijs.0.65693-0
Ibrahim HAH. 2012. Antibacterial carotenoids of three Holothuria species in Hurghada, Egypt. Egyptian Journal of Aquatic Research 38, 185–194. https://doi.org/10.1016/j.ejar.2013.01.004
Indarjo A, Wijadmoko M, Munasik. 2004. Kondisi Terumbu Karang di Perairan Pulau Panjang Jepara. Ilmu Kelautan. 9 (4), 217 – 224. DOI: https://doi.org/10.14710/ik.ijms.9.4.217-224
Karuppusamy S. 2009. A review on trends in production of secondary metabolites from higher plants by in vitro tissue, organ and cell cultures. J Med Plants Res. 3,1222-39. DOI: 10.5897/JMPR
Kjer J, Debbab A, Aly AH, and Proksch P. 2010. Methods for isolation of marine-derived endophytic fungi and their bioactive secondary products. Nat. Protoc. 5(3), 479–90. DOI: 10.1038/nprot.2009.223.
Khoo HE, Prasad KN, Kong KW, Jiang Y, Ismail A. 2011. Carotenoids and their isomers: Color pigments in fruits and vegetables. Molecules. 16,1710–1738. doi: 10.3390/molecules16021710
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 33,1870-1874. DOI: 10.1093/molbev/msw054
Kumar SA, Chaudhuri S, Dutta D. 2016. Antioxidant efficacy of carotenoid extract from bacterial strain Kocuria marina DAGII. Mater Today Proc. 3,3427–3433. doi: 10.1016/j.matpr.2016.10.023
Kusmita L, Mutiara EV, Nuryadi H, Pratama PA, Wiguna AS, Radjasa OK. 2017. Characterization of carotenoid pigments from bacterial symbionts of soft-coral Sarcophyton sp. from North Java Sea. Int Aquat Res. 9,61–69. doi: 10.1007/s40071-017-0157-2.
Mansur JS, Breder MNR, Mansur MCA, Azulay RD. 1986. Determinação do fator de proteção solar por espectrofotometria. An. Bras. Dermatol., Rio de Janeiro, v. 61, p. 121-124.
Manuputty AEW. 2016. The Common Soft Corals (Octocorallia: Alcyonacea) in East Biak Waters. Oseanologi dan Limnologi in Indonesia. 1 (2), 47 – 59.
Maoka T., 2011. Carotenoids in Marine Animals. Mar. Drugs. 9, 278 – 293. doi:10.3390/md9020278
Murniasih T. 2005. Subtansi Kimia Untuk Pertahanan Diri dari Hewan Laut Tak Bertulang Belakang. Oseana. 30(2), 19 – 27.
Murti DB, Susanto A, Radjasa OK, Rondonuwu FS. 2016. Pigments Characterization and Molecular Identification of Bacterial Symbionts of Brown Algae Padina sp . Collected from Karimunjawa Island. 21,59–64. doi: 10.14710/ik.ijms.21.2.59-64
Nugraheni SA, Khoeri MM, Kusmita L, Widyastuti Y, and Radjasa OK. 2010 Charakterization Of Carotenoid Pigments From Bacterial Symbionts Of Seagrass Thalassia hemprichii. J Coast Dev. 14,51-60.
Odum EP. 1993. Dasar-dasar Ekologi. Edisi ketiga. Gadjah Mada Press Yogyakarta. p. 134–162.
Puspasari F, Nurachman Z, Noer AA, Radjasa OK,van der Maarel MJEC, and Natalia D. 2011. Characteristics of Raw starch Degrading ?-amylase from Bacillus aquimaris MKSC 6.2 associated with soft coral Sinularia sp. Strarch. 63, 462 – 467. https://doi.org/10.1002/star.201000127
Radjasa OK, Sabdono A, Zocchi J, Zocchi E. 2007a. Richness of secondary metabolite-producing marine bacteria associated with sponge Haliclona sp. Int J Pharmacol. 3,275–279. doi: 10.3923/ijp.2007.275.279.
Radjasa OK, Salasia SIO, Sabdono A, Weise J, Johannes F, Imhoff, Lammler C, and Risk M. 2007b. Antibacterial Activity of Marine Bacterium Pseudomonas sp. Associated with Soft Coral Sinularia polydacta against Streptococcus equi Subsp. zooepidemicus. Int J Pharmacol 3:170–174. doi: 10.3923/ijp.2007.170.174
Radjasa OK, Vaske YM, Navarro G, Vervoort HC, Tenney K, Linington RG, Crews P. 2011. Highlights of marine invertebrate-derived biosynthetic products: their biomedical potential and possible production by microbial associants. Bioorg Med Chem. 19,6658–6674. https://doi.org/10.1016/j.bmc.2011.07.017.
Radjasa OK, Khoeri MM, Darusallam CC, Trimasanto H, Sudoyo H. 2013. Bacterial symbionts of reef invertebrates: screening for anti-pathogenic bacteria activity. Biodiversity. 14,80–86. https://doi.org/10.1080/14888386.2013.774937
Radušiene J, Karpaviciene B, Stanius Ž. 2012. Effect of external and Internal factors on secondary metabolites accumulation in St. John’s worth. Bot. Lith. 18. http://dx.doi.org/10.2478/v10279-012-0012-8.
Ramakrishna A, and Ravishankar GA. 2011. Influence of abiotic stress signals on secondary metabolite in plants. Plant Signaling & Behavior. 6:11, 1720-1731. DOI: 10.4161/psb.6.11.17613
Riccioni G, D’Orazio N, Franceschelli S, and Speranza L. 2011. Marine Carotenoids and Cardiovascular Risk Markers. Marine Drugs. 9, 1166-1175. doi: 10.3390/md9071166.
Riley PA. 1994. Free radicals in biology: oxidative stress and effects of ionizing radiation. Int J Rad Biol. 65, 27-33. DOI: 10.1080/09553009414550041
Rodriguez-Amaya DB, and Kimura M. 2004. HarvestPlus Handbook for Carotenoid Analysis. Washington, DC and Cali: International Food Policy Reasearch Institute (IFPRI) and International Center for Tropical Agliculture (CIAT)
Sabdono A, Sawonua PH, Kartika AGD, Amelia JM, Radjasa OK. 2015. Coral diseases in Panjang Island, Java Sea: diversity of anti–pathogenic bacterial coral symbionts. Procedia Chemistry. 14,15–21 DOI 10.1016/J.PROCHE.2015.03.004.
Salmin. 2015. Oksigen terlarut (DO) dan Kebutuhan Oksigen Biologi (BOD) sebagai Salah Satu Indikator untuk Menentukan Kualitas Perairan. Oseana. 30 (3), 21-26
Sibero MT, Bachtiarini TU, Trianto A, Lupita AH, Sari DP, Igarashi Y, Harunari E, Sharma AR, Radjasa OK, Sabdono A. 2019. Characterization of a yellow pigmented coral-associated bacterium exhibiting anti-Bacterial Activity Against Multidrug Resistant (MDR) Organism. Egyptian Journal of Aquatic Research. 45, 81–87.https://doi.org/10.1016/j.ejar.2018.11.007
Stahl W, and Sies H. 2003. Antioxidant activity of carotenoids. Mol Aspects Med. 24,345–351. doi: 10.1016/S0098-2997(03)00030-X
Sudha G. Ravishankar GA. 2003. Elicitation of anthocyanin production in callus cultures of Daucus carota and involvement of calcium channel modulators. Curr Sci. 84(6),775-779.
Suparmi, Radjasa OK, Limantara L. 2007. Mikroorganisme yang Berasosiasi Dengan Sponge: Potensinya Sebagai Sumber Biopigmen dan Upaya Budidayanya. Aquacultura Indonesiana. 8(2), 121-133
Verma N, Shukla S. 2015. Impact of various factors responsible for fluctuation in plant secondary metabolites. J. Appl. Res. Med. Aromatic Plants. 2(4), 105–113. http://dx.doi.org/10.1016/j.jarmap.2015.09.002.
Vilchez C, Forjan E, Cuaresma M, Bédmar F, Garbayo I, and Vega JM. 2011. Marine Carotenoids: Biological Functions and Commercial Aplications. Mar. Drugs. 9(3), 319-333. doi: 10.3390/md9030319.
Vershinin A. 1999. Biological Functions of Carotenoid—diversity and evolution. Biofactor. 10(2-3), 99 – 105. DOI: 10.1002/biof.5520100203.
Wardoyo STH. 1982. Water Analysis Manual Tropical Aquatic Biology Program. Biotrop SEAMEO. Bogor. p 81.
Widiadmoko W. 2013. Pemantauan Kualitas Air secara Fisika dan Kimia di Perairan Teluk Hurun. Bandar Lampung: Balai Besar Pengembangan Budidaya Laut (BBPBL) Lampung.
Zainudin M, Ambariyanto, Widowati I. 2013. Kajian Kualitas Perairan Jepara terhadap Kelimpahan dan Senyawa Bioaktif Antimikrobia Ekstrak Seaweed Spesies Sargassaceae (Phaeophyta, Fucales), Prosiding Seminar Nasional III. Fakultas Perikanan dan Ilmu Kelautan Universitas Diponegoro.
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