Isolation and identification of thermophilic amylolytic bacteria from Likupang Marine Hydrothermal, North Sulawesi, Indonesia
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Abstract. Ginting EL, Wantania LL, Moko EM, Tumbol RA, Siby MS, Wulur S. 2021. Isolation and identification of thermophilic amylolytic bacteria from Likupang Marine Hydrothermal, North Sulawesi, Indonesia. Biodiversitas 22: 3326-3332. The aims of the research were to isolate and identify the amylase-producing thermophilic bacteria from Likupang Marine Hydrothermal, North Sulawesi, Indonesia. The bacteria were characterized based on the colony and cell morphology and subsequently screened for their amylase activities. The bacterial isolates were identified based on 16S rRNA gene sequences. There were 12 thermophilic bacteria isolates from Likupang Marine Hydrothermal that were able to produce amylase. Two selected isolates (L3 and L9) had an amylolytic index value in the range of 3.04-3.52 at 55oC. The colonies of L3 and L9 are circular, and they are Gram positive, rod-shaped, and motile bacteria. Based on the 16S rRNA gene sequences and phylogenetic tree analysis showed that L3 was closely related to Bacillus caldotenax with 93% similarity while L9 had 99% similarity to B. caldotenax. Hence, we identified L3 isolate as Bacillus sp. strain L3 and L9 isolate as B. caldotenax strain L9. Both of these bacteria were grouped as Geobacillus thermoleovorans.
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References
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Ashwini K, Gaurav K, Karthik L, Bhaskara RKV. 2011. Optimization, production and partial purification of extra cellular ? amylase from Bacillus sp. Marini Arch Appl Sci Res 3 (1): 33-42.
Charbonneau DM, Meddeb-Mouelhi F, Boissinot M, Sirois M, Beauregard M. 2012. Identification of thermophilic bacterial strains producing thermotolerant hydrolytic enzymes from manure compost. Indian J Microbiol 52 (1): 41-47. DOI: 10.1007/s12088-011-0156-8.
Cihan AC, Tekin N, Ozcan B, Cokmus C. 2012. The genetic diversity of genus Bacillus and the related genera revealed by 16s rRNA gene sequences and ardra analyses isolated from geothermal regions of Turkey. Braz J Micribiol, 43: 309-324. DOI: 10.1590/S1517-838220120001000037.
De Souza PM, Magalhaes PO. 2010. Application of microbial ?-amylase in industry: A review. Braz J Microbiol 41: 850-861. DOI: 10.1590/S1517-83822010000400004.
Dinsdale AE, Halket G, Coorevits A, Van Landschoot A, Busse H-JB, De Vos P, Logan NA. 2011. Emended descriptions of Geobacillus thermoleovorans and Geobacillus thermocatenulatus. Int J Syst Evol Microbiol. 61:1802-1810. DOI: 10.1099/ijs.0.025445-0.
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Ginting EL, Kemer K, Wullur S, Uria AR. 2019. Identification of proteolytic thermophiles from Moinit coastal hot-spring, North Sulawesi, Indonesia. Geomicrobiology Journal 37 (1): 50-58. DOI: 10.1080/01490451.2019.1662524.
Gomes I, Gomes J, Steiner W. 2003. Highly thermostable amylase and pullulanase of the extreme thermophilic eubacterium Rhodothermus marinus: production and partial characterization. Bioresour Technol 90: 207-214. DOI: 10.1016/s0960-8524(03)00110-x.
Gugliandolo C, Lentini V, Spano A, Maugeri TL. 2012. New bacilli from shallow hydrothermal vents of Panarea Island (Italy) and their biotechnological potential. Journal of Applied Microbiology 112: 1102-1112. DOI: 10.1111/j.1365-2672.2012.05272.x.
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Kambourova M. 2018. Thermostable enzymes and polysaccharides produced by thermophilic bacteria isolated from Bulgarian hot springs. Eng. Life sci. 18:758-767. DOI: 10.1002/elsc.201800022.
Keller M, Loder AJ, Basen M, Izquierdo J, Kelly RM, Adams MW. 2014. Production of lignofuels and electrofuels by extremely thermophilic microbes. Biofuels 5: 499-515. DOI: 10.1080/17597269.2014.996729.
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.
Luang-In V, Yotchaisarn M, Saengha W, Udomwong P, Deeseenthum S, Maneewan K. 2019. Isolation and identification of amylase-producing bacteria from soil in Nasinuan Community Forest, Maha Sarakham, Thailand. Biomedical & Pharmacology Journal 12: 1061-1068. DOI: 10.13005/bpj/1735.
Mohammad BT, Al Daghistani HI, Jaouani A, Abdel-Latif S, Kennes C. 2017. Isolation and characterization of thermophilic bacteria from Jordanian Hot Springs: Bacillus licheniformis and Thermomonas hydrothermalis isolates as potential producers of thermostable enzymes. Hindawi
International Journal of Microbiology, 2017: 1-12. DOI: 10.1155/2017/6943952.
Msarah MJ, Ibrahim I, Hamid AA, Aqma WS. 2020. Optimisation and production of alpha amylase from thermophilic Bacillus spp. and its application in food waste biodegradation. Heliyon 6: 1-9. DOI: 10.1016/j.heliyon.2020.e04183.
Myung-Ji S, Kim J, Pyun Y. 2012. 16S rRNA Gene sequence-based microbial diversity analyses of the geothermal areas of Cisolok, Kamojang, and Likupang in Indonesia. Korean J Microbiol Biotechnol 40 (3): 268-273. DOI: 10.4014/kjmb.1205.05001.
Nazina T, Tourova T, Poltaraus A, Novikova E, Grigoryan A, Ivanova A, Lysenko A, Petrunyaka V, Osipov G, Belyaev S, Ivanov M. 2001. Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov.and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermoglucosidasius and Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasiusand, G. thermodenitrificans. Int J Syst Evol Microbiol 51 (2): 433-446. DOI: 10.1099/00207713-51-2-433.
Nazina TN, Sokolova DS, Grigoryan AA, Shestakova NM, Mikhailova EM, Poltaraus AB. 2005. Geobacillus jurassicus sp. nov., a new thermophilic bacterium isolated from a high-temperature petroleum reservoir, and the validation of the Geobacillus species. Syst Appl Microbiol 28: 43-53. DOI: 10.1016/j.syapm.2004.09.001.
Nguyen QD, Rezessy-Szabó JM, Claeyssens M, Stals I, Hoschke A. 2002. Purification and characterization of amylolytic enzymes from thermophilic fungus Thermomyces lanuginosus strain ATCC 34626. Enzyme Microb Technol 31 (3): 345-52. DOI: 10.1016/S0141-0229(02)00128-X.
Nihaya I, Sarjono PR, Aminin ALN. 2013. Studi filogeni dan uji potensi antibakteri serta enzim ekstraseluler isolat Geobacillus sp. dari sumber air panas Gedongsongo. Jurnal Kimia Sains dan Aplikasi 16: 38- 41. DOI: 10.14710/jksa.16.2.38-41 [Indonesian].
Oziengbe EO, Onilude AA. 2012. Production of a thermostable ?-amylase and its assay using Bacillus licheniformis isolated from excavated land sites in Ibadan, Nigeria. Bayero Journal of Pure and Applied Sciences 5 (1): 132-138. DOI: 10.4314/bajopas.v5i1.24.
Poletto TV, Vieira CRW, Silva CP, Fracalossi DM. 2018. Isolation and identification of a potential amylolytic probiotic bacterium from the gut of Jundiá catfish. Rhamdia Quelen Braz Arch Biol Technol 61: 1-9. DOI: 10.1590/1678-4324-2018161205.
Prakash O, Jaiswal N. 2010. Alpha-amylase: An ideal representative of thermostable enzymes. Appl Biochem Biotechnol 160: 2401-2414. DOI: 10.1007/s12010-009-8735-4.
Raddadi N, Cherif A, Daffonchio D, Neifar M, Fava F. 2015. Biotechnological applications of extremophiles, extremozymes and extremolytes. Appl Microbiol Biotechnol 99 (19): 7907-7913. DOI: 10.1007/s00253-015-6874-9.
Satrimafitrah P, Razak AR, Hardi J, Puspitasari DJ, Yelenggete I, Rafik. 2020. Thermostable amylase activity produced by thermophilic bacteria isolated from Pulu Hotspring, Central Sulawesi. J. Phys.: Conf. Ser. 1434. National Seminar on Physics, Palu, 28 September 2019. DOI: 10.1088/1742-6596/1434/1/012034.
Sharma P, Gupta S, Sourirajan A, Dev K. 2015. Characterization of extracellular thermophilic amylase from Geobacillus sp. isolated from Tattapani Hot Spring of Himachal Pradesh, India. Current Biotechnology 4 (2): 202-209. DOI: 10.2174/2211550104666150612223748.
Singh G, Bhalla A, Kaur P, Capalash N, Sharma P. 2011. Laccase from prokaryotes: A new source for an old enzyme. Reviews in Environmental Science and Biotechnology 10: 309-326. DOI: 10.1007/s11157-011-9257-4.
Thairu Y, Nasir IA, Usman Y. 2014. Laboratory Perspective of Gram Staining and its Significance in Investigations of Infectious Diseases. Sub-Saharan African Journal of Medicine, 1: 168-174. DOI: 10.4103/2384-5147.144725.
Wantania LL, Wullur S, Ginting EL, Mantiri DM, Undap SL, Sumilat DA, Gerung GS. 2019. Isolation and amplification of 16S rRNA gen of associated microbial isolates in red algae Kappaphycus alvarezii from Belang, Southeast Minahasa Regency, North Sulawesi. Jurnal Ilmiah Platax 7 (1): 220-226. DOI: https://doi.org/10.35800/jip.7.1.2019.22808 [Indonesian]
Wullur S, Napitupulu H, Wantania LL, Ginting EL, Warouw V, Tilaar SO, Tallei TE, Rumengan IFM. 2020. Molecular identification of bacteria isolated from culture medium of rotifer fed on fishery waste diet. Biodiversitas 21 (6): 1735-1740. DOI: 10.13057/biodiv/d210649.
Zeigler DR. 2005. Application of a recN sequence similarity analysis to the identification of species within the bacterial genus Geobacillus. Int J Syst Evol Microbiol 55: 1171-1179. DOI: 10.1099/ijs.0.63452-0.
Zhang RY, Bin Z, Yan YW, Jeon CO, Li M, Cai M, Quan ZX. 2020. Design of targeted primers based on 16S rRNA sequences in meta-transcriptomic datasets and identification of a novel taxonomic group in the Asgard archaea. BMC Microbiology 20: 1-10. DOI: 10.1186/s12866-020-1707-0.
Aliyu H, Lebre P, Blom J, Cowan D, De Maayer P. 2016. Phylogenomic reassessment of the thermophilic genus Geobacillus. Syst Appl Microbiol 39: 527-533. DOI: 10.1016/j.syapm.2016.09.004.
Ardhi A, Sidauruk AN, Suraya N, Pratiwi NW, Pato U, Saryono. 2020. Molecular identification of amylase-producing thermophilic bacteria isolated from Bukit Gadang Hot Spring, West Sumatra, Indonesia. Biodiversitas 21 (3): 994-1000. DOI: 10.13057/biodiv/d210319.
Ashwini K, Gaurav K, Karthik L, Bhaskara RKV. 2011. Optimization, production and partial purification of extra cellular ? amylase from Bacillus sp. Marini Arch Appl Sci Res 3 (1): 33-42.
Charbonneau DM, Meddeb-Mouelhi F, Boissinot M, Sirois M, Beauregard M. 2012. Identification of thermophilic bacterial strains producing thermotolerant hydrolytic enzymes from manure compost. Indian J Microbiol 52 (1): 41-47. DOI: 10.1007/s12088-011-0156-8.
Cihan AC, Tekin N, Ozcan B, Cokmus C. 2012. The genetic diversity of genus Bacillus and the related genera revealed by 16s rRNA gene sequences and ardra analyses isolated from geothermal regions of Turkey. Braz J Micribiol, 43: 309-324. DOI: 10.1590/S1517-838220120001000037.
De Souza PM, Magalhaes PO. 2010. Application of microbial ?-amylase in industry: A review. Braz J Microbiol 41: 850-861. DOI: 10.1590/S1517-83822010000400004.
Dinsdale AE, Halket G, Coorevits A, Van Landschoot A, Busse H-JB, De Vos P, Logan NA. 2011. Emended descriptions of Geobacillus thermoleovorans and Geobacillus thermocatenulatus. Int J Syst Evol Microbiol. 61:1802-1810. DOI: 10.1099/ijs.0.025445-0.
Finore I, Kasavi C, Poli A, Romano I, Oner ET, Kirdar B, Dipasquale L, Nicolaus B, Lama L. 2011. Purification, biochemical characterization and gene sequencing of a thermostable raw starch digesting ?-amylase from Geobacillus thermoleovorans subsp. stromboliensis subsp. nov. World J Microbiol Biotechnol 27: 2425-2433. DOI: 10.1007/s11274-011-0715-5.
Frock AD, Kelly RM. 2012. Extreme thermophiles: moving beyond single-enzyme biocataysis. Curr Opin Chem Eng 1: 363-372. DOI: 10.1016/j.coche.2012.07.003.
Gazali FM, Ananda M, Suwastika IN. 2018. Characterization of ?-amylase activity from thermophilic bacteria isolated from Bora Hot spring, Central Sulawesi. Natural Science: Journal of Science and Technology 7 (1): 99-109. [Indonesian]
Gazali FM, Suwastika IN. 2018. Thermostable ?-amylase activity from thermophilic bacteria isolated from Bora Hot Spring, Central Sulawesi. J. Phys.: Conf. Ser. 979. The 2nd International Conference on Science (ICOS), Makasar, 2-3 November 2017. DOI: doi:10.1088/1742-6596/979/1/012001.
Ginting EL, Kemer K, Wullur S, Uria AR. 2019. Identification of proteolytic thermophiles from Moinit coastal hot-spring, North Sulawesi, Indonesia. Geomicrobiology Journal 37 (1): 50-58. DOI: 10.1080/01490451.2019.1662524.
Gomes I, Gomes J, Steiner W. 2003. Highly thermostable amylase and pullulanase of the extreme thermophilic eubacterium Rhodothermus marinus: production and partial characterization. Bioresour Technol 90: 207-214. DOI: 10.1016/s0960-8524(03)00110-x.
Gugliandolo C, Lentini V, Spano A, Maugeri TL. 2012. New bacilli from shallow hydrothermal vents of Panarea Island (Italy) and their biotechnological potential. Journal of Applied Microbiology 112: 1102-1112. DOI: 10.1111/j.1365-2672.2012.05272.x.
Jiang T, Menghao MC, Huang M, He H, Lu J, Zhou X, Zhang Y. 2015. Characterization of a thermostable raw-starch hydrolyzing a-amylase from deep-sea thermophile Geobacillus sp. Protein Expression and Purification 114: 15-22. DOI: 10.1016/j.pep.2015.06.002.
Kambourova M. 2018. Thermostable enzymes and polysaccharides produced by thermophilic bacteria isolated from Bulgarian hot springs. Eng. Life sci. 18:758-767. DOI: 10.1002/elsc.201800022.
Keller M, Loder AJ, Basen M, Izquierdo J, Kelly RM, Adams MW. 2014. Production of lignofuels and electrofuels by extremely thermophilic microbes. Biofuels 5: 499-515. DOI: 10.1080/17597269.2014.996729.
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.
Luang-In V, Yotchaisarn M, Saengha W, Udomwong P, Deeseenthum S, Maneewan K. 2019. Isolation and identification of amylase-producing bacteria from soil in Nasinuan Community Forest, Maha Sarakham, Thailand. Biomedical & Pharmacology Journal 12: 1061-1068. DOI: 10.13005/bpj/1735.
Mohammad BT, Al Daghistani HI, Jaouani A, Abdel-Latif S, Kennes C. 2017. Isolation and characterization of thermophilic bacteria from Jordanian Hot Springs: Bacillus licheniformis and Thermomonas hydrothermalis isolates as potential producers of thermostable enzymes. Hindawi
International Journal of Microbiology, 2017: 1-12. DOI: 10.1155/2017/6943952.
Msarah MJ, Ibrahim I, Hamid AA, Aqma WS. 2020. Optimisation and production of alpha amylase from thermophilic Bacillus spp. and its application in food waste biodegradation. Heliyon 6: 1-9. DOI: 10.1016/j.heliyon.2020.e04183.
Myung-Ji S, Kim J, Pyun Y. 2012. 16S rRNA Gene sequence-based microbial diversity analyses of the geothermal areas of Cisolok, Kamojang, and Likupang in Indonesia. Korean J Microbiol Biotechnol 40 (3): 268-273. DOI: 10.4014/kjmb.1205.05001.
Nazina T, Tourova T, Poltaraus A, Novikova E, Grigoryan A, Ivanova A, Lysenko A, Petrunyaka V, Osipov G, Belyaev S, Ivanov M. 2001. Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov.and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermoglucosidasius and Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasiusand, G. thermodenitrificans. Int J Syst Evol Microbiol 51 (2): 433-446. DOI: 10.1099/00207713-51-2-433.
Nazina TN, Sokolova DS, Grigoryan AA, Shestakova NM, Mikhailova EM, Poltaraus AB. 2005. Geobacillus jurassicus sp. nov., a new thermophilic bacterium isolated from a high-temperature petroleum reservoir, and the validation of the Geobacillus species. Syst Appl Microbiol 28: 43-53. DOI: 10.1016/j.syapm.2004.09.001.
Nguyen QD, Rezessy-Szabó JM, Claeyssens M, Stals I, Hoschke A. 2002. Purification and characterization of amylolytic enzymes from thermophilic fungus Thermomyces lanuginosus strain ATCC 34626. Enzyme Microb Technol 31 (3): 345-52. DOI: 10.1016/S0141-0229(02)00128-X.
Nihaya I, Sarjono PR, Aminin ALN. 2013. Studi filogeni dan uji potensi antibakteri serta enzim ekstraseluler isolat Geobacillus sp. dari sumber air panas Gedongsongo. Jurnal Kimia Sains dan Aplikasi 16: 38- 41. DOI: 10.14710/jksa.16.2.38-41 [Indonesian].
Oziengbe EO, Onilude AA. 2012. Production of a thermostable ?-amylase and its assay using Bacillus licheniformis isolated from excavated land sites in Ibadan, Nigeria. Bayero Journal of Pure and Applied Sciences 5 (1): 132-138. DOI: 10.4314/bajopas.v5i1.24.
Poletto TV, Vieira CRW, Silva CP, Fracalossi DM. 2018. Isolation and identification of a potential amylolytic probiotic bacterium from the gut of Jundiá catfish. Rhamdia Quelen Braz Arch Biol Technol 61: 1-9. DOI: 10.1590/1678-4324-2018161205.
Prakash O, Jaiswal N. 2010. Alpha-amylase: An ideal representative of thermostable enzymes. Appl Biochem Biotechnol 160: 2401-2414. DOI: 10.1007/s12010-009-8735-4.
Raddadi N, Cherif A, Daffonchio D, Neifar M, Fava F. 2015. Biotechnological applications of extremophiles, extremozymes and extremolytes. Appl Microbiol Biotechnol 99 (19): 7907-7913. DOI: 10.1007/s00253-015-6874-9.
Satrimafitrah P, Razak AR, Hardi J, Puspitasari DJ, Yelenggete I, Rafik. 2020. Thermostable amylase activity produced by thermophilic bacteria isolated from Pulu Hotspring, Central Sulawesi. J. Phys.: Conf. Ser. 1434. National Seminar on Physics, Palu, 28 September 2019. DOI: 10.1088/1742-6596/1434/1/012034.
Sharma P, Gupta S, Sourirajan A, Dev K. 2015. Characterization of extracellular thermophilic amylase from Geobacillus sp. isolated from Tattapani Hot Spring of Himachal Pradesh, India. Current Biotechnology 4 (2): 202-209. DOI: 10.2174/2211550104666150612223748.
Singh G, Bhalla A, Kaur P, Capalash N, Sharma P. 2011. Laccase from prokaryotes: A new source for an old enzyme. Reviews in Environmental Science and Biotechnology 10: 309-326. DOI: 10.1007/s11157-011-9257-4.
Thairu Y, Nasir IA, Usman Y. 2014. Laboratory Perspective of Gram Staining and its Significance in Investigations of Infectious Diseases. Sub-Saharan African Journal of Medicine, 1: 168-174. DOI: 10.4103/2384-5147.144725.
Wantania LL, Wullur S, Ginting EL, Mantiri DM, Undap SL, Sumilat DA, Gerung GS. 2019. Isolation and amplification of 16S rRNA gen of associated microbial isolates in red algae Kappaphycus alvarezii from Belang, Southeast Minahasa Regency, North Sulawesi. Jurnal Ilmiah Platax 7 (1): 220-226. DOI: https://doi.org/10.35800/jip.7.1.2019.22808 [Indonesian]
Wullur S, Napitupulu H, Wantania LL, Ginting EL, Warouw V, Tilaar SO, Tallei TE, Rumengan IFM. 2020. Molecular identification of bacteria isolated from culture medium of rotifer fed on fishery waste diet. Biodiversitas 21 (6): 1735-1740. DOI: 10.13057/biodiv/d210649.
Zeigler DR. 2005. Application of a recN sequence similarity analysis to the identification of species within the bacterial genus Geobacillus. Int J Syst Evol Microbiol 55: 1171-1179. DOI: 10.1099/ijs.0.63452-0.
Zhang RY, Bin Z, Yan YW, Jeon CO, Li M, Cai M, Quan ZX. 2020. Design of targeted primers based on 16S rRNA sequences in meta-transcriptomic datasets and identification of a novel taxonomic group in the Asgard archaea. BMC Microbiology 20: 1-10. DOI: 10.1186/s12866-020-1707-0.
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