Isolation, identification and antimicrobial activities of Lactic Acid Bacteria from fruits of wild plants in Tambrauw Forest, West Papua, Indonesia
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Abstract. Dinoto A, Rosyidah A, Susilo ARPS, Julistiono H. 2020. Isolation, identification and antimicrobial activities of Lactic Acid Bacteria from fruits of wild plants in Tambrauw Forest, West Papua, Indonesia. Biodiversitas 21: 3391-3397. Presence of culturable lactic acid bacteria (LAB) in fruits of wild plants and their antimicrobial activities has not been widely reported. The purposes of this study were to isolate LAB from the fruits of wild plants found in the Tambrauw forest area, West Papua Indonesia, and to evaluate their antimicrobial activities. Isolation of LAB from fruit was conducted using MRS medium supplemented with 1% CaCO3. Isolates of LAB were identified based on 16S rRNA gene using BLAST analysis. Antimicrobial assays were carried out by determining the minimum inhibitory concentration (MIC) based on thiazolyl blue tetrazolium blue (MTT) using indicator microorganisms Escherichia coli, Staphylococcus aureus, and Mycobacterium smegmatis. The results showed that total of fourteen isolates of LAB with different characteristics was successfully isolated from 8 of 14 collected wild plants. Based on 16S rRNA sequences, isolates had closest relationships with Lactococcus lactis, Lactococcus garvieae, Weissella confusa, Weissella oryzae, and Enterococcus faecalis with the similarity of 99%. All 16S rRNA nucleotides of these strains have been deposited in the GenBank. Assays for antimicrobial activities were demonstrated by the highest inhibition of supernatant of Lac. lactis HM 1.1 from fruit plant Donax canniformis and W. confusa H14.2 from fruit plant Capparis sp. against E. coli, S. aureus, and M. smegmatis even though the MIC values of those strains were lower than that of bacterial strain from the commercial probiotic product. This study showed that wild fruit from Tambrauw forest harbor beneficial lactic acid bacteria that could be important for health of animals and humans as well. In addition, this study provided basic information on indigenous LAB for promoting further development of medicinal antibacterial compounds.
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References
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Barth M, Hankinson TR, Zhuang H, Breidt F. 2009. Microbiological spoilage of foods and beverages. In: Sperbe WH, Doyle MP (eds) Compendium of the Microbiological Spoilage of Foods and Beverages, pp. 135–183. Springer Science+Business Media, New York. doi:10.1007/978-1-4419-0826-1.
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Chen Y, Wang L, Liao Y, Lan Y, Chang C, Chang Y, Wu H, Lo H, Otoguro M, Yanagida F. 2017. Lactobacillus musae sp. nov., a novel lactic acid bacterium isolated from banana fruits. Int J Syst Evol Microbiol 67: 5144–5149. doi:10.1099/ijsem.0.002429.
Chen Y, Wu H, Yanagida F. 2010. Isolation and characterization of lactic acid bacteria from ripe mulberries in Taiwan. Braz J Microbiol 41: 916–921.
Choi JI, Yoon KH, Kalichamy SS, Yoon SS, Lee JI. 2016. A natural odor attraction between lactic acid bacteria and the nematode Caenorhabditis elegans. ISME J 10: 558–567. doi:10.1038/ismej.2015.134.
Cotter PD, Ross RP, Hill C. 2013. Bacteriocins - a viable alternative to antibiotics? Nat Rev Microbiol 11 (2): 95–105. doi:10.1038/nrmicro2937.
de Godoy I, Moraes DFSD, Pitchenin LC, Rosa JMA, Kagueyama FC, da Silva AJ, Dutra V, Nakazato L. 2016. Antimicrobial susceptibility profiles of Staphylococcus spp. from domestic and wild animals. Cienc Rural 46 (12): 2148–51. doi:10.1590/0103-8478cr20160373.
El Baz A, Shetaia YM. 2005. Evaluation of different assays for the activity of yeast killer toxin. Int J Agric Biol 7 (6): 1003–1006.
Emerenini EC, Afolabi OR, Okolie PI, Akintokun AK. 2013. Isolation and molecular characterization of lactic acid bacteria isolated from fresh fruits and vegetables using nested PCR analysis. Br Microbiol Res J 3 (3): 368–377. doi:10.9734/BMRJ/2013/2520
Endo A. 2012. Fructophilic lactic acid bacteria inhabit fructose-rich niches in nature. Microb Ecol Health Dis 23: 6–9. doi:10.3402/mehd.v23i0.18563.
Fairfax MR, Lephart PR, Salimnia H. 2014. Weissella confusa: problems with identification of an opportunistic pathogen that has been found in fermented foods and proposed as a probiotic. Front Microbiol 5: 254. doi:10.3389/fmicb.2014.00254.
Ferrario C, Ricci G, Milani C, Lugli GA, Ventura M, Eraclio G, Borgo F, Fortina MG. 2013. Lactococcus garvieae: where is it from? A first approach to explore the evolutionary history of this emerging pathogen. PLoS ONE 8 (12): e84796. doi:10.1371/journal.pone.0084796.
Gowri RS, Meenambigai P, Prabhavathi P, Raja Rajeswari P, Yesudoss LA. 2016. Probiotics and its effects on human health - A review. Int J Curr Microbiol Appl Sci 5 (4): 384–392. doi:10.20546/ijcmas.2016.504.046.
Grosu-Tudor SS, Stancu MM, Pelinescu D, Zamfir M. 2014. Characterization of some bacteriocins produced by lactic acid bacteria isolated from fermented foods. World J Microbiol Biotechnol 30 (9): 2459–2469. doi:10.1007/s11274-014-1671-7.
Hwanhlem N, Chobert JM, H-Kittikun A. 2014. Bacteriocin-producing lactic acid bacteria isolated from mangrove forests in southern Thailand as potential bio-control agents in food: Isolation, screening and optimization. Food Control 41: 202–211. doi:10.1016/j.foodcont.2014.01.021.
Iovine RO, Dejuste C, Miranda F, Filoni C, Bueno MG, de Carvalho VM. 2015. Isolation of Escherichia coli and Salmonella spp. from free-ranging wild animals. Braz J Microbiol 46 (4): 1257–1263. doi:10.1590/s1517-838246420140843.
Kamaladevi A, Ganguli A, Balamurugan K. 2016. Lactobacillus casei stimulates phase-II detoxification system and rescues malathion-induced physiological impairments in Caenorhabditis elegans. Comp Biochem Physiol C Toxicol Pharmacol 179: 19–28. doi:10.1016/j.cbpc.2015.08.004.
Kamaladevi A, Ganguli A, Kumar M, Balamurugan K. 2013. Lactobacillus casei protects malathion induced oxidative stress and macromolecular changes in Caenorhabditis elegans. Pestic Biochem Phys 105 (3): 213–223. doi:10.1016/j.pestbp.2013.02.005.
Karyawati AT, Nuraida L, Lestari Y, Meryandini A. 2018. Characterization of abundance and diversity of lactic acid bacteria from Apis dorsata hives and flowers in East Nusa Tenggara, Indonesia. Biodiversitas 19 (3): 899-905. doi:10.13057/biodiv/d190319.
Lane DJ, Pace B, Olsen GJ, Stahlt DA, Sogint ML, Pace NR. 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. PNAS 82: 6955–6959.
Leong K, Chen Y, Pan S, Chen J, Wu H, Chang Y, Yanagida F. 2014. Diversity of lactic acid bacteria associated with fresh coffee cherries in Taiwan. Curr Microbiol 68: 440–447. doi:10.1007/s00284-013-0495-2.
Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A et al. 2006. Comparative genomics of the lactic acid bacteria. PNAS 103 (42): 15611–15616. doi:10.1073/pnas.0607117103.
Mangunwardoyo W, Salamah A, Sukara E, Sulistiani, Dinoto A. 2016. Diversity and distribution of culturable lactic acid bacterial species in Indonesian Sayur Asin. Iran J Microbiol 8 (4): 274–281.
Maria M, Janakiraman S. 2012. Detection of heat stable bacteriocin from Lactobacillus acidophilus NCIM5426 by liquid chromatography/mass spectrometry. Indian J Sci Technol 5 (3): 2325–2332.
Moodley S, Koorbanally NA, Moodley T, Ramjugernath D, Pillay M. 2014. The 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) assay is a rapid, cheap, screening test for the in vitro anti-tuberculous activity of chalcones. J. Microbiol Methods 104: 72–78. doi:10.1016/j.mimet.2014.06.014.
Morita H, Toh H, Oshima K, Yoshizaki M, Kawanishi M, Nakaya K, Suzuki T et al. 2011. Complete genome sequence and comparative analysis of the fish pathogen Lactococcus garvieae. PLoS ONE 6 (8): e23184. doi:10.1371/journal.pone.0023184.
Ray RC, Montet D, Zakhia-Rozis N. 2014. Lactic acid fermentation of vegetables and fruits. In: Ray RC, Montet D (eds) Microorganisms and Fermentation of Traditional Foods, pp. 108–140. CRC Press, Boca Raton. doi:10.13140/2.1.2374.1127.
Reis JA, Paula AT, Casarotti SN, Penna ALB. 2012. Lactic acid bacteria antimicrobial compounds: characteristics and applications. Food Eng Rev 4 (2): 124–140. doi:10.1007/s12393-012-9051-2.
Robiansyah I. 2018. Diversity and biomass of tree species in Tambrauw, West Papua, Indonesia. Biodiversitas 19 (2): 377–386. doi:10.13057/biodiv/d190204.
Saito H, Miura K-I. 1963. Preparation of transforming deoxyribonucleic acid by phenol treatment. Biochim Biophysi Acta 72: 619–629.
Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 (4): 406–425.
Sangari FJ, Goodman J, Petrofsky M, Kolonoski P, Bermudez LE. 2001. Mycobacterium avium invades the intestinal mucosa primarily by interacting with enterocytes. Infect Immun 69 (3): 1515–1520. doi:10.1128/iai.69.3.1515-1520.2001.
Sosunov V, Mischenko V, Eruslanov B, Svetoch E, Shakina Y, Stern N, Majorov K, Sorokoumova G, Selishcheva A, Apt A. 2007. Antimycobacterial activity of bacteriocins and their complexes with liposomes. J Antimicrob Chemoth 59 (5): 919–925. doi:10.1093/jac/dkm053.
Sulistiani, Abinawanto, Sukara E, Salamah A, Dinoto A, Mangunwardoyo W. 2014. Identification of lactic acid bacteria in sayur asin from Central Java (Indonesia) based on 16S rDNA sequence. Int Food Res J 21 (2): 527–532.
Swain MR, Anandharaj M, Ray RC, Rani RP. 2014. Fermented fruits and vegetables of Asia: A potential source of probiotics. Biotechnol Res Int 2014: 250424. doi:10.1155/2014/250424.
Tanizawa Y, Fujisawa T, Mochizuki T, Kaminuma E, Suzuki Y, Nakamura Y, Tohno M. 2014. Draft genome sequence of Weissella oryzae SG25T, isolated from fermented rice grains. Genome Announc 2 (4): e00667. doi:0.1128/genomeA.00667-14.
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL _ X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25 (24): 4876–4882.
Tohno M, Kitahara M, Inoue H, Uegaki R, Irisawa T, Ohkuma M, Tajima K. 2013. Weissella oryzae sp. nov., isolated from fermented rice grains. Int J Syst Evol Microbiol 63: 1417–1420. doi:10.1099/ijs.0.043612-0.
Tsuchida S, Takahashi S, Nguema MPP, Fujita S, Kitahara M, Yamagiwa J, Ngomanda A, Ohkuma M, Ushida K. 2014. Bifidobacterium moukalabense sp. nov., isolated from the faeces of wild west lowland gorilla (Gorilla gorilla gorilla). Int J Syst Evol Microbiol 64: 449–455. doi:10.1099/ijs.0.055186-0.
Wanger A. 2007. Disk diffusion test and gradient methodologies. In: Schwalbe R, Steele-Moore L, Goodwin AC (eds) Antimicrobial Susceptibility Testing Protocols, pp. 53–73. CRC Press, New York. doi:10.1201/9781420014495.ch3.
Yu C, Hui L, Yanagida F. 2017. Diversity of lactic acid bacteria associated with banana fruits in Taiwan. Curr Microbiol 74 (4): 484–490. doi:10.1007/s00284-017-1213-2.
Ali AA. 2010. Beneficial role of lactic acid bacteria in food preservation and human health: A review. Res J Microbiol 5 (12): 1213–1221. doi:10.3923/jm.2010.1213.1221.
Bae S, Fleet GH, Heard GM. 2006. Lactic acid bacteria associated with wine grapes from several Australian vineyards. J Appl Microbiol 100: 712–727. doi:10.1111/j.1365-2672.2006.02890.x.
Barth M, Hankinson TR, Zhuang H, Breidt F. 2009. Microbiological spoilage of foods and beverages. In: Sperbe WH, Doyle MP (eds) Compendium of the Microbiological Spoilage of Foods and Beverages, pp. 135–183. Springer Science+Business Media, New York. doi:10.1007/978-1-4419-0826-1.
Benavides AB, Ulcuango M, Yépez L, Tenea GN. 2016. Assessment of the in vitro bioactive properties of lactic acid bacteria isolated from native ecological niches of Ecuador. Rev Argent Microbiol 48 (3): 236–244. doi:10.1016/j.ram.2016.05.003.
Chen Y, Wang L, Liao Y, Lan Y, Chang C, Chang Y, Wu H, Lo H, Otoguro M, Yanagida F. 2017. Lactobacillus musae sp. nov., a novel lactic acid bacterium isolated from banana fruits. Int J Syst Evol Microbiol 67: 5144–5149. doi:10.1099/ijsem.0.002429.
Chen Y, Wu H, Yanagida F. 2010. Isolation and characterization of lactic acid bacteria from ripe mulberries in Taiwan. Braz J Microbiol 41: 916–921.
Choi JI, Yoon KH, Kalichamy SS, Yoon SS, Lee JI. 2016. A natural odor attraction between lactic acid bacteria and the nematode Caenorhabditis elegans. ISME J 10: 558–567. doi:10.1038/ismej.2015.134.
Cotter PD, Ross RP, Hill C. 2013. Bacteriocins - a viable alternative to antibiotics? Nat Rev Microbiol 11 (2): 95–105. doi:10.1038/nrmicro2937.
de Godoy I, Moraes DFSD, Pitchenin LC, Rosa JMA, Kagueyama FC, da Silva AJ, Dutra V, Nakazato L. 2016. Antimicrobial susceptibility profiles of Staphylococcus spp. from domestic and wild animals. Cienc Rural 46 (12): 2148–51. doi:10.1590/0103-8478cr20160373.
El Baz A, Shetaia YM. 2005. Evaluation of different assays for the activity of yeast killer toxin. Int J Agric Biol 7 (6): 1003–1006.
Emerenini EC, Afolabi OR, Okolie PI, Akintokun AK. 2013. Isolation and molecular characterization of lactic acid bacteria isolated from fresh fruits and vegetables using nested PCR analysis. Br Microbiol Res J 3 (3): 368–377. doi:10.9734/BMRJ/2013/2520
Endo A. 2012. Fructophilic lactic acid bacteria inhabit fructose-rich niches in nature. Microb Ecol Health Dis 23: 6–9. doi:10.3402/mehd.v23i0.18563.
Fairfax MR, Lephart PR, Salimnia H. 2014. Weissella confusa: problems with identification of an opportunistic pathogen that has been found in fermented foods and proposed as a probiotic. Front Microbiol 5: 254. doi:10.3389/fmicb.2014.00254.
Ferrario C, Ricci G, Milani C, Lugli GA, Ventura M, Eraclio G, Borgo F, Fortina MG. 2013. Lactococcus garvieae: where is it from? A first approach to explore the evolutionary history of this emerging pathogen. PLoS ONE 8 (12): e84796. doi:10.1371/journal.pone.0084796.
Gowri RS, Meenambigai P, Prabhavathi P, Raja Rajeswari P, Yesudoss LA. 2016. Probiotics and its effects on human health - A review. Int J Curr Microbiol Appl Sci 5 (4): 384–392. doi:10.20546/ijcmas.2016.504.046.
Grosu-Tudor SS, Stancu MM, Pelinescu D, Zamfir M. 2014. Characterization of some bacteriocins produced by lactic acid bacteria isolated from fermented foods. World J Microbiol Biotechnol 30 (9): 2459–2469. doi:10.1007/s11274-014-1671-7.
Hwanhlem N, Chobert JM, H-Kittikun A. 2014. Bacteriocin-producing lactic acid bacteria isolated from mangrove forests in southern Thailand as potential bio-control agents in food: Isolation, screening and optimization. Food Control 41: 202–211. doi:10.1016/j.foodcont.2014.01.021.
Iovine RO, Dejuste C, Miranda F, Filoni C, Bueno MG, de Carvalho VM. 2015. Isolation of Escherichia coli and Salmonella spp. from free-ranging wild animals. Braz J Microbiol 46 (4): 1257–1263. doi:10.1590/s1517-838246420140843.
Kamaladevi A, Ganguli A, Balamurugan K. 2016. Lactobacillus casei stimulates phase-II detoxification system and rescues malathion-induced physiological impairments in Caenorhabditis elegans. Comp Biochem Physiol C Toxicol Pharmacol 179: 19–28. doi:10.1016/j.cbpc.2015.08.004.
Kamaladevi A, Ganguli A, Kumar M, Balamurugan K. 2013. Lactobacillus casei protects malathion induced oxidative stress and macromolecular changes in Caenorhabditis elegans. Pestic Biochem Phys 105 (3): 213–223. doi:10.1016/j.pestbp.2013.02.005.
Karyawati AT, Nuraida L, Lestari Y, Meryandini A. 2018. Characterization of abundance and diversity of lactic acid bacteria from Apis dorsata hives and flowers in East Nusa Tenggara, Indonesia. Biodiversitas 19 (3): 899-905. doi:10.13057/biodiv/d190319.
Lane DJ, Pace B, Olsen GJ, Stahlt DA, Sogint ML, Pace NR. 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. PNAS 82: 6955–6959.
Leong K, Chen Y, Pan S, Chen J, Wu H, Chang Y, Yanagida F. 2014. Diversity of lactic acid bacteria associated with fresh coffee cherries in Taiwan. Curr Microbiol 68: 440–447. doi:10.1007/s00284-013-0495-2.
Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A et al. 2006. Comparative genomics of the lactic acid bacteria. PNAS 103 (42): 15611–15616. doi:10.1073/pnas.0607117103.
Mangunwardoyo W, Salamah A, Sukara E, Sulistiani, Dinoto A. 2016. Diversity and distribution of culturable lactic acid bacterial species in Indonesian Sayur Asin. Iran J Microbiol 8 (4): 274–281.
Maria M, Janakiraman S. 2012. Detection of heat stable bacteriocin from Lactobacillus acidophilus NCIM5426 by liquid chromatography/mass spectrometry. Indian J Sci Technol 5 (3): 2325–2332.
Moodley S, Koorbanally NA, Moodley T, Ramjugernath D, Pillay M. 2014. The 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) assay is a rapid, cheap, screening test for the in vitro anti-tuberculous activity of chalcones. J. Microbiol Methods 104: 72–78. doi:10.1016/j.mimet.2014.06.014.
Morita H, Toh H, Oshima K, Yoshizaki M, Kawanishi M, Nakaya K, Suzuki T et al. 2011. Complete genome sequence and comparative analysis of the fish pathogen Lactococcus garvieae. PLoS ONE 6 (8): e23184. doi:10.1371/journal.pone.0023184.
Ray RC, Montet D, Zakhia-Rozis N. 2014. Lactic acid fermentation of vegetables and fruits. In: Ray RC, Montet D (eds) Microorganisms and Fermentation of Traditional Foods, pp. 108–140. CRC Press, Boca Raton. doi:10.13140/2.1.2374.1127.
Reis JA, Paula AT, Casarotti SN, Penna ALB. 2012. Lactic acid bacteria antimicrobial compounds: characteristics and applications. Food Eng Rev 4 (2): 124–140. doi:10.1007/s12393-012-9051-2.
Robiansyah I. 2018. Diversity and biomass of tree species in Tambrauw, West Papua, Indonesia. Biodiversitas 19 (2): 377–386. doi:10.13057/biodiv/d190204.
Saito H, Miura K-I. 1963. Preparation of transforming deoxyribonucleic acid by phenol treatment. Biochim Biophysi Acta 72: 619–629.
Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 (4): 406–425.
Sangari FJ, Goodman J, Petrofsky M, Kolonoski P, Bermudez LE. 2001. Mycobacterium avium invades the intestinal mucosa primarily by interacting with enterocytes. Infect Immun 69 (3): 1515–1520. doi:10.1128/iai.69.3.1515-1520.2001.
Sosunov V, Mischenko V, Eruslanov B, Svetoch E, Shakina Y, Stern N, Majorov K, Sorokoumova G, Selishcheva A, Apt A. 2007. Antimycobacterial activity of bacteriocins and their complexes with liposomes. J Antimicrob Chemoth 59 (5): 919–925. doi:10.1093/jac/dkm053.
Sulistiani, Abinawanto, Sukara E, Salamah A, Dinoto A, Mangunwardoyo W. 2014. Identification of lactic acid bacteria in sayur asin from Central Java (Indonesia) based on 16S rDNA sequence. Int Food Res J 21 (2): 527–532.
Swain MR, Anandharaj M, Ray RC, Rani RP. 2014. Fermented fruits and vegetables of Asia: A potential source of probiotics. Biotechnol Res Int 2014: 250424. doi:10.1155/2014/250424.
Tanizawa Y, Fujisawa T, Mochizuki T, Kaminuma E, Suzuki Y, Nakamura Y, Tohno M. 2014. Draft genome sequence of Weissella oryzae SG25T, isolated from fermented rice grains. Genome Announc 2 (4): e00667. doi:0.1128/genomeA.00667-14.
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL _ X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25 (24): 4876–4882.
Tohno M, Kitahara M, Inoue H, Uegaki R, Irisawa T, Ohkuma M, Tajima K. 2013. Weissella oryzae sp. nov., isolated from fermented rice grains. Int J Syst Evol Microbiol 63: 1417–1420. doi:10.1099/ijs.0.043612-0.
Tsuchida S, Takahashi S, Nguema MPP, Fujita S, Kitahara M, Yamagiwa J, Ngomanda A, Ohkuma M, Ushida K. 2014. Bifidobacterium moukalabense sp. nov., isolated from the faeces of wild west lowland gorilla (Gorilla gorilla gorilla). Int J Syst Evol Microbiol 64: 449–455. doi:10.1099/ijs.0.055186-0.
Wanger A. 2007. Disk diffusion test and gradient methodologies. In: Schwalbe R, Steele-Moore L, Goodwin AC (eds) Antimicrobial Susceptibility Testing Protocols, pp. 53–73. CRC Press, New York. doi:10.1201/9781420014495.ch3.
Yu C, Hui L, Yanagida F. 2017. Diversity of lactic acid bacteria associated with banana fruits in Taiwan. Curr Microbiol 74 (4): 484–490. doi:10.1007/s00284-017-1213-2.
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