Lipolytic bacteria and the dynamics of flavor production in Indonesian tempeh
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Abstract. Nur N, Meryandini A, Suhartono MT, Suwanto A. 2020 Lipolytic bacteria and the dynamics of flavor production in Indonesian Tempeh. Biodiversitas 21: 3818-3825. During the process of tempeh maturation, lipolytic bacteria become an integral part of tempeh and even have important roles in determining the quality of resulting tempeh. This study was conducted to examine correlation between lipolytic bacteria which were present in three tempeh samples i.e. CMG, EMP, RTI, and their roles in liberation of free fatty acid. Lipolytic bacteria were found in each tempeh sample which were approximately 0.1 % of total bacterial population. CMG harbored the highest lipolytic bacterial population at 1.04 × 106 cfu g-1 followed by EMP at 2.88 × 105 cfu g-1, and RTI at 1.72 × 104 cfu g-1. Tempeh aroma and texture showed strong correlation between the numbers of bacterial population during the period or stages of tempeh maturation. Moreover, we also found a unique correlation between dynamic of lipolytic population and aroma changes. Free fatty acid profiling indicates that lipolysis activity was presence during fermentation of tempe where each tempeh samples showed some differences in liberation of dominant free fatty acid. 16S rRNA sequencing from a hundred of lipolytic isolates was identified and classified as member of the phylum Proteobacteria, Firmicutes, and Actinobacteria, other isolates were classified as uncultured clone.
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References
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Astuti M, Meliala A, Dalais FS, Wahlqvist ML. 2000. Tempe, a nutritious and healthy food from Indonesia. Asia Pacific J Clin Nutr. 9(4): 322–325. DOI: 10.1046/j.1440-6047.2000.00176.x.
Babu PD, Bhakyaraj R, Vidhyalakshmi R. 2009. A low cost nutritious food “Tempeh” – a review. World J Dairy Food Sci. 4(1): 22-27.
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Cappuccino JG, Sherman N. 2001. Microbiology A Laboratory Manual. Benjamin Cummings, New York.
Carvalho SM, Mendonça MA, Pinho DMM, Resck IS, Suarez PAZ. 2012. Chromatographic analyses of fatty acid methyl esters by HPLC-UV and GC-FID. J Braz Chem Soc. 23(4): 763-769. DOI: 10.1590/S0103-50532012000400023.
Christen P, López?Munguía A. 2009. Enzymes and food flavor?A review. Food Biotechnol. 8 (2-3): 167-190. DOI 10.1080/08905439409549874.
Feller G, Thiry M, Gerday C. 1991. Nucleotide sequence of the lipase gene lip2 from the antarctic psychrotroph Moraxella TA144 and site-specific mutagenesis of the conserved serine and histidine residues. DNA Cell Biol. 10(5): 381-388. DOI: 10.1089/dna.1991.10.381.
Fox PF, Guinee TP, Cogan TM, McSweeney PLH. 2000. Fundamentals of Cheese Science. Aspen Publishers Inc, Gaithersburg.
Fox PF, Wallace JM. 1997. Formation of flavour compounds in cheese. Advan App Microbiol. 45: 17–85. DOI: 10.1016/s0065-2164(08)70261-2.
Gunasekaran V, Kotay SM, Das D. 2006. Alkaline lipase production by Citrobacter freundii IIT-BT L139. Indian J Exp Biol. 44(6): 485-491.
Gunawan-Puteri MDPT, Hassanein TR, Prabawati EK, Wijaya CH, Mutukumira AN. 2015. Sensory characteristics of seasoning powders from overripe tempeh, a solid state fermented soybean. Proced Chem. 14: 263-269. DOI: 10.1016/j.proche.2015.03.037.
Hagedorn S, Kaphammer B. 1994. Microbial biocatalysis in the generation of flavor and fragrance chemical. Annu Rev Microbiol. 48: 773-800. DOI: 10.1146/annurev.mi.48.100194.004013.
Hassaenin TR, Prabawati EK, Gunawan-Puteri MDPT. 2015. Analysis of chemical and microbial changes during storage of overripe tempeh powder as seasoning material. Inter J Sci Eng. 8(2): 131-134. DOI: 10.12777/ijse.8.2.131-134.
Jarvis GN, Strömpl C, Moore ERB, Thiele JH. 1997. Isolation and characterisation of obligately anaerobic, lipolytic bacteria from the rumen of red deer. Syst Appl Microbiol. 21(1): 135-43. DOI: 10.1016/S0723-2020(98)80017-9.
Keuth S, Bisping B. 1994. Vitamin B12 production by Citrobacter freundii or Klebsiella pneumonia during tempeh fermentation and proof of enterotoxin absence by PCR. Appl Environ Microbiol. 60(5): 1495-1499.
Klus K, Borger-Papendorf G, Barz W. 1993. Formation of 6,7,4 tryhidroxyisoflavone (factor 2) from soybean seed isoflavone by bacteria isolated from tempe. J Phytochem 34:979-981.
Korman TP, Bowie JU. 2012. Crystal Structure of Proteus mirabilis Lipase, a Novel lipase from the proteus/psychrophilic subfamily of lipase family I.1. PlosONE. 7(12): e52890. DOI: 10.1371/journal.pone.0052890
Kouker G, Jaeger KE. 1987. Specific and sensitive plate assay for bacterial lipases. Appl Environ Microbiol. 53: 211–213.
Kumar D, kumar L, Nagar S, Raina C, Parshad R, Gupta VK. 2012a. Screening, isolation and production of lipase/esterase producing Bacillus sp . strain DVL 2 and its potential evaluation in esterification and resolution reactions. Arc App Sci Res. 4(4): 1763-1770.
Leitao MFF, Menezes TJB, Tango JS. 1967. Production of tempeh - a fermented soy product. Coletanea do Instituto de Tecnologia de Alimentos Campinas. 2: 333-39.
Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG. 1998. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol. 64(2):795-799.
McSweeney PLH, Sousa MJ. 2000. Biochemical pathways for the production of flavour compounds in cheeses during ripening: A review. Le Lait. 80: 293-324. DOI: 10.1051/lait:2000127
Mienda BS, Idi A, Umar A. 2011. Microbiological features of solid state fermentation and its applications - an overview. Res Biotechnol. 2(6): 21-26.
Nawar WW. 1996. Lipids. In: Fennema, O.R. (eds). Food chemistry, third ed. Marcel Dekker in, New York.
Olivares A, Navvaro JL, Flores M. 2011. Effect of fat content on aroma generation during processing of dry fermented sausages. Meat Sci. 87: 264-273. DOI: 10.1016/j.meatsci.2010.10.021.
Ritvanen T, Lampolahti S, Lilleberg L, Tupasela T, Isoniemi M, Appelbye U, Lyytikainen T, Eerola S, Uusi-Rauva E. 2005. Sensory evaluation, chemical composition and consumer acceptance of full fat and reduced fat cheeses in the Finnish market. Food Qual Pref. 16: 479-492. DOI: 10.1016/j.foodqual.2004.10.001.
Shurtleff W, Aoyagi A. 1979. The Book of Tempeh, A Cultured Soyfood, second edition. Ten Speed Press, California.
Snellman EA, Sullivan ER, Colwell RR. 2002. Purification and properties of the extracellular lipase, LipA, of Acinetobacter sp. RAG?1. Eur J Biochem. 269 (23): 5771-5779. DOI: 10.1046/j.1432-1033.2002.03235.x.
Utami R, Wijaya CH, Lioe HN. 2015. Taste of water-soluble extracts obtained from over-fermented tempe. Int J Food Prop. 19(9): 2063-2073. DOI: 10.1080/10942912.2015.1104509.
Woodman ME. Savage CR., Arnold WK, Stevenson B. 2016. Direct PCR of Intact Bacteria (Colony PCR). Curr Protoc Microbiol. 42: A.3D.1-A.3D.7. DOI:10.1002/cpmc.14.
Astuti M, Meliala A, Dalais FS, Wahlqvist ML. 2000. Tempe, a nutritious and healthy food from Indonesia. Asia Pacific J Clin Nutr. 9(4): 322–325. DOI: 10.1046/j.1440-6047.2000.00176.x.
Babu PD, Bhakyaraj R, Vidhyalakshmi R. 2009. A low cost nutritious food “Tempeh” – a review. World J Dairy Food Sci. 4(1): 22-27.
Barus T, Suwanto A, Wahyudi AT, Wijaya H. 2008. Role of bacteria in tempe bitter taste formation microbiological and molecular biological analysis based on 16S rRNA gene. Microbiol Indones. 2(1): 17-21. DOI: 10.5454/mi.2.1.4.
Cappuccino JG, Sherman N. 2001. Microbiology A Laboratory Manual. Benjamin Cummings, New York.
Carvalho SM, Mendonça MA, Pinho DMM, Resck IS, Suarez PAZ. 2012. Chromatographic analyses of fatty acid methyl esters by HPLC-UV and GC-FID. J Braz Chem Soc. 23(4): 763-769. DOI: 10.1590/S0103-50532012000400023.
Christen P, López?Munguía A. 2009. Enzymes and food flavor?A review. Food Biotechnol. 8 (2-3): 167-190. DOI 10.1080/08905439409549874.
Feller G, Thiry M, Gerday C. 1991. Nucleotide sequence of the lipase gene lip2 from the antarctic psychrotroph Moraxella TA144 and site-specific mutagenesis of the conserved serine and histidine residues. DNA Cell Biol. 10(5): 381-388. DOI: 10.1089/dna.1991.10.381.
Fox PF, Guinee TP, Cogan TM, McSweeney PLH. 2000. Fundamentals of Cheese Science. Aspen Publishers Inc, Gaithersburg.
Fox PF, Wallace JM. 1997. Formation of flavour compounds in cheese. Advan App Microbiol. 45: 17–85. DOI: 10.1016/s0065-2164(08)70261-2.
Gunasekaran V, Kotay SM, Das D. 2006. Alkaline lipase production by Citrobacter freundii IIT-BT L139. Indian J Exp Biol. 44(6): 485-491.
Gunawan-Puteri MDPT, Hassanein TR, Prabawati EK, Wijaya CH, Mutukumira AN. 2015. Sensory characteristics of seasoning powders from overripe tempeh, a solid state fermented soybean. Proced Chem. 14: 263-269. DOI: 10.1016/j.proche.2015.03.037.
Hagedorn S, Kaphammer B. 1994. Microbial biocatalysis in the generation of flavor and fragrance chemical. Annu Rev Microbiol. 48: 773-800. DOI: 10.1146/annurev.mi.48.100194.004013.
Hassaenin TR, Prabawati EK, Gunawan-Puteri MDPT. 2015. Analysis of chemical and microbial changes during storage of overripe tempeh powder as seasoning material. Inter J Sci Eng. 8(2): 131-134. DOI: 10.12777/ijse.8.2.131-134.
Jarvis GN, Strömpl C, Moore ERB, Thiele JH. 1997. Isolation and characterisation of obligately anaerobic, lipolytic bacteria from the rumen of red deer. Syst Appl Microbiol. 21(1): 135-43. DOI: 10.1016/S0723-2020(98)80017-9.
Keuth S, Bisping B. 1994. Vitamin B12 production by Citrobacter freundii or Klebsiella pneumonia during tempeh fermentation and proof of enterotoxin absence by PCR. Appl Environ Microbiol. 60(5): 1495-1499.
Klus K, Borger-Papendorf G, Barz W. 1993. Formation of 6,7,4 tryhidroxyisoflavone (factor 2) from soybean seed isoflavone by bacteria isolated from tempe. J Phytochem 34:979-981.
Korman TP, Bowie JU. 2012. Crystal Structure of Proteus mirabilis Lipase, a Novel lipase from the proteus/psychrophilic subfamily of lipase family I.1. PlosONE. 7(12): e52890. DOI: 10.1371/journal.pone.0052890
Kouker G, Jaeger KE. 1987. Specific and sensitive plate assay for bacterial lipases. Appl Environ Microbiol. 53: 211–213.
Kumar D, kumar L, Nagar S, Raina C, Parshad R, Gupta VK. 2012a. Screening, isolation and production of lipase/esterase producing Bacillus sp . strain DVL 2 and its potential evaluation in esterification and resolution reactions. Arc App Sci Res. 4(4): 1763-1770.
Leitao MFF, Menezes TJB, Tango JS. 1967. Production of tempeh - a fermented soy product. Coletanea do Instituto de Tecnologia de Alimentos Campinas. 2: 333-39.
Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG. 1998. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microbiol. 64(2):795-799.
McSweeney PLH, Sousa MJ. 2000. Biochemical pathways for the production of flavour compounds in cheeses during ripening: A review. Le Lait. 80: 293-324. DOI: 10.1051/lait:2000127
Mienda BS, Idi A, Umar A. 2011. Microbiological features of solid state fermentation and its applications - an overview. Res Biotechnol. 2(6): 21-26.
Nawar WW. 1996. Lipids. In: Fennema, O.R. (eds). Food chemistry, third ed. Marcel Dekker in, New York.
Olivares A, Navvaro JL, Flores M. 2011. Effect of fat content on aroma generation during processing of dry fermented sausages. Meat Sci. 87: 264-273. DOI: 10.1016/j.meatsci.2010.10.021.
Ritvanen T, Lampolahti S, Lilleberg L, Tupasela T, Isoniemi M, Appelbye U, Lyytikainen T, Eerola S, Uusi-Rauva E. 2005. Sensory evaluation, chemical composition and consumer acceptance of full fat and reduced fat cheeses in the Finnish market. Food Qual Pref. 16: 479-492. DOI: 10.1016/j.foodqual.2004.10.001.
Shurtleff W, Aoyagi A. 1979. The Book of Tempeh, A Cultured Soyfood, second edition. Ten Speed Press, California.
Snellman EA, Sullivan ER, Colwell RR. 2002. Purification and properties of the extracellular lipase, LipA, of Acinetobacter sp. RAG?1. Eur J Biochem. 269 (23): 5771-5779. DOI: 10.1046/j.1432-1033.2002.03235.x.
Utami R, Wijaya CH, Lioe HN. 2015. Taste of water-soluble extracts obtained from over-fermented tempe. Int J Food Prop. 19(9): 2063-2073. DOI: 10.1080/10942912.2015.1104509.
Woodman ME. Savage CR., Arnold WK, Stevenson B. 2016. Direct PCR of Intact Bacteria (Colony PCR). Curr Protoc Microbiol. 42: A.3D.1-A.3D.7. DOI:10.1002/cpmc.14.
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