Hydroxycinnamic acids used as external acceptors of electrons: An energetic advantage for strictly heterofermentative lactic acid bacteria

Applied and Environmental Microbiology

Volumn 80, Issue 24, 2014, Pages 7574-7582

  Filannino, Pasquale ^a   Gobbetti, Marco ^a   De Angelis, Maria ^a   Di Cagno, Raffaella ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CARBON; ENZYME ACTIVITY; METABOLISM; PHYSIOLOGY; VOLATILE FATTY ACIDS;

ALCOHOL DEHYDROGENASE; CONCENTRATION OF ACETIC ACID; HYDROXYCINNAMIC ACIDS; LACTIC ACID BACTERIA; LACTOBACILLUS BREVIS; LACTOBACILLUS CURVATUS; LACTOBACILLUS FERMENTUM; LEUCONOSTOC MESENTEROIDES;

LACTIC ACID;

ACETIC ACID; ANOXIC CONDITIONS; BIOCHEMISTRY; CONCENTRATION (COMPOSITION); ENZYME ACTIVITY; FERMENTATION; METABOLISM; MICROBIAL ACTIVITY;

LACTOBACILLUS BREVIS; LACTOBACILLUS CURVATUS; LACTOBACILLUS FERMENTUM; LACTOBACILLUS ROSSIAE; LEUCONOSTOC MESENTEROIDES; WEISSELLA;

ACETATE KINASE; ADENOSINE TRIPHOSPHATE; ALCOHOL DEHYDROGENASE; BACTERIAL PROTEIN; COUMARIC ACID; CULTURE MEDIUM; LACTIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE;

CULTURE MEDIUM; ELECTRON TRANSPORT; ENERGY METABOLISM; ENZYMOLOGY; FERMENTATION; LACTOBACILLUS; METABOLISM; WEISSELLA;

ACETATE KINASE; ADENOSINE TRIPHOSPHATE; ALCOHOL DEHYDROGENASE; BACTERIAL PROTEINS; COUMARIC ACIDS; CULTURE MEDIA; ELECTRON TRANSPORT; ENERGY METABOLISM; FERMENTATION; LACTIC ACID; LACTOBACILLUS; NAD; WEISSELLA;

EID: 84917727201     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02413-14     Document Type: Article

References (40)

1. Rodrìguez H, Landete JM, Rivas BDL, Muñoz R. 2008. Metabolism of food phenolic acids by Lactobacillus plantarum CECT 748T. Food Chem. 107:1393-1398. http://dx.doi.org/10.1016/j.foodchem.2007.09.067.
2. Naczk M, Shahidi F. 2006. Phenolics in cereals, fruits and vegetables: occurrence, extraction and analysis. J. Pharm. Biomed. Anal. 41:1523-1542. http://dx.doi.org/10.1016/j.jpba.2006.04.002.
3. Rodrìguez H, Curiel JA, Landete JM, de Las Rivas B, de Felipe FL, Gòmez-Cordovés C. 2009. Food phenolics and lactic acid bacteria. Int. J. Food Microbiol. 132:79-90. http://dx.doi.org/10.1016/j.ijfoodmicro.2009.03.025.
4. Barthelmebs L, Divies C, Cavin JF. 2000. Knockout of the p-coumarate decarboxylase gene from Lactobacillus plantarum reveals the existence of two other inducible enzymatic activities involved in phenolic acid metabolism. Appl. Environ. Microbiol. 66:3368-3375. http://dx.doi.org/10.1128/AEM.66.8.3368-3375.2000.
5. Jung JY, Lee SH, Lee HJ, Seo HY, Park WS, Jeon CO. 2012. Effects of Leuconostoc mesenteroides starter cultures on microbial communities and metabolites during kimchi fermentation. Int. J. Food Microbiol. 153:378-387. http://dx.doi.org/10.1016/j.ijfoodmicro.2011.11.030.
6. Kostinek M, Specht I, Edward VA, Pinto C, Egounlety M, Sossa C, Mbugua S, Dortu C, Thonart P, Taljaard L, Mengu M, Franz CMAP, Holzapfel WH. 2007. Characterisation and biochemical properties of predominant lactic acid bacteria from fermenting cassava for selection as starter cultures. Int. J. Food Microbiol. 114:342-351. http://dx.doi.org/10.1016/j.ijfoodmicro.2006.09.029.
7. Di Cagno R, Surico RF, Siragusa S, De Angelis M, Paradiso A, Minervini F, De Gara L, Gobbetti M. 2008. Selection and use of autochthonous mixed starter for lactic acid fermentation of carrots, French beans or marrows. Int. J. Food Microbiol. 127:220-228. http://dx.doi.org/10.1016/j.ijfoodmicro.2008.07.010.
8. Di Cagno R, Surico RF, Paradiso A, De Angelis M, Salmon JC, Buchin S, De Gara L, Gobbetti M. 2009. Effect of autochthonous lactic acid bacteria starters on health-promoting and sensory properties of tomato juices. Int. J. Food Microbiol. 128:473-483. http://dx.doi.org/10.1016/j.ijfoodmicro.2008.10.017.
9. Silva I, Campos FM, Hogg T, Couto JA. 2011. Factors influencing the production of volatile phenols by wine lactic acid bacteria. Int. J. Food Microbiol. 145:471-475. http://dx.doi.org/10.1016/j.ijfoodmicro.2011.01.029.
10. Selma MV, Espin JC, Tomas-Barberan FA. 2009. Interaction between phenolics and gut microbiota: role in human health. J. Agric. Food Chem. 57:6485-6501. http://dx.doi.org/10.1021/jf902107d.
11. Sanchez-Maldonado AF, Schieber A, Gänzle MG. 2011. Structure-function relationships of the antibacterial activity of phenolic acids and their metabolism by lactic acid bacteria. J. Appl. Microbiol. 111:1176-1184. http://dx.doi.org/10.1111/j.1365-2672.2011.05141.x.
12. Filannino P, Bai Y, Di Cagno R, Gobbetti M, Gänzle MG. 2014. Metabolism of phenolic compounds by Lactobacillus spp. during fermentation of cherry juice and broccoli puree. Food Microbiol. 46:272-279. http://dx.doi.org/10.1016/j.fm.2014.08.018.
13. Minervini F, De Angelis M, Di Cagno R, Gobbetti M. 2014. Ecological parameters influencing microbial diversity and stability of traditional sourdough. Int. J. Food Microbiol. 171:136-146. http://dx.doi.org/10.1016/j.ijfoodmicro.2013.11.021.
14. Vermeulen N, Czerny M, Gänzle MG, Schieberle P, Vogel RF. 2007. Reduction of (E)-2-nonenal and (E, E)-2,4-decadienal during sourdough fermentation. J. Cereal Sci. 45:78-87. http://dx.doi.org/10.1016/j.jcs.2006.07.002.
15. Di Cagno R, Minervini G, Rizzello CG, De Angelis M, Gobbetti M. 2011. Effect of lactic acid fermentation on antioxidant, texture, color and sensory properties of red and green smoothies. Food Microbiol. 28:1062-1071. http://dx.doi.org/10.1016/j.fm.2011.02.011.
16. Di Cagno R, Cardinali G, Minervini G, Antonielli L, Rizzello CG, Ricciuti P, Gobbetti M. 2010. Taxonomic structure of the yeasts and lactic acid bacteria microbiota of pineapple (Ananas comosus L. Merr.) and use of autochthonous starters for minimally processing. Food Microbiol. 27:381-389. http://dx.doi.org/10.1016/j.fm.2009.11.012.
17. Di Cagno R, Surico RF, Minervini G, De Angelis M, Rizzello CG, Gobbetti M. 2009. Use of autochthonous starters to ferment red and yellow peppers (Capsicum annum L.) to be stored at room temperature. Int. J. Food Microbiol. 130:108-116. http://dx.doi.org/10.1016/j.ijfoodmicro.2009.01.019.
18. Di Cagno R, Coda R, De Angelis M, Gobbetti M. 2013. Exploitation of vegetables and fruits through lactic acid fermentation. Food Microbiol. 33:1-10. http://dx.doi.org/10.1016/j.fm.2012.09.003.
19. Rizzello CG, Losito I, Gobbetti M, Carbonara T, De Bari MD, Zambonin PG. 2005. Antibacterial activities of peptides from the watersoluble extracts of Italian cheese varieties. J. Dairy Sci. 88:2348-2360. http://dx.doi.org/10.3168/jds. S0022-0302(05)72913-1.
20. McFeeters RF, Chen KH. 1986. Utilization of electron acceptors for anaerobic mannitol metabolism by Lactobacillus plantarum. Compounds which serve as electron acceptors. Food Microbiol. 3:73-81.
21. Zwietering MH, Jongeberger I, Roumbouts FM, Van't Riet K. 1990. Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56:1875-1881.
22. Zeppa G, Conterno L, Gerbi V. 2001. Determination of organic acids, sugars, diacetyl, and acetoin in cheese by high-performance liquid chromatography. J. Agric. Food. Chem. 49:2722-2726. http://dx.doi.org/10.1021/jf0009403.
23. Bradford MM. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
24. Amárita F, Fernández-Esplá D, Requena T, Pelaez C. 2001. Conversion of methionine to methional by Lactococcus lactis. FEMS Microbiol. Lett. 204:189-195. http://dx.doi.org/10.1111/j.1574-6968.2001.tb10884.x.
25. Fowler ML, Ingram-Smith CJ, Smith KS. 2011. Direct detection of the acetate-forming activity of the enzyme acetate kinase. J. Vis. Exp. 2011: 3474. http://dx.doi.org/10.3791/3474.
26. Manach C, Scalbert A, Morand C, Rémés C, Jiménez L. 2004. Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79:727-747.
27. Clifford MN. 1999. Chlorogenic acids and other cinnamates-nature, occurrence and dietary burden. J. Sci. Food Agric. 79:362-372. http://dx.doi.org/10.1002/(SICI)1097-0010(20000515)80:71033::AID-JSFA5953.0.CO;2-T.
28. Macheix JJ, Fleuriet A, Billot J. 1990. Fruit phenolics. CRC Press, Boca Raton, FL.
29. Corsetti A, Settanni L, van Sinderen D, Felis GE, Dellaglio F, Gobbetti M. 2005. Lactobacillus rossii sp. nov. isolated from wheat sourdough. Int. J. Syst. Evol. Microbiol. 55:35-40. http://dx.doi.org/10.1099/ijs.0.63075-0.
30. Siragusa S, Di Cagno R, Ercolini D, Minervini F, Gobbetti M, De Angelis M. 2009. Taxonomic structure and monitoring of the dominant population of lactic acid bacteria during wheat flour sourdough type I propagation using Lactobacillus sanfranciscensis starters. Appl. Environ. Microbiol. 75:1099-1109. http://dx.doi.org/10.1128/AEM.01524-08.
31. Scheirlinck I, Van der Meulen R, De Vuyst L, Vandamme P, Huys G. 2009. Molecular source tracking of predominant lactic acid bacteria in traditional Belgian sourdoughs and their production environments. J. Appl. Microbiol. 106:1081-1092. http://dx.doi.org/10.1111/j.1365-2672.2008.04094.x.
32. Minervini F, De Angelis M, Di Cagno R, Pinto D, Siragusa S, Rizzello CG, Gobbetti M. 2010. Robustness of Lactobacillus plantarum starters during daily propagation of wheat flour sourdough type I. Food Microbiol. 27:897-908. http://dx.doi.org/10.1016/j.fm.2010.05.021.
33. Di Cagno R, Rizzello CG, Gagliardi F, Ricciuti P, Ndagijimana M, Francavilla R, Guerzoni ME, Crecchio C, Gobbetti M, De Angelis M. 2009. Different fecal microbiotas and volatile organic compounds in treated and untreated children with celiac disease. Appl. Environ. Microbiol. 75:3963-3971. http://dx.doi.org/10.1128/AEM.02793-08.
34. De Angelis M, Siragusa S, Berloco M, Caputo L, Settanni L, Alfonsi G, Amerio M, Grandi A, Ragni A, Gobbetti M. 2006. Selection of potential probiotic lactobacilli from pig feces to be used as additives in pelleted feeding. Res. Microbiol. 157:792-801. http://dx.doi.org/10.1016/j.resmic.2006.05.003.
35. Silva FAM, Borges F, Guimarães C, Lima JLFC, Matos C, Reis S. 2000. Phenolic acids and derivatives: studies on the relationship among structure, radical scavenging activity, and physicochemical parameters. J. Agric. Food Chem. 48:2122-2126. http://dx.doi.org/10.1021/jf9913110.
36. Huang J, de Paulis T, May JM. 2004. Antioxidant effects of dihydrocaffeic acid in human EA.hy926 endothelial cells. J. Nutr. Biochem. 15:722-729. http://dx.doi.org/10.1016/j.jnutbio.2004.07.002.
37. Cavin JF, Barthelmebs L, Diviès C. 1997. Molecular characterization of an inducible p-coumaric acid decarboxylase from Lactobacillus plantarum: gene cloning, transcriptional analysis, overexpression in Escherichia coli, purification, and characterization. Appl. Environ. Microbiol. 63:1939-1944.
38. Iwamoto K, Tsuruta H, Nishitani Y, Osawa R. 2008. Identification and cloning of a gene encoding tannase (tannin acylhydrolase) from Lactobacillus plantarum ATCC 14917T. Syst. Appl. Microbiol. 31:269-277. http://dx.doi.org/10.1016/j.syapm.2008.05.004.
39. Landete JM, Rodríguez H, De Las Rivas B, Muñoz R. 2008. Characterization of a benzyl alcohol dehydrogenase from Lactobacillus plantarum WCFS1. J. Agric. Food Chem. 56:4497-4503. http://dx.doi.org/10.1021/jf800500v.
40. Filannino P, Cardinali G, Rizzello CG, Buchin B, De Angelis M, Gobbetti M, Di Cagno R. 2014. Metabolic responses of Lactobacillus plantarum strains during fermentation and storage of vegetable and fruit juices. Appl. Environ. Microbiol. 80:2206-2215. http://dx.doi.org/10.1128/AEM.03885-13.