The Pentose Moiety of Adenosine and Inosine is an Important Energy Source for the Fermented-meat Starter Culture Lactobacillus Sakei CTC 494

Overview

Journal Appl Environ Microbiol

Specialties Environmental Health
Microbiology

Date 2011 Aug 2

PMID 21803903

Citations 18

Authors

T Rimaux

G Vrancken

B Vuylsteke

L De Vuyst

F Leroy

Affiliations

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Abstract

The genome sequence of Lactobacillus sakei 23K has revealed that the species L. sakei harbors several genes involved in the catabolism of energy sources other than glucose in meat, such as glycerol, arginine, and nucleosides. In this study, a screening of 15 L. sakei strains revealed that arginine, inosine, and adenosine could be used as energy sources by all strains. However, no glycerol catabolism occurred in any of the L. sakei strains tested. A detailed kinetic analysis of inosine and adenosine catabolism in the presence of arginine by L. sakei CTC 494, a fermented-meat starter culture, was performed. It showed that nucleoside catabolism occurred as a mixed-acid fermentation in a pH range (pH 5.0 to 6.5) relevant for sausage fermentation. This resulted in the production of a mixture of acetic acid, formic acid, and ethanol from ribose, while the nucleobase (hypoxanthine and adenine in the case of fermentations with inosine and adenosine, respectively) was excreted into the medium stoichiometrically. This indicates that adenosine deaminase activity did not take place. The ratios of the different fermentation end products did not vary with environmental pH, except for the fermentation with inosine at pH 5.0, where lactic acid was produced too. In all cases, no other carbon-containing metabolites were found; carbon dioxide was derived only from arginine catabolism. Arginine was cometabolized in all cases and resulted in the production of both citrulline and ornithine. Based on these results, a pathway for inosine and adenosine catabolism in L. sakei CTC 494 was presented, whereby both nucleosides are directly converted into their nucleobase and ribose, the latter entering the heterolactate pathway. The present study revealed that the pentose moiety (ribose) of the nucleosides inosine and adenosine is an effective fermentable substrate for L. sakei. Thus, the ability to use these energy sources offers a competitive advantage for this species in a meat environment.

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References

Van der Meulen R, Makras L, Verbrugghe K, Adriany T, De Vuyst L . In vitro kinetic analysis of oligofructose consumption by Bacteroides and Bifidobacterium spp. indicates different degradation mechanisms. Appl Environ Microbiol. 2006; 72(2):1006-12. PMC: 1392924. DOI: 10.1128/AEM.72.2.1006-1012.2006. View

Ravyts F, De Vuyst L . Prevalence and impact of single-strain starter cultures of lactic acid bacteria on metabolite formation in sourdough. Food Microbiol. 2011; 28(6):1129-39. DOI: 10.1016/j.fm.2011.03.004. View

Takahashi S, Abbe K, Yamada T . Purification of pyruvate formate-lyase from Streptococcus mutans and its regulatory properties. J Bacteriol. 1982; 149(3):1034-40. PMC: 216493. DOI: 10.1128/jb.149.3.1034-1040.1982. View

Smid E, Hugenholtz J . Functional genomics for food fermentation processes. Annu Rev Food Sci Technol. 2011; 1:497-519. DOI: 10.1146/annurev.food.102308.124143. View

Falony G, Verschaeren A, De Bruycker F, De Preter V, Verbeke K, Leroy F . In vitro kinetics of prebiotic inulin-type fructan fermentation by butyrate-producing colon bacteria: implementation of online gas chromatography for quantitative analysis of carbon dioxide and hydrogen gas production. Appl Environ Microbiol. 2009; 75(18):5884-92. PMC: 2747863. DOI: 10.1128/AEM.00876-09. View

Surette M, Gill T, Maclean S . Purification and characterization of purine nucleoside phosphorylase from Proteus vulgaris. Appl Environ Microbiol. 1990; 56(5):1435-9. PMC: 184424. DOI: 10.1128/aem.56.5.1435-1439.1990. View

Chaillou S, Champomier-Verges M, Cornet M, Crutz-Le Coq A, Dudez A, Martin V . The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K. Nat Biotechnol. 2005; 23(12):1527-33. DOI: 10.1038/nbt1160. View

Vrancken G, Rimaux T, Weckx S, De Vuyst L, Leroy F . Environmental pH determines citrulline and ornithine release through the arginine deiminase pathway in Lactobacillus fermentum IMDO 130101. Int J Food Microbiol. 2009; 135(3):216-22. DOI: 10.1016/j.ijfoodmicro.2009.07.035. View

Lauret R, Morel-Deville F, Berthier F, Champomier-Verges M, Postma P, Ehrlich S . Carbohydrate Utilization in Lactobacillus sake. Appl Environ Microbiol. 1996; 62(6):1922-7. PMC: 1388869. DOI: 10.1128/aem.62.6.1922-1927.1996. View

10.

Champomier-Verges M, Chaillou S, Cornet M, Zagorec M . Lactobacillus sakei: recent developments and future prospects. Res Microbiol. 2002; 152(10):839-48. DOI: 10.1016/s0923-2508(01)01267-0. View

11.

Champomier Verges M, Zuniga M, Morel-Deville F, Perez-Martinez G, Zagorec M, Ehrlich S . Relationships between arginine degradation, pH and survival in Lactobacillus sakei. FEMS Microbiol Lett. 1999; 180(2):297-304. DOI: 10.1111/j.1574-6968.1999.tb08809.x. View

12.

Ravyts F, Barbuti S, Frustoli M, Parolari G, Saccani G, De Vuyst L . Competitiveness and antibacterial potential of bacteriocin-producing starter cultures in different types of fermented sausages. J Food Prot. 2008; 71(9):1817-27. DOI: 10.4315/0362-028x-71.9.1817. View

13.

Lefeber T, Janssens M, Camu N, De Vuyst L . Kinetic analysis of strains of lactic acid bacteria and acetic acid bacteria in cocoa pulp simulation media toward development of a starter culture for cocoa bean fermentation. Appl Environ Microbiol. 2010; 76(23):7708-16. PMC: 2988588. DOI: 10.1128/AEM.01206-10. View

14.

Samelis J, Metaxopoulos J, Vlassi M, Pappa A . Stability and safety of traditional Greek salami -- a microbiological ecology study. Int J Food Microbiol. 1998; 44(1-2):69-82. DOI: 10.1016/s0168-1605(98)00124-x. View

15.

Kilstrup M, Hammer K, Jensen P, Martinussen J . Nucleotide metabolism and its control in lactic acid bacteria. FEMS Microbiol Rev. 2005; 29(3):555-90. DOI: 10.1016/j.femsre.2005.04.006. View

16.

Schuch R, Garibian A, Saxild H, Piggot P, Nygaard P . Nucleosides as a carbon source in Bacillus subtilis: characterization of the drm-pupG operon. Microbiology (Reading). 1999; 145 ( Pt 10):2957-66. DOI: 10.1099/00221287-145-10-2957. View

17.

Vrancken G, Rimaux T, De Vuyst L, Leroy F . Kinetic analysis of growth and sugar consumption by Lactobacillus fermentum IMDO 130101 reveals adaptation to the acidic sourdough ecosystem. Int J Food Microbiol. 2008; 128(1):58-66. DOI: 10.1016/j.ijfoodmicro.2008.08.001. View

18.

Leroy F, Verluyten J, De Vuyst L . Functional meat starter cultures for improved sausage fermentation. Int J Food Microbiol. 2005; 106(3):270-85. DOI: 10.1016/j.ijfoodmicro.2005.06.027. View

19.

Cocolin L, Dolci P, Rantsiou K, Urso R, Cantoni C, Comi G . Lactic acid bacteria ecology of three traditional fermented sausages produced in the North of Italy as determined by molecular methods. Meat Sci. 2010; 82(1):125-32. DOI: 10.1016/j.meatsci.2009.01.004. View

20.

Chaillou S, Daty M, Baraige F, Dudez A, Anglade P, Jones R . Intraspecies genomic diversity and natural population structure of the meat-borne lactic acid bacterium Lactobacillus sakei. Appl Environ Microbiol. 2008; 75(4):970-80. PMC: 2643555. DOI: 10.1128/AEM.01721-08. View