Biochemical analysis of respiratory metabolism in the heterofermentative Lactobacillus spicheri and Lactobacillus reuteri

Journal of Applied Microbiology

Volumn 119, Issue 3, 2015, Pages 763-775

  Ianniello, R G ^a,b   Zheng, J ^c   Zotta, T ^d   Ricciardi, A ^b   Ganzle M G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF BASILICATA   (Italy)

^c HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^d CNR   (Italy)

Author keywords

Genome analysis; Lactobacillus reuteri; Lactobacillus spicheri; Metabolism; Respiration

Indexed keywords

GENE EXPRESSION; OXYGEN; PHYSIOLOGY;

AEROBIC CULTURES; BIOCHEMICAL ANALYSIS; GENES EXPRESSION; GENOME ANALYSIS; IN-SILICO; LACTOBACILLUS REUTERI; LACTOBACILLUS SPICHERI; PYRUVATE OXIDASE; RESPIRATION; SOURDOUGH FERMENTATION;

METABOLISM;

ACETIC ACID; ACETOIN; CYTOCHROME; CYTOCHROME C OXIDASE; LACTIC ACID; PEROXIDASE; PYRUVATE DEHYDROGENASE; PYRUVATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; BACTERIAL PROTEIN; NAD+ PEROXIDASE; OXYGEN;

ACETATE; BACTERIUM; BIOCHEMICAL COMPOSITION; BIOMASS; ENZYME ACTIVITY; FERMENTATION; GENE EXPRESSION; GENOME; METABOLISM; METABOLITE; OXYGEN; PHENOTYPE; RESPIRATION;

AEROBIC METABOLISM; ARTICLE; BACTERIAL METABOLISM; BIOCHEMICAL ANALYSIS; BIOMASS PRODUCTION; BREATHING; CONTROLLED STUDY; FERMENTATION; GENE EXPRESSION; GENOME ANALYSIS; LACTOBACILLUS; LACTOBACILLUS CASEI; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; LACTOBACILLUS SPICHERI; METABOLITE; NONHUMAN; OXYGEN CONSUMPTION; RESPIRATORY METABOLISM; ENZYMOLOGY; GENETICS; METABOLISM;

LACTOBACILLUS CASEI; LACTOBACILLUS REUTERI; LACTOBACILLUS SPICHERI;

AEROBIOSIS; BACTERIAL PROTEINS; FERMENTATION; LACTOBACILLUS; LACTOBACILLUS REUTERI; OXYGEN; PEROXIDASES; PYRUVATE OXIDASE;

EID: 84939574585     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12853     Document Type: Article

References (52)

1. Axelsson, L. (2003) Lactic acid bacteria: classification and physiology. In Lactic Acid Bacteria: Microbiological and Functional Aspects, 3rd edn ed. Salminen, S. and von Wright, A. pp. 1-66. New York, NY: Marcel Dekker.
2. Baranyi, J. and Roberts, T.A. (1994) A dynamic approach to predicting bacterial growth in food. Int J Food Microbiol 23, 277-294.
3. Baranyi, J. and Le Marc, Y. (1996) Dmfit Manual Version 2.0. Institute of Food Research, Norwich, UK.
4. Böcker, G., Stolz, P. and Hammes, W.P. (1995) Neue Erkenntnisse zum Okosystem Sauerteig und zur Physiologie der sauerteigtypischen Stamme Lactobacillus sanfrancisco und Lactobacillus pontis. Getreide Mehl Brot 49, 370-374.
5. Brooijmans, R.J., Poolman, B., Schuurman-Wolters, G.K., de Vos, W.M. and Hugenholtz, J. (2007) Generation of a membrane potential by Lactococcus lactis through aerobic electron transport. J Bacteriol 189, 5203-5209.
6. Brooijmans, R., Smit, B., Santos, F., van Riel, J., de Vos, W.M. and Hugenholtz, J. (2009) Heme and menaquinone induced electron transport in lactic acid bacteria. Microbiol Cell Fact 8, 28.
7. Carvalho, A.S., Silva, J., Hob, P., Teixeira, P., Malcata, F.X. and Gibbs, P. (2004) Relevant factors for the preparation of freeze-dried lactic acid bacteria. Int Dairy J 14, 835-847.
8. Duwat, P., Sourice, S., Cesselin, B., Lamberet, G., Vido, K., Gaudu, P., Le Loir, Y., Violet, F. et al. (2001) Respiration capacity of the fermenting bacterium Lactococcus lactis and its positive effects on growth and survival. J Bacteriol 183, 4509-4516.
9. Frese, S.A., Benson, A.K., Tannock, G.W., Loach, D.M., Kim, J., Zhang, M., Oh, P.L., Heng, N.C. et al. (2011) The evolution of host specialization in the vertebrate gut symbiont Lactobacillus reuteri. PLoS Genet 7, e1001314.
10. Gänzle, M.G., Vermeulen, N. and Vogel, R.F. (2007) Carbohydrate, peptide and lipid metabolism of lactic acid bacteria in sourdough. Food Microbiol 24, 128-138.
11. Gaudu, P., Vido, K., Cesselin, B., Kulakauskas, S., Tremblay, J., Rezaiki, L., Lamberet, G., Sourice, S. et al. (2002) Respiration capacity and consequences in Lactococcus lactis. Antonie Van Leeuwenhoek 82, 263-269.
12. Gaudu, P., Lamberet, G., Poncet, S. and Gruss, A. (2003) CcpA regulation of aerobic and respiration growth in Lactococcus lactis. Mol Microbiol 50, 183-192.
13. Goffin, P., Muscariello, L., Lorquet, F., Stukkens, A., Prozzi, D., Saccom, M. and Hols, P. (2006) Involvement of pyruvate oxidase activity and acetate production in the survival of Lactobacillus plantarum during the stationary phase of aerobic growth. Appl Environ Microbiol 72, 7933-7940.
14. Guidone, A., Ianniello, R.G., Ricciardi, A., Zotta, T. and Parente, E. (2013) Aerobic metabolism and oxidative stress tolerance in the Lactobacillus plantarum group. World J Microbiol Biotechnol 29, 1713-1722.
15. 2 and acetate dependency of Lactobacillus johnsonii NCC 533. PLoS ONE 8, e57235.
16. Holzapfel, W.H. and Wood, B.J.B. (2014) Introduction to the LAB. In Lactic Acid Bacteria: Biodiversity and Taxonomy ed. Holfapfel, W.H. and Wood, B.J.B. pp. 1-12. New York, NY: John Wiley & Sons.
17. Iacumin, L., Ginaldi, F., Manzano, M., Anastasi, V., Reale, A., Zotta, T., Rossi, F., Coppola, R. et al. (2015) High resolution melting analysis (HRM) as a new tool for the identification of species belonging to the Lactobacillus casei group and comparison with species-specific PCRs and multiplex PCR. Food Microbiol 46, 357-367.
18. Ianniello, R.G., Ricciardi, A., Parente, E., Tramutola, A., Reale, A. and Zotta, T. (2015) Aeration and supplementation with haeme and menaquinone affect survival to stresses and antioxidant capability of Lactobacillus casei strains. LWT - Food Sci Technol 60, 817-824.
19. Jääskeläinen, E., Johansson, P., Kostiainen, O., Nieminen, T., Schmidt, G., Somervuo, P., Mohsina, M., Vanninen, P. et al. (2013) Significance of heme-based respiration in meat spoilage caused by Leuconostoc gasicomitatum. Appl Environ Microbiol 79, 1078-1085.
20. T. Food Microbiol 28, 29-37.
21. Jensen, N.B.S., Melchiorsen, C.R., Jokumsen, K.V. and Villadsen, A.J. (2001) Metabolic behaviour of Lactococcus lactis MG1363 in microaerobic continuous cultivation at a low dilution rate. Appl Environ Microbiol 67, 2677-2682.
22. Kandler, O. (1983) Carbohydrate metabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 49, 209-224.
23. Kang, T.S., Korber, D.R. and Tanaka, T. (2013) Influence of oxygen on NADH recycling and oxidative stress resistance systems in Lactobacillus panis PM1. AMB Express 3, 10.
24. Kelley, D.R., Schatz, M.C. and Salzberg, S.L. (2010) Quake: quality-aware detection and correction of sequencing errors. Genome Biol 11, R116.
25. Knauf, H.J., Vogel, R.F. and Hammes, W.P. (1992) Cloning, sequence, and phenotypic expression of katA, which encodes the catalase of Lactobacillus sakei LTH677. Appl Environ Microbiol 58, 832-839.
26. Korithoski, B., Levesque, C.M. and Cvitkovitch, D.G. (2008) The involvement of the pyruvate dehydrogenase E1 α subunit, in Streptococcus mutans acid tolerance. FEMS Microbiol Lett 289, 13-19.
27. Lorquet, F., Goffin, P., Muscariello, L., Baudry, J.B., Ladero, V., Sacco, M., Kleerebezem, M. and Hols, P. (2004) Characterization and functional analysis of the poxB gene, which encodes pyruvate oxidase in Lactobacillus plantarum. J Bacteriol 186, 3749-3759.
28. McLeod, A., Zagorec, M., Champomier-Verges, M.C., Naterstad, K. and Axelsson, L. (2010) Primary metabolism in Lactobacillus sakei food isolates by proteomic analysis. BMC Microbiol 10, 120.
29. Meroth, C.B., Hammes, W.P. and Hertel, C. (2004) Characterisation of the microbiota of rice sourdoughs and description of Lactobacillus spicheri sp. nov. Syst Appl Microbiol 27, 151-159.
30. Monedero, V., Poncet, S., Mijakovic, I., Fieulaine, S., Dossonnet, V., Martin-Verstraete, I., Nessler, S. and Deutscher, J. (2001) Mutations lowering the phosphatase activity of HPr kinase/phosphatase switch off carbon metabolism. EMBO J 20, 3928-3937.
31. Olguín, N., Bordons, A. and Reguant, C. (2009) Influence of ethanol and pH on the gene expression of the citrate pathway in Oenococcus oeni. Food Microbiol 26, 197-203.
32. Paramithiotis, S., Sofou, A., Tsakalidou, E. and Kalantzopoulos, G. (2007) Flour carbohydrate catabolism and metabolite production by sourdough lactic acid bacteria. World J Microbiol Biotechnol 23, 1417-1423.
33. Pedersen, M.B., Garrigues, C., Tuphile, K., Brun, C., Vido, K., Bennedsen, M., Møllgaard, H., Gaudu, P. et al. (2008) Impact of aeration and heme-activated respiration on Lactococcus lactis gene expression: identification of a heme-responsive operon. J Bacteriol 190, 4903-4911.
34. Pedersen, M.B., Gaudu, P., Lechardeur, D., Petit, M.A. and Gruss, A. (2012) Aerobic respiration metabolism in lactic acid bacteria and uses in biotechnology. Ann Rev Food SciTechnol 3, 37-58.
35. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45.
36. Quatravaux, S., Remize, F., Bryckaert, E., Colavizza, D. and Guzzo, J. (2006) Examination of Lactobacillus plantarum lactate metabolism side effects in relation to the modulation of aeration parameters. J Appl Microbiol 101, 903-912.
37. Rezaiki, L., Cesselin, B., Yamamoto, Y., Vido, K., van West, E., Gaudu, P. and Gruss, A. (2004) Respiration metabolism reduces oxidative and acid stress to improve long-term survival of Lactococcus lactis. Mol Microbiol 53, 1331-1342.
38. Ricciardi, A., Ianniello, R.G., Tramutola, A., Parente, E. and Zotta, T. (2014) Rapid detection assay for oxygen consumption in the Lactobacillus casei group. Ann Microbiol 64, 1861-1864.
39. Savino, F., Pelle, E., Palumeri, E., Oggero, R. and Miniero, R. (2007) Lactobacillus reuteri (American Type Culture Collection Strain 55730) versus simethicone in the treatment of infantile colic: a prospective randomized study. Pediatrics 119, e124-e130.
40. Schwab, C. and Gänzle, M.G. (2006) Effect of membrane lateral pressure on the expression of fructosyl transferases in Lactobacillus reuteri. Syst Appl Microbiol 29, 89-99.
41. Sekwati-Monang, B. and Gänzle, M.G. (2011) Microbiological and chemical characterization of ting, a sorghum-based sourdough product from Botswana. Int J Food Microbiol 150, 115-121.
42. Simpson, J.T., Wong, K., Jackman, S.D., Schein, J.E., Jones, S.J. and Birol, I. (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19, 1117-1123.
43. Stolz, P., Vogel, R.F. and Hammes, W.P. (1995a) Utilization of electron acceptors by lactobacilli isolated from sourdough. II. Lactobacillus pontis, L. reuteri, L. amylovorus, and L. fermentum. Z Lebensm Unters Forsch 201, 402-410.
44. Stolz, P., Böcker, G., Hammes, W.P. and Vogel, R.F. (1995b) Utilization of electron acceptors by lactobacilli isolated from sourdough. I. Lactobacillus sanfrancisco. Z Lebensm Unters Forsch 201, 91-96.
45. Su, M.S., Oh, P.L., Walter, J. and Gänzle, M.G. (2012) Intestinal origin of sourdough Lactobacillus reuteri isolates as revealed by phylogenetic, genetic, and physiological analysis. Appl Environ Microbiol 78, 6777-6780.
46. Tsau, J.L., Guffanti, A.A. and Montville, T.J. (1992) Conversion of pyruvate to acetoin helps to maintain pH homeostasis in Lactobacillus plantarum. Appl Environ Microbiol 58, 891-894.
47. Turner, M.S., Woodberry, T., Hafner, L.M. and Giffard, P.M. (1999) ThebspA locus of Lactobacillus fermentum BR11 encodes an L-cystine uptake system. J Bacteriol 181, 2192-2198.
48. Valcheva, R., Korakli, M., Onno, B., Prèvost, H., Ivanova, I., Ehrmann, M.A., Dousset, X., Gänzle, M.G. et al. (2005) Lactobacillus hammesii sp. nov. isolated from French sourdough. Syst Appl Microbiol 27, 151-159.
49. Watanabe, M., van der Veen, S., Nakajima, H. and Abee, T. (2012) Effect of respiration and manganese on oxidative stress resistance of Lactobacillus plantarum WCFS1. Microbiology 158, 293-300.
50. Zotta, T., Guidone, A., Ianniello, R.G., Parente, E. and Ricciardi, A. (2013) Temperature and respiration affect the growth and stress resistance of Lactobacillus plantarum C17. J Appl Microbiol 115, 848-858.
51. Zotta, T., Ianniello, R.G., Guidone, A., Parente, E. and Ricciardi, A. (2014a) Selection of mutants tolerant of oxidative stress from respiratory cultures of Lactobacillus plantarum C17. J Appl Microbiol 116, 632-643.
52. Zotta, T., Ricciardi, A., Ianniello, R.G., Parente, E., Reale, A., Rossi, F., Iacumin, L., Comi, G. et al. (2014b) Assessment of aerobic and respiratory growth in the Lactobacillus casei group. PLoS ONE 9, e99189.