Channel-mediated lactic acid transport: A novel function for aquaglyceroporins in bacteria

Biochemical Journal

Volumn 454, Issue 3, 2013, Pages 559-570

  Bienert, Gerd P ^a,b   Desguin, Benoît ^a   Chaumont, François ^a   Hols, Pascal ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

Aquaporin; Bacterial aquaglyceroporin; GlpF; Lactic acid transport; Lactobacillus plantarum

Indexed keywords

AQUAGLYCEROPORIN; BACTERIAL PROTEIN; COMPLEMENTARY RNA; DIHYDROXYACETONE; GENOMIC DNA; GLYCEROL; HYBRID PROTEIN; LACTIC ACID; MEMBRANE PROTEIN; WATER; YELLOW FLUORESCENT PROTEIN;

ARTICLE; CONTROLLED STUDY; DELETION MUTANT; GENE DELETION; GRAM POSITIVE BACTERIUM; LACTIC ACID BACTERIUM; LACTOBACILLUS PLANTARUM; MEMBRANE PERMEABILITY; NONHUMAN; OOCYTE; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RACEMIZATION; XENOPUS LAEVIS;

ANIMALS; AQUAGLYCEROPORINS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL MEMBRANE PERMEABILITY; CLONING, MOLECULAR; DIHYDROXYACETONE; GLYCEROL; HYDROGEN PEROXIDE; LACTIC ACID; LACTOBACILLUS PLANTARUM; OOCYTES; PEDIOCOCCUS; PHYLOGENY; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; UREA; WATER; XENOPUS LAEVIS;

EID: 84883422622     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130388     Document Type: Article

References (54)

1. Engel, A. and Stahlberg, H. (2002) Aquaglyceroporins: channel proteins with a conserved core, multiple functions, and variable surfaces. Int. Rev. Cytol. 215, 75-104
2. Ishibashi, K. (2009) New members of mammalian aquaporins: AQP10-AQP12. Handb. Exp. Pharmacol. 190, 251-262
3. Zardoya, R. (2005) Phylogeny and evolution of the major intrinsic protein family. Biol. Cell 97, 397-414
4. Maurel, C., Reizer, J., Schroeder, J. I., Chrispeels, M. J. and Saier, Jr., M. H. (1994) Functional characterization of the Escherichia coli glycerol facilitator, GlpF, in Xenopus oocytes. J. Biol. Chem. 269, 11869-11872
5. Calamita, G., Bishai, W. R., Preston, G. M., Guggino, W. B. and Agre, P. (1995) Molecular cloning and characterization of AqpZ, a water channel from Escherichia coli. J. Biol. Chem. 270, 29063-29066
6. Froger, A., Rolland, J. P., Bron, P., Lagree, V., Le Caherec, F., Deschamps, S., Hubert, J. F., Pellerin, I., Thomas, D. and Delamarche, C. (2001) Functional characterization of a microbial aquaglyceroporin. Microbiology 147, 1129-1135
7. Rodriguez, M. C., Froger, A., Rolland, J. P., Thomas, D., Aguero, J., Delamarche, C. and Garcia-Lobo, J. M. (2000) A functional water channel protein in the pathogenic bacterium Brucella abortus. Microbiology 146, 3251-3257
8. Tanghe, A., Van Dijck, P. and Thevelein, J. M. (2006) Why do microorganisms have aquaporins? Trends Microbiol. 14, 78-85
9. Lorca, G. L., Barabote, R. D., Zlotopolski, V., Tran, C., Winnen, B., Hvorup, R. N., Stonestrom, A. J., Nguyen, E., Huang, L. W., Kim, D. S. and Saier, Jr, M. H. (2007) Transport capabilities of eleven Gram-positive bacteria: comparative genomic analyses. Biochim. Biophys. Acta 1768, 1342-1366
10. Faghiri, Z., Camargo, S. M., Huggel, K., Forster, I. C., Ndegwa, D., Verrey, F. and Skelly, P. J. (2010) The tegument of the human parasitic worm Schistosoma mansoni as an excretory organ: the surface aquaporin SmAQP is a lactate transporter. PLoS ONE 5, e10451
11. Tsukaguchi, H., Weremowicz, S., Morton, C. C. and Hediger, M. A. (1999) Functional and molecular characterization of the human neutral solute channel aquaporin-9. Am. J. Physiol. 277, F685-F696
12. Choi, W. G. and Roberts, D. M. (2007) Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J. Biol. Chem. 282, 24209-24218
13. Salema, M., Poolman, B., Lolkema, J. S., Dias, M. C. and Konings, W. N. (1994) Uniport of monoanionic L-malate in membrane vesicles from Leuconostoc oenos. Eur. J. Biochem. 225, 289-295
14. Tseng, C. P., Tsau, J. L. and Montville, T. J. (1991) Bioenergetic consequences of catabolic shifts by Lactobacillus plantarum in response to shifts in environmental oxygen and pH in chemostat cultures. J. Bacteriol. 173, 4411-4416
15. Otto, R., Sonnenberg, A. S., Veldkamp, H. and Konings, W. N. (1980) Generation of an electrochemical proton gradient in Streptococcus cremoris by lactate efflux. Proc. Natl. Acad. Sci. U.S.A. 77, 5502-5506
16. Olsen, E. B., Russell, J. B. and Henick-Kling, T. (1991) Electrogenic L-malate transport by Lactobacillus plantarum: a basis for energy derivation from malolactic fermentation. J. Bacteriol. 173, 6199-6206
17. Poolman, B., Molenaar, D., Smid, E. J., Ubbink, T., Abee, T., Renault, P. P. and Konings, W. N. (1991) Malolactic fermentation: electrogenic malate uptake and malate/lactate antiport generate metabolic energy. J. Bacteriol. 173, 6030-6037
18. Marty-Teysset, C., Posthuma, C., Lolkema, J. S., Schmitt, P., Divies, C. and Konings, W. N. (1996) Proton motive force generation by citrolactic fermentation in Leuconostoc mesenteroides. J. Bacteriol. 178, 2178-2185
19. Konings, W. N. (2006) Microbial transport: adaptations to natural environments. Antonie van Leeuwenhoek 90, 325-342
20. Pudlik, A. M. and Lolkema, J. S. (2011) Citrate uptake in exchange with intermediates in the citrate metabolic pathway in Lactococcus lactis IL1403. J. Bacteriol. 193, 706-714
21. + symporter in Arabidopsis. Plant Cell 15, 790-800
22. Bienert, G. P., Moller, A. L., Kristiansen, K. A., Schulz, A., Moller, I. M., Schjoerring, J. K. and Jahn, T. P. (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282, 1183-1192
23. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn, Cold Spring Harbour Laboratory Press, Cold Spring Harbor
24. Lambert, J. M., Bongers, R. S. and Kleerebezem, M. (2007) Cre-lox-based system for multiple gene deletions and selectable-marker removal in Lactobacillus plantarum. Appl. Environ. Microbiol. 73, 1126-1135
25. Nour-Eldin, H. H., Hansen, B. G., Norholm, M. H., Jensen, J. K. and Halkier, B. A. (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res. 34, e122
26. Nour-Eldin, H. H., Norholm, M. H. and Halkier, B. A. (2006) Screening for plant transporter function by expressing a normalized Arabidopsis full-length cDNA library in Xenopus oocytes. Plant Methods 2, 17
27. Fetter, K., Van Wilder, V., Moshelion, M. and Chaumont, F. (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16, 215-228
28. Bienert, G. P., Cavez, D., Besserer, A., Berny, M. C., Gilis, D., Rooman, M. and Chaumont, F. (2012) A conserved cysteine residue is involved in disulfide bond formation between plant plasma membrane aquaporin monomers. Biochem. J. 445, 101-111
29. Carbrey, J. M., Gorelick-Feldman, D. A., Kozono, D., Praetorius, J., Nielsen, S. and Agre, P. (2003) Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc. Natl. Acad. Sci. U.S.A. 100, 2945-2950
30. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
31. 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
32. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948
33. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425
34. Stover, B. C. and Muller, K. F. (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinf. 11, 7
35. Goffin, P., Deghorain, M., Mainardi, J. L., Tytgat, I., Champomier-Verges, M. C., Kleerebezem, M. and Hols, P. (2005) Lactate racemization as a rescue pathway for supplying D-lactate to the cell wall biosynthesis machinery in Lactobacillus plantarum. J. Bacteriol. 187, 6750-6761
36. Zurbriggen, A., Jeckelmann, J. M., Christen, S., Bieniossek, C., Baumann, U. and Erni, B. (2008) X-ray structures of the three Lactococcus lactis dihydroxyacetone kinase subunits and of a transient intersubunit complex. J. Biol. Chem. 283, 35789-35796
37. Uzcategui, N. L., Szallies, A., Pavlovic-Djuranovic, S., Palmada, M., Figarella, K., Boehmer, C., Lang, F., Beitz, E. and Duszenko, M. (2004) Cloning, heterologous expression, and characterization of three aquaglyceroporins from Trypanosoma brucei. J. Biol. Chem. 279, 42669-42676
38. Durnin, G., Clomburg, J., Yeates, Z., Alvarez, P. J., Zygourakis, K., Campbell, P. and Gonzalez, R. (2009) Understanding and harnessing the microaerobic metabolism of glycerol in Escherichia coli. Biotechnol. Bioeng. 103, 148-161
39. Ishibashi, K., Kuwahara, M., Gu, Y., Tanaka, Y., Marumo, F. and Sasaki, S. (1998) Cloning and functional expression of a new aquaporin (AQP9) abundantly expressed in the peripheral leukocytes permeable to water and urea, but not to glycerol. Biochem. Biophys. Res. Commun. 244, 268-274
40. Hansen, M., Kun, J. F., Schultz, J. E. and Beitz, E. (2002) A single, bi-functional aquaglyceroporin in blood-stage Plasmodium falciparum malaria parasites. J. Biol. Chem. 277, 4874-4882
41. Chaumont, F., Barrieu, F., Jung, R. and Chrispeels, M. J. (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol. 122, 1025-1034
42. Liu, L. H., Ludewig, U., Gassert, B., Frommer, W. B. and von Wiren, N. (2003) Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol. 133, 1220-1228
43. Casal, M., Paiva, S., Andrade, R. P., Gancedo, C. and Leao, C. (1999) The lactate-proton symport of Saccharomyces cerevisiae is encoded by JEN1. J. Bacteriol. 181, 2620-2623
44. Tsukaguchi, H., Shayakul, C., Berger, U. V., Mackenzie, B., Devidas, S., Guggino, W. B., van Hoek, A. N. and Hediger, M. A. (1998) Molecular characterization of a broad selectivity neutral solute channel. J. Biol. Chem. 273, 24737-24743
45. Fu, D., Libson, A., Miercke, L. J., Weitzman, C., Nollert, P., Krucinski, J. and Stroud, R. M. (2000) Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290, 481-486
46. Pieterse, B., Leer, R. J., Schuren, F. H. and van der Werf, M. J. (2005) Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 151, 3881-3894
47. Kozono, D., Ding, X., Iwasaki, I., Meng, X., Kamagata, Y., Agre, P. and Kitagawa, Y. (2003) Functional expression and characterization of an archaeal aquaporin. AqpM from Methanothermobacter marburgensis. J. Biol. Chem. 278, 10649-10656
48. Heller, K. B., Lin, E. C. and Wilson, T. H. (1980) Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J. Bacteriol. 144, 274-278
49. Hub, J. S. and de Groot, B. L. (2008) Mechanism of selectivity in aquaporins and aquaglyceroporins. Proc. Natl. Acad. Sci. U.S.A. 105, 1198-1203
50. Ishibashi, K. (2006) Aquaporin superfamily with unusual npa boxes: S-aquaporins (superfamily, sip-like and subcellular-aquaporins). Cell. Mol. Biol. 52, 20-27
51. Pettersson, N., Filipsson, C., Becit, E., Brive, L. and Hohmann, S. (2005) Aquaporins in yeasts and filamentous fungi. Biol. Cell. 97, 487-500
52. Harold, F. M. and Levin, E. (1974) Lactic acid translocation: terminal step in glycolysis by Streptococcus faecalis. J. Bacteriol. 117, 1141-1148
53. Gätje, G., Müller, V. and Gottschalk, G. (1991) Lactic acid excretion via carrier-mediated facilitated diffusion in Lactobacillus helveticus. Appl. Microbiol. Biotechnol. 34, 778-782
54. Nunez, M. F., Kwon, O., Wilson, T. H., Aguilar, J., Baldoma, L. and Lin, E. C. (2002) Transport of L-lactate, D-lactate, and glycolate by the LldP and GlcA membrane carriers of Escherichia coli. Biochem. Biophys. Res. Commun. 290, 824-829