Rhizobial acyl carrier proteins and their roles in the formation of bacterial cell-surface components that are required for the development of nitrogen-fixing root nodules on legume hosts
Otto Geiger,
Isabel M López-Lara,
Corresponding Author
Otto Geiger
Centro de Investigación sobre Fijación de Nitrógeno, Universidad Nacional Autónoma de México, Apdo. Postal 565-A, Cuernavaca, Morelos CP62210, Mexico
*Corresponding author. Tel.: +52 (7773) 131697; Fax: +52 (7773) 175581, E-mail: [email protected]Search for more papers by this authorIsabel M López-Lara
Centro de Investigación sobre Fijación de Nitrógeno, Universidad Nacional Autónoma de México, Apdo. Postal 565-A, Cuernavaca, Morelos CP62210, Mexico
Search for more papers by this authorOtto Geiger,
Isabel M López-Lara,
Corresponding Author
Otto Geiger
Centro de Investigación sobre Fijación de Nitrógeno, Universidad Nacional Autónoma de México, Apdo. Postal 565-A, Cuernavaca, Morelos CP62210, Mexico
*Corresponding author. Tel.: +52 (7773) 131697; Fax: +52 (7773) 175581, E-mail: [email protected]Search for more papers by this authorIsabel M López-Lara
Centro de Investigación sobre Fijación de Nitrógeno, Universidad Nacional Autónoma de México, Apdo. Postal 565-A, Cuernavaca, Morelos CP62210, Mexico
Search for more papers by this authorAbstract
Acyl carrier protein (ACP) of Escherichia coli is a small acidic protein which functions as carrier of growing acyl chains during their biosynthesis and as donor of acyl chains during transfer to target molecules. This unique ACP of E. coli is expressed constitutively. In more complex bacteria, multiple ACPs are present, indicating a channeling of pools of multi-carbon units into different biosynthetic routes. In rhizobia, for example, besides the constitutive ACP (AcpP) involved in the biosynthesis and transfer of common fatty acids, three specialized ACPs have been reported: (1) the flavonoid-inducible nodulation protein NodF, (2) AcpXL that transfers 27-hydroxyoctacosanoic acid to a sugar backbone during lipid A biosynthesis, and (3) the RkpF protein which is required for the biosynthesis of rhizobial capsular polysaccharides. All three of those specialized rhizobial ACPs are required for the biosynthesis of cell-surface molecules that play a role in establishing the symbiotic relationship between rhizobia and their legume hosts. Surprisingly, the recently sequenced genomes from Mesorhizobium loti and Sinorhizobium meliloti suggest even more candidates for ACPs in rhizobia.
References
- [1] Geiger, O. (1998) Phospholipids and alternative membrane lipids. In: The Rhizobiaceae. Molecular Biology of Model Plant-Associated Bacteria (Spaink, H.P., Kondorosi, A. and Hooykaas, P.J.J., Eds.), pp. 55–80. Kluwer Academic Publishers, Dordrecht.
- [2] Rawlings, M, Cronan, J.E. (1992) The gene encoding Escherichia coli acyl carrier protein lies within a cluster of fatty acid biosynthetic genes. J. Biol. Chem. 267, 5751–5754.
- [3] Withers, H, Swift, S, Williams, P (2001) Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr. Opin. Microbiol. 4, 186–193.
- [4] Tang, L, Weissborn, A.C., Kennedy, E.P. (1997) Domains of Escherichia coli acyl carrier protein important for membrane-derived oligosaccharide biosynthesis. J. Bacteriol. 179, 3697–3705.
- [5] Moulin, L, Munive, A, Dreyfus, B, Boivin-Masson, C (2001) Nodulation of legumes by members of the beta-subclass of proteobacteria. Nature 411, 948–950.
- [6] López-Lara, I.M., Geiger, O (2000) Expression and purification of four different rhizobial acyl carrier proteins. Microbiology 146, 839–849.
- [7] Spaink, H.P. (2000) Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 54, 257–288.
- [8] John, M, Röhrig, H, Schmidt, J, Wieneke, U, Schell, J (1993) Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc. Natl. Acad. Sci. USA 90, 625–629.
- [9] Schultze, M, Kondorosi, A (1995) The role of Nod signal structures in the determination of host specificity in the Rhizobium-legume symbiosis. World J. Microbiol. Biotechnol. 12, 137–149.
- [10] Shearman, C.A., Rossen, L, Johnston, A.W.B., Downie, J.A. (1986) The Rhizobium leguminosarum nodulation gene nodF encodes a polypeptide similar to acyl-carrier protein and is regulated by nodD plus a factor in pea root exudate. EMBO J. 5, 647–652.
- [11] Geiger, O, Thomas-Oates, J.E., Glushka, J, Spaink, H.P., Lugtenberg, B.J.J. (1994) Phospholipids of Rhizobium contain nodE-determined highly unsaturated fatty acid moieties. J. Biol. Chem. 269, 11090–11097.
- [12] Geiger, O, Spaink, H.P., Kennedy, E.P. (1991) Isolation of Rhizobium leguminosarum NodF nodulation protein: NodF carries a 4′-phosphopantetheine prosthetic group. J. Bacteriol. 173, 2872–2878.
- [13] Ritsema, T, Geiger, O, van Dillewijn, P, Lugtenberg, B.J.J., Spaink, H.P. (1994) Serine residue 45 of nodulation protein NodF of Rhizobium leguminosarum biovar viciae is essential for biological function. J. Bacteriol. 176, 7740–7743.
- [14] Ritsema, T, Gehring, A.M., Stuitje, A.R., van der Drift, K.M.G.M., Dandal, I, Lambalot, R.H., Walsh, C.T., Thomas-Oates, J.E., Lugtenberg, B.J.J., Spaink, H.P. (1998) Functional analysis of an interspecies chimera of acyl carrier proteins indicates a specialized domain for protein recognition. Mol. Gen. Genet. 257, 641–648.
- [15] Demont, N, Debellé, F, Aurelle, H, Dénarié, J, Promé, J.C. (1993) Role of the Rhizobium meliloti nodF and nodE genes in the biosynthesis of the lipo-oligosaccharidic nodulation factors. J. Biol. Chem. 268, 20134–20142.
- [16] Bloemberg, G.V., Kamst, E, Harteveld, M, van der Drift, K.M.G.M., Haverkamp, J, Thomas-Oates, J.E., Lugtenberg, B.J.J., Spaink, H.P. (1995) A central domain of Rhizobium NodE protein mediates host specificity by determining the hydrophobicity of fatty acyl moieties of nodulation factors. Mol. Microbiol. 16, 1123–1136.
- [17] Lerouge, P, Roche, P, Faucher, C, Maillet, F, Truchet, G, Promé, J.C., Dénarie, J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature (Lond.) 344, 781–784.
- [18] Schultze, M, Quiclet-Sire, B, Kondorosi, E, Virelizier, H, Glushka, J.N., Endre, G, Gero, S.D., Kondorosi, A (1992) Rhizobium meliloti produces a family of sulfated lipo-oligosaccharides exhibiting different degrees of host specificity. Proc. Natl. Acad. Sci. USA 89, 192–196.
- [19] Spaink, H.P., Sheeley, D.M., van Brussel, A.A.N., Glushka, J, York, W.S., Tak, T, Geiger, O, Kennedy, E.P., Reinhold, V.N., Lugtenberg, B.J.J. (1991) A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354, 125–130.
- [20] van der Drift, K.M.G.M., Spaink, H.P., Bloemberg, G.V., van Brussel, A.A.N., Lugtenberg, B.J.J., Haverkamp, J, Thomas-Oates, J.E. (1996) Rhizobium leguminosarum bv. trifolii produces lipo-chitin oligosaccharides with nodE-dependent highly unsaturated fatty acyl moieties. J. Biol. Chem. 271, 22563–22569.
- [21] Yang, G.-P, Debellé, F, Savagnac, A, Ferro, M, Schiltz, O, Maillet, F, Promé, D, Treilhou, M, Vialas, C, Lindstrom, K, Dénarié, J, Promé, J.-C (1999) Structure of the Mesorhizobium huakuii and Rhizobium galegae Nod factors: a cluster of phylogenetically related legumes are nodulated by rhizobia producing Nod factors with α,β-unsaturated N-acyl substitutions. Mol. Microbiol. 34, 227–237.
- [22] Poinsot, V, Bélanger, E, Laberge, S, Yang, G.-P, Antoun, H, Cloutier, J, Treilhou, M, Dénarié, J, Promé, J.-C, Debellé, F (2001) Unusual methyl-branched α,β-unsaturated acyl chain substitutions in the Nod factors of an arctic Rhizobium, Mesorhizobium sp. strain N33 (Oxytropis arctobia). J. Bacteriol. 183, 3721–3728.
- [23] Niwa, S, Kawaguchi, M, Imaizumi-Anraku, H, Chechetka, S.A., Ishizaka, M, Ikuta, A, Kouchi, H (2001) Responses of a model legume Lotus japonicus to lipochitin oligosaccharide nodulation factors purified from Mesorhizobium loti JRL501. Mol. Plant–Microbe Interact. 14, 848–856.
- [24] López-Lara, I.M., Geiger, O (2001) The nodulation protein NodG shows the enzymatic activity of an 3-oxoacyl-acyl carrier protein reductase. Mol. Plant–Microbe Interact. 14, 349–357.
- [25] Geiger, O, Glushka, J, Lugtenberg, B.J.J., Spaink, H.P., Thomas-Oates, J.E. (1998) NodFE-dependent fatty acids that lack an α-β unsaturation are subject to differential transfer, leading to novel phospholipids. Mol. Plant–Microbe Interact. 11, 33–44.
- [26] Debellé, F, Plazanet, C, Roche, P, Pujol, C, Savagnac, A, Rosenberg, C, Promé, J.-C, Dénarié, J (1996) The NodA proteins of Rhizobium meliloti and Rhizobium tropici specify the N-acylation of Nod factors by different fatty acids. Mol. Microbiol. 22, 303–314.
- [27] Ritsema, T, Wijfjes, A.H.M., Lugtenberg, B.J.J., Spaink, H.P. (1996) Rhizobium nodulation protein NodA is a host-specific determinant of the transfer of fatty acids in Nod factor biosynthesis. Mol. Gen. Genet. 251, 44–51.
- [28] Gressent, F, Drouillard, S, Mantegazza, N, Samain, E, Geremia, R.A., Canut, H, Niebel, A, Driguez, H, Ranjeva, R, Cullimore, J, Bono, J.-J (1999) Ligand specificity of a high-affinity binding site for lipo-chitooligosaccharidic Nod factors in Medicago cell suspension cultures. Proc. Natl. Acad. Sci. USA 96, 4704–4709.
- [29] Schlaman, H.R.M., Gisel, A.A., Quaedvlieg, N.E.M., Bloemberg, G.V., Lugtenberg, B.J.J., Kijne, J.W., Potrykus, I, Spaink, H.P., Sautter, C (1997) Chitin oligosaccharides can induce cortical cell division in roots of Vicia sativa when delivered by ballistic microtargeting. Development 124, 4887–4893.
- [30] Staehelin, C, Schultze, M, Kondorosi, E, Mellor, R.B., Boller, T, Kondorosi, A (1994) Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. Plant J. 5, 319–330.
- [31] Spaink, H.P., Wijfjes, A.H., Lugtenberg, B.J.J. (1995) Rhizobium NodI and NodJ proteins play a role in the efficiency of secretion of lipochitin oligosaccharides. J. Bacteriol. 177, 6276–6281.
- [32] Orgambide, G.G., Lee, J, Hollingsworth, R.I., Dazzo, F.B. (1995) Structurally diverse chitolipooligosaccharide Nod factors accumulate primarily in membranes of wild type Rhizobium leguminosarum biovar trifolii. Biochemistry 34, 3832–3840.
- [33] Bhat, U.R., Mayer, H, Yokota, A, Hollingsworth, R.I., Carlson, R.W. (1991) Occurence of lipid A variants with 27-hydroxyoctacosanoic acid in lipopolysaccharides from members of the family Rhizobiaceae. J. Bacteriol. 173, 2155–2159.
- [34] Brozek, K.A., Carlson, R.W., Raetz, C.R.H. (1996) A special acyl carrier protein for transferring long hydroxylated fatty acids to lipid A in Rhizobium. J. Biol. Chem. 271, 32126–32136.
- [35] Que, N.L.S., Ribeiro, A.A., Raetz, C.R.H. (2000) Two-dimensional NMR spectroscopy and structures of six lipid A species from Rhizobium etli CE3. J. Biol. Chem. 275, 28017–28027.
- [36] Demont, N, Ardourel, M, Maillet, F, Promé, D, Ferro, M, Promé, J.-C, Dénarié, J (1994) The Rhizobium meliloti regulatory nodD3 and syrM genes control the synthesis of a particular class of nodulation factors N-acylated by (ω-1)-hydroxylated fatty acids. EMBO J. 13, 2139–2149.
- [37] Reuhs, B.L., Carlson, R.W., Kim, J.S. (1993) Rhizobium fredii and Rhizobium meliloti produce 3-deoxy-d-manno-2-octulosonic acid-containing polysaccharides that are structurally analogous to group II K antigens (capsular polysaccharides) found in Escherichia coli. J. Bacteriol. 175, 3570–3580.
- [38] Petrovics, G, Putnoky, P, Reuhs, B, Kim, J, Thorp, T.A., Noel, K.D., Carlson, R.W., Kondorosi, A (1993) The presence of a novel type surface polysaccharide in Rhizobium meliloti requires a new fatty acid synthase-like gene cluster involved in symbiotic nodule development. Mol. Microbiol. 8, 1083–1094.
- [39] Epple, G, van der Drift, K.M.G.M., Thomas-Oates, J.E., Geiger, O (1998) Characterization of a novel acyl carrier protein, RkpF, encoded by an operon involved in capsular polysaccharide biosynthesis in Sinorhizobium meliloti. J. Bacteriol. 180, 4950–4954.
- [40] Ghose, R, Geiger, O, Prestegard, J.H. (1996) NMR investigations of the structural properties of the nodulation protein, NodF, from Rhizobium leguminosarum and its homology with Escherichia coli acyl carrier protein. FEBS Lett. 388, 66–72.
- [41] Fowler, C.A., Tian, F, Al-Hashimi, H.M., Prestegard, J.H. (2000) Rapid determination of protein folds using residual dipolar couplings. J. Mol. Biol. 304, 447–460.
- [42] Crump, M.P., Crosby, J, Dempsey, C.E., Parkinson, J.A., Murray, M, Hopwood, D.A., Simpson, T.J. (1997) Solution structure of the actinorhodin polyketide synthase acyl carrier protein from Streptomyces coelicolor A3. Biochemistry 36, 6000–6008.
- [43] Bergès, H., Checroun, C., Guiral, S., Garnerone, A.-M., Boistard, P. and Batut, J. (2001) A glutamine-amidotransferase-like protein modulates FixT antikinase activity in Sinorhizobium meliloti. BMC Microbiology 1, http://www.biomedcentral.com/1471-2180/1/6.
- [44] Wu, K, Chung, L, Revill, W.P., Katz, L, Reeves, C.D. (2000) The FK520 gene cluster of Streptomyces hygroscopicus var. ascomyceticus (ATCC 14891) contains genes for biosynthesis of unusual polyketide extender units. Gene 251, 81–90.
- [45] Heath, R.J., Rock, C.O. (1995) Enoyl-acyl carrier protein reductase (fabI) plays a determinant role in completing cycles of fatty acid elongation in Escherichia coli. J. Biol. Chem. 270, 26538–26542.
