Regulation of D-galacturonate metabolism in Caulobacter crescentus by HumR, a LacI-family transcriptional repressor


The oligotrophic freshwater bacterium Caulobacter crescentus encodes a cluster of genes (CC_1487 to CC_1495) shown here to be necessary for metabolism of D-galacturonate, the primary constituent of pectin, a major plant polymer. Sequence analysis suggests that these genes encode a version of the bacterial hexuronate isomerase pathway. A conserved 14 bp sequence motif is associated with promoter regions of three operons within this cluster, and is conserved in homologous gene clusters in related alpha-Proteobacteria. Embedded in the hexuronate gene cluster is a gene (CC_1489) encoding a member of the LacI family of bacterial transcription factors. This gene product, designated here as HumR (hexuronate metabolism regulator), represses expression of the uxaA and uxaC operon promoters by binding to the conserved operator sequence. Repression is relieved in the presence of galacturonate or, to a lesser extent, by glucuronate. Other genes potentially involved in pectin degradation and hexuronate transport are also under the control of HumR. Adoption of a LacI-type repressor to control hexuronate metabolism parallels the regulation of xylose, glucose, and maltose utilization in C. crescentus, but is distinct from the use of GntR-type repressors to control pectin and hexuronate utilization in gamma-Proteobacteria such as Escherichia coli.

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Sheikh, A. , Caswell, D. , Dick, C. , Gang, S. , Jarrell, J. , Kohli, A. , Lieu, A. , Lumpe, J. , Garrett, M. , Parker, J. and Stephens, C. (2013) Regulation of D-galacturonate metabolism in Caulobacter crescentus by HumR, a LacI-family transcriptional repressor. Advances in Bioscience and Biotechnology, 4, 63-74. doi: 10.4236/abb.2013.410A3008.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Mohnen, D. (2008) Pectin structure and biosynthesis. Current Opinion in Plant Biology, 11, 266-277.
[2] Abbott, D.W. and Boraston, A.B. (2008) Structural biology of pectin degradation by Enterobacteriaceae. Microbiology and Molecular Biology Reviews, 72, 301-316.
[3] Richard, P. and Hilditch, S. (2009) D-galacturonic acid catabolism in microorganisms and its biotechnological relevance. Applied Microbiology and Biotechnology, 82, 597-604.
[4] Yadav, S., Yadav, P., Yadav, D. and Yadav, K. (2009) Pectin lyase: A review. Process Biochemistry, 44, 1-10.
[5] Hugouvieux-Cotte-Pattat, N. and Robert-Baudouy, J. (1987) Hexuronate catabolism in Erwinia chrysanthemi. Journal of Bacteriology, 169, 1223-1231.
[6] Entcheva-Dimitrov, P. and Spormann, A.M. (2004) Dynamics and control of biofilms of the oligotrophic bacterium Caulobacter crescentus. Journal of Bacteriology, 186, 8254-8266.
[7] Poindexter, J. (1964) Biological properties and classification of the Caulobacter group. Bacteriology Reviews, 28, 231-295.
[8] Nierman, W.C., Feldblyum, T.V., Laub, M.T., Paulsen, I.T., Nelson, K.E., Eisen, J., et al. (2001) Complete genome sequence of Caulobacter crescentus. Proceedings of the National Academy of Sciences of USA, 98, 4136-4141.
[9] Mannisto, M.K., Tiirola, M.A., Salkinoja-Salonen, M.S., Kulomaa, M.S. and Puhakka, J.A. (1999) Diversity of chlorophenol-degrading bacteria isolated from contaminated boreal groundwater. Archives of Microbiology, 171, 189-197.
[10] Luo, Y., Xu, X., Ding, Z., Liu, Z., Zhang, B., Yan, Z., Sun, J., Hu, S. and Hu, X. (2008) Complete genome of Phenylobacterium zucineum, a novel facultative intracellular bacterium isolated from human erythroleukemia cell line K562. BioMed Central Genomics, 9, 386.
[11] Hottes, A.K., Meewan, M., Yang, D., Arana, N., Romero, P., McAdams, H.H. and Stephens, C. (2004) Transcriptional profiling of Caulobacter crescentus during growth on complex and minimal media. Journal of Bacteriology, 186, 1448-1461.
[12] Stephens, C., Christen, B., Fuchs, T., Sundaram, V., Watanabe, K. and Jenal, U. (2007) Genetic analysis of a novel pathway for D-xylose metabolism in Caulobacter crescentus. Journal of Bacteriology, 189, 2181-2185.
[13] Stephens, C., Christen, B., Watanabe, K., Fuchs, T. and Jenal, U. (2008) Regulation of D-xylose metabolism in Caulobacter crescentus by a LacI-type repressor. Journal of Bacteriology, 189, 8828-8834.
[14] Meisenzahl, A.C., Shapiro, L. and Jenal, U. (1997) Isolation and characterization of a xylose-dependent promoter from Caulobacter crescentus. Journal of Bacteriology, 179, 592-600.
[15] Ely, B. (1991) Genetics of Caulobacter crescentus. Methods in Enzymology, 204, 372-384.
[16] Bochner, B.R. (2003) New technologies to assess genotype-phenotype relationships. Nature Reviews Genetics, 4, 309-314.
[17] West, L., Yang, D. and Stephens, C. (2002) Use of the Caulobacter crescentus genome sequence to develop a method for systematic genetic mapping. Journal of Bacteriology, 184, 2155-2166.
[18] Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31, 3406-3415.
[19] Stephens, C. and Shapiro, L. (1993) An unusual promoter controls cell-cycle regulation and dependence on DNA replication of the Caulobacter fliLM early flagellar operon. Molecular Microbiology, 9, 1169-1179.
[20] Hruz, T., Wyss, M., Docquier, M., Pfaffl, M., Masanetz, S., Borghi, L., et al. (2011) RefGenes: identification of reliable and condition specific reference genes for RTqPCR data normalization. BMC Genomics, 12, 156.
[21] Lohmiller, S., Hantke, K., Patzer, S.I. and Braun, V. (2008) TonB-dependent maltose transport by Caulobacter crescentus. Microbiology, 154, 1748-1754.
[22] Livak, K.J. and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2[-Δ Δ C[T]] method]. Methods, 25, 402-408.
[23] Williams, K.P., Sobral, B. and Dickerman, A. (2007) A robust species tree for the Alphaproteobacteria. Journal of Bacteriology, 189, 4578-4586.
[24] Boer, H., Maaheimo, H., Koivula, A., Penttila, M. and Richard, P. (2009) Identification in Agrobacterium tumefaciens of the galacturonic acid dehydrogenase gene. Applied Microbiology and Biotechnology, 86, 901-909.
[25] Riley, R.G. and Kolodziej, B.J. (1976) Pathway of glucose catabolism in Caulobacter crescentus. Microbios, 1, 219-226.
[26] Bailey, T., Bodén, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., et al. (2009) MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Research, 37, W202-W208.
[27] Fischer, M., Zhang, Q.Y., Hubbard, R.E. and Thomas, G.H. (2010) Caught in a TRAP: Substrate-binding proteins in secondary transport. Trends in Microbiology, 18, 471-478.
[28] Haseloff, B.J., Freeman, T.L., Valmeekam, V., Melkus, M.W., Oner, F., Valachovic, M.S. and San Francisco, M.J. (1998) The exuT gene of Erwinia chrysanthemi EC16: Nucleotide sequence, expression, localization, and relevance of the gene product. Molecular Plant-Microbe Interactions, 11, 270-276.
[29] Collmer, A., Whalen, C., Beer, S. and Bateman, D. (1982) An exo-poly-α-D-galacturonosidase implicated in the regulation of extracellular pectatelyase production in Erwiniachrystanthemi. Journal of Bacteriology, 149, 626-634.
[30] Swint-Kruse, L. and Matthews, K. (2009) Allostery in the LacI/GalR family: Variations on a theme. Current Opinions in Microbiology, 12, 129-137.
[31] Lin, J.-S. and Shaw, G.-C. (2007) Regulation of the kduID operon of Bacillus subtilis by the KdgR repressor and the ccpA gene: Identification of two KdgR-binding sites within the kdgR-kduI intergenic region. Microbiology, 153, 701-710.
[32] Blanvillain, S., Meyer, D., Boulanger, A., Lautier, M., Guynet, C., Denanc, A.N., Vasse, J., Lauber, E. and Arlat, M. (2007) Plant carbohydrate scavenging through TonB-dependent receptors: A feature shared by phytopathogenic and aquatic bacteria. PLoS One, 2, e224.
[33] Hugouvieux-Cotte-Pattat, N., Condemine, G., Nassar, W. and Reverchon, S. (1996) Regulation of pectinolysis in Erwinia chrysanthemi. Annual Review of Microbiology, 50, 213-257.
[34] Rodionov, D.A., Gelfand, M.S. and Hugouvieux-Cotte-Pattat, N. (2004) Comparative genomics of the KdgR regulon in Erwinia chrysanthemi 3937 and other gamma-proteobacteria. Microbiology, 150, 3571-3590.
[35] Rodionov, D.A., Mironov, A.A., Rakhmaninova, A.B. and Gelfand, M.S. (2000) Transcriptional regulation of transport and utilization systems for hexuronides, hexuronates and hexonates in gamma purple bacteria. Molecular Microbiology, 38, 673-683.
[36] Da Silva, A.C., Ferro, J.A., Reinach, F.C., Farah, C.S., Furlan, L.R., Quaggio, R.B., et al. (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature, 417, 459-463.
[37] Price, M.N., Dehal, P. and Arkin, A. (2008) Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli. Genome Biology, 9, R4.

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