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Galactitol catabolism in Sinorhizobium meliloti is dependent on a chromosomally encoded sorbitol dehydrogenase and a pSymB-encoded operon necessary for tagatose catabolism

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Abstract

The legume endosymbiont Sinorhizobium meliloti can utilize a broad range of carbon compounds to support its growth. The linear, six-carbon polyol galactitol is abundant in vascular plants and is metabolized in S. meliloti by the contribution of two loci SMb21372-SMb21377 and SMc01495-SMc01503 which are found on pSymB and the chromosome, respectively. The data suggest that several transport systems, including the chromosomal ATP-binding cassette (ABC) transporter smoEFGK, contribute to the uptake of galactitol, while the adjacent gene smoS encodes a protein for oxidation of galactitol into tagatose. Subsequently, genes SMb21374 and SMb21373, encode proteins that phosphorylate and epimerize tagatose into fructose-6-phosphate, which is further metabolized by the enzymes of the Entner–Doudoroff pathway. Of note, it was found that SMb21373, which was annotated as a 1,6-bis-phospho-aldolase, is homologous to the E. coli gene gatZ, which is annotated as encoding the non-catalytic subunit of a tagatose-1,6-bisphosphate aldolase heterodimer. When either of these genes was introduced into an Agrobacterium tumefaciens strain that carries a tagatose-6-phosphate epimerase mutation, they are capable of complementing the galactitol growth deficiency associated with this mutation, strongly suggesting that these genes are both epimerases. Phylogenetic analysis of the protein family (IPR012062) to which these enzymes belong, suggests that this misannotation is systemic throughout the family. S. meliloti galactitol catabolic mutants do not exhibit symbiotic deficiencies or the inability to compete for nodule occupancy.

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Acknowledgements

This work was funded by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants awarded to IJO and TMF. MGK acknowledges support from the University of Manitoba Faculty of Science Award and the University of Manitoba Faculty of Graduate Studies GETS program.

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This study was funded by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants awarded to IJO and TMF.

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  1. Department of Microbiology, University of Manitoba, Winnipeg, MB, R3T 2N2, Canada

    MacLean G. Kohlmeier & Ivan J. Oresnik

  2. Department of Biology, McMaster University, Hamilton, ON, Canada

    Catherine E. White, Jane E. Fowler & Turlough M. Finan

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Fig. S1 Digital version of the phylogeny displayed in Figure 8, zooming in reveals organism names and bootstrap values (EPS 9819 KB)

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Kohlmeier, M.G., White, C.E., Fowler, J.E. et al. Galactitol catabolism in Sinorhizobium meliloti is dependent on a chromosomally encoded sorbitol dehydrogenase and a pSymB-encoded operon necessary for tagatose catabolism. Mol Genet Genomics 294, 739–755 (2019). https://doi.org/10.1007/s00438-019-01545-z

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