Role of Trehalose Transport and Utilization in Sinorhizobium meliloti-Alfalfa Interactions

Abstract

Genes thuA and thuB in Sinorhizobium meliloti Rm1021 code for a major pathway for trehalose catabolism and are induced by trehalose but not by related structurally similar disaccharides like sucrose or maltose. S. meliloti strains mutated in either of these two genes were severely impaired in their ability to grow on trehalose as the sole source of carbon. ThuA and ThuB show no homology to any known enzymes in trehalose utilization. ThuA has similarity to proteins of unknown function in Mesorhizobium loti, Agrobacterium tumefaciens, and Brucella melitensis, and ThuB possesses homology to dehydrogenases containing the consensus motif AGKHVXCEKP. thuAB genes are expressed in bacteria growing on the root surface and in the infection threads but not in the symbiotic zone of the nodules. Even though thuA and thuB mutants were impaired in competitive colonization of Medicago sativa roots, these strains were more competitive than the wild-type Rml021 in infecting alfalfa roots and forming nitrogen-fixing nodules. Possible reasons for their increased competitiveness are discussed.

The thuEFGKAB Operon of Rhizobia and Agrobacterium tumefaciens Codes for Transport of Trehalose, Maltitol, and Isomers of Sucrose and Their Assimilation through the Formation of Their 3-Keto Derivatives

“…The biochemical functions of the thuAB genes are currently unknown. As reported in our earlier study (20), we were also unable to detect glucose as a product of trehalose catabolism in S. meliloti. We have also been consistently unsuccessful in our attempts to detect other known intermediates of trehalose breakdown, such as glucose-6-phosphate, in reaction mixtures containing trehalose and induced S. meliloti cells or cell extracts, through thin-layer chromatography (TLC), HPLC, or HPLC-MS (results not presented).…”

“…We have reported that in S. meliloti, the thu operon (thuEFGKAB) is the major system for the transport and utilization of the disaccharide trehalose (19)(20)(21). The entire thu operon is also present in similar organizations with various degrees of homology and identity in the sequenced genomes of several other members of the Rhizobiaceae, as shown in Fig.…”

“…2 show that only Rm9628 is able to grow on palatinose. To determine whether growth on other carbon sources is also affected, we screened the trehalose utilization mutant Sm7024, which carries a mutation in thuB (20), for growth with various carbon sources using the commercially available phenotype microarray system Biolog (Biolog Inc., Hayward, CA). The results show that Sm7024 was impaired in the utilization of palatinose and maltitol, in addition to trehalose.…”

“…Previously, we identified and characterized the trehalose-inducible thu operon, thuEFGKAB, involved in the transport and assimilation of trehalose in Sinorhizobium meliloti and demonstrated that the genes thuEFGK of this operon code for an ATP-binding cassette for transport of trehalose and that disruption of thuAB sequences results in accumulation of trehalose in the cells, implying their role in trehalose utilization. In addition, we showed that disruption of the thuAB genes increases the nodulation competitiveness of S. meliloti, depending on the interacting host genotype (19)(20)(21). However, identification of the biochemical function(s) of the thuAB genes and elucidation of the pathway for trehalose utilization in S. meliloti have remained elusive.…”

Transcriptome Profiling Reveals the Importance of Plasmid pSymB for Osmoadaptation of Sinorhizobium meliloti

“…Induction of the thuA, thuE, and thuG genes was also observed upon an osmotic upshift. These genes are part of a cluster of six genes involved in trehalose transport and utilization (25,26).…”