Lack of trehalose catabolism in Sinorhizobium species increases their nodulation competitiveness on certain host genotypes

Abstract

Summary• The role of host and bacterial genotypes in determining the competitiveness of trehalose utilization mutants of Sinorhizobium meliloti and Sinorhizobium medicae was investigated here.• Trehalose utilization mutants of S. meliloti and S. medicae were obtained by mutagenesis of their trehalose utilization gene thuB. The mutant strains and the wild type were coinoculated on three cultivars of alfalfa (Medicago sativa) and two cultivars of Medicago truncatula and assessed for competitiveness in root colonization, and nodule occupancy.• The thuB mutants formed more nodules than their parent strains on two of the three alfalfa lines tested and on one of the two M. truncatula lines tested. They were not more competitive on the other alfalfa and M. truncatula lines. Their competitiveness for nodule occupancy did not correlate positively with their ability to colonize these roots but correlated with the extent of thuB induction in the infection threads. Induction of thuB was shown to be dependent on the concentration of trehalose in the environment.• These results suggest a direct role for host trehalose metabolism in early plantsymbiont interactions and show that the ability to manage host-induced stresses during infection, rather than the ability to colonize the root, is critical for competitive nodulation.

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

“…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.…”

“…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.…”

Functional Role of Bradyrhizobium japonicum Trehalose Biosynthesis and Metabolism Genes during Physiological Stress and Nodulation

“…For example, R. leguminosarum mutants lacking the OtsAB and TreYZ pathways were reported to form effective nitrogenfixing nodules on Trifolium repens, although the mutants had enhanced competitiveness relative to the wild-type strain (20). In contrast, thuB mutants, which lacked trehalose catabolism, showed an enhanced competitiveness phenotype only on certain host genotypes in the Sinorhizobium-Medicago symbiotic interaction (1). Similarly, trehalose concentration in bacteroids has been shown to vary in different host genotypes that have been inoculated by Bradyrhizobium strains (34,38).…”

“…Suarez et al (39) reported an increase in root nodule number and nitrogen fixation by Phaseolus vulgaris inoculated with a trehalose-6-phosphate synthase-overexpressing strain of Rhizobium etli. In contrast, trehalose accumulation in Rhizobium leguminosarum and Sinorhizobium meliloti cells did not result in an increase in nitrogen-fixing nodules but led to enhancement of competitiveness on clover and on certain alfalfa genotypes, respectively (1,16,20).…”

“…Suarez et al (39) reported an increase in root nodule number and nitrogen fixation by Phaseolus vulgaris inoculated with a trehalose-6-phosphate synthase-overexpressing strain of Rhizobium etli. In contrast, trehalose accumulation in Rhizobium leguminosarum and Sinorhizobium meliloti cells did not result in an increase in nitrogen-fixing nodules but led to enhancement of competitiveness on clover and on certain alfalfa genotypes, respectively (1,16,20).Four trehalose biosynthetic pathways, mediated by OtsAB, TreS, TreYZ, and TreT, have been reported thus far for prokaryotes (8,25). The OtsAB pathway results in the condensation of glucose-6-phosphate with UDP-glucose by trehalose-6-phosphate synthase (OtsA) to form trehalose-6-phosphate.…”