Protein phosphorylation and regulation of adaptive responses in bacteria.

Infection of legume roots or stems with soil bacteria of the Rhizobiaceae results in the formation of nodules that become symbiotic nitrogen-fixing organs. Within the infected cells of these nodules, bacteria are enveloped in a membrane of plant origin, called the peribacteroid membrane (PBM), and divide and differentiate to form nitrogen-fixing bacteroids. The organelle-like structure comprised of PBM and bacteroids is termed the symbiosome, and is the basic nitrogen-fixing unit of the nodule. The major exchange of nutrients between the symbiotic partners is reduced carbon from the plant, to fuel nitrogenase activity in the bacteroid, and fixed nitrogen from the bacteroid, which is assimilated in the plant cytoplasm. However, many other metabolites are also exchanged. The metabolic interaction between the plant and the bacteroids is regulated by a series of transporters and channels on the PBM and the bacteroid membrane, and these form the focus of this review.

Metabolite transport across symbiotic membranes of legume nodules

We report the identification and cloning of an ntrA-like (glnF rpoN) gene of Rhizobium meliloti and show that the R. meliloti ntrA product (NtrA) is required for C4-dicarboxylate transport as well as for nitrate assimilation and symbiotic nitrogen fixation. DNA sequence analysis showed that R. meliloti NtrA is 38% homologous with Klebsiella pneumoniae NtrA. Subcloning and complementation analysis suggested that the R. meliloti ntrA promoter lies within 125 base pairs of the initiation codon and may be constitutively expressed.

Rhizobium meliloti ntrA (rpoN) gene is required for diverse metabolic functions.

Nitrogen fixation within legume nodules results from a complex metabolic exchange between bacteria of the family Rhizobiaciae and the plant host. Carbon is supplied to the differentiated bacterial cells, termed bacteroids, in the form of dicarboxylic acids to fuel nitrogen fixation. In exchange, fixed nitrogen is transferred to the plant. Both the bacteroid and the plant-derived peribacteroid membrane tightly regulate the exchange of metabolites. In the bacteroid oxidation of dicarboxylic acids via the TCA cycle occurs in an oxygen-limited environment. This restricts the TCA cycle at key points, such as the 2-oxoglutarate dehydrogenase complex, and requires that inputs of carbon and reductant are balanced with outputs from the TCA cycle. This may be achieved by metabolism through accessory pathways that can remove intermediates, reductant, or ATP from the cycle. These include synthesis of the carbon polymers PHB and glycogen and bypass pathways such as the recently identified 2-oxoglutarate decarboxylase reaction in soybean bacteroids. Recent labeling data have shown that bacteroids synthesize and secrete amino acids, which has led to controversy over the role of amino acids in nodule metabolism. Here we review bacteroid carbon metabolism in detail, evaluate the labeling studies that relate to amino acid metabolism by bacteroids, and place the work in context with the genome sequences of Mesorhizobium loti and Sinorhizobium meliloti. We also consider a wider range of metabolic pathways that are probably of great importance to rhizobia in the rhizosphere, during nodule initiation, infection thread development, and bacteroid development.

Metabolism of Rhizobium bacteroids

Crude extracts of Rhizobium trifolii strain 7000 contained enzymes of the Entner-Doudoroff and pentose phosphate pathways. No phosphofructokinase (EC 2.7.1.11) activity and only a low activity of fructose-1,6-bisphosphate aldolase (EC 4.1.2.13) were found, suggesting that the Embden-Meyerhof-Parnas pathway was not physiologically important in this strain.
Independent carbohydrate-negative mutants of R. trifolii were isolated and characterized as deficient in glucokinase (glk; EC 2.7.1.2), fructose uptake (fup), the Entner-Doudoroff pathway (edp) and pyruvate carboxylase (pyc;EC 6.4.1.1). Glucokinase was essential for glucose phosphorylation in R. trifolii and was also required for growth on sucrose. The edp mutant was impaired in growth on all hexoses tested except galactose, suggesting that the ED pathway was the major pathway used by R. trifolii for the catabolism of these sugars. Galactose may be catabolized via a different pathway, possibly involving an NADP+-linked galactose dehydrogenase. Pyruvate carboxylase was an important anaplerotic enzyme in R. trifolii required for growth on all carbon sources tested, except succinate.
All the mutants, including a glk fup double mutant, formed an effective symbiosis on red clover, suggesting that neither glucose, fructose nor sucrose are used by the bacteroids to provide ATP and reductant for nitrogen fixation. The bacteroids probably receive a supply of tricarboxylic acid cycle intermediates from the plant cytosol, and these may be their major source of energy.

Carbohydrate Metabolism in Rhizobium trifolii: Identification and Symbiotic Properties of Mutants

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Carbohydrate Metabolism in Rhizobium trifolii: Identification and Symbiotic Properties of Mutants