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The bacterial cell envelope is of critical importance to the function and survival of the cell; it acts as a barrier against harmful toxins while allowing the flow of nutrients into the cell. It also serves as a point of physical contact between a bacterial cell and its host. Hence, the cell envelope of Rhizobium leguminosarum is critical to cell survival under both free-living and symbiotic conditions. Transposon mutagenesis of R. leguminosarum strain 3841 followed by a screen to isolate mutants with defective cell envelopes led to the identification of a novel conserved operon (RL3499-RL3502) consisting of a putative moxR -like AAA + ATPase, a hypothetical protein with a domain of unknown function (designated domain of unknown function 58), and two hypothetical transmembrane proteins. Mutation of genes within this operon resulted in increased sensitivity to membrane-disruptive agents such as detergents, hydrophobic antibiotics, and alkaline pH. On minimal media, the mutants retain their rod shape but are roughly 3 times larger than the wild type.
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On media containing glycine or peptides such as yeast extract, the mutants form large, distorted spheres and are incapable of sustained growth under these culture conditions. Expression of the operon is maximal during the stationary phase of growth and is reduced in a chvG mutant, indicating a role for this sensor kinase in regulation of the operon. Our findings provide the first functional insight into these genes of unknown function, suggesting a possible role in cell envelope development in Rhizobium leguminosarum. Given the broad conservation of these genes among the Alphaproteobacteria. the results of this study may also provide insight into the physiological role of these genes in other Alphaproteobacteria. including the animal pathogen Brucella.
Rhizobium leguminosarum is a Gram-negative, rod-shaped, soil-dwelling bacterium that forms a mutualistic association with leguminous plants (20 ). R. leguminosarum must be able to adapt to diverse environmental conditions, both in the soil and during its transition into a host plant. R. leguminosarum. and rhizobia in general, has a complex cell envelope consisting of the cytoplasmic membrane, the peptidoglycan cell wall, the outer membrane (with several lipopolysaccharide [LPS] modifications), and a number of excreted surface polysaccharides (21. 48 ).
Numerous studies have investigated the importance of the cell envelope for survival of rhizobia both under free-living conditions and during symbiosis (11. 13. 24. 58. 61 ).
For example, the outer membranes of Rhizobium spp. are critical for resisting the harmful effects of detergents, hydrophobic antibiotics, and cationic peptides (11. 24.
58 ). In addition, loss of both the O antigen and exopolysaccharides in Rhizobium etli biovar phaseoli CE3 causes increased sensitivity to plant-derived toxic compounds such as coumestrol, suggesting that the cell envelope plays an important role in protecting rhizobia from toxins encountered in the rhizosphere (13 ). Hyper- and hypo-osmotic stress tolerances have also been associated with cell envelope components. Periplasmic cyclic β-1,2-glucans and very-long-chain fatty acid (VLCFA)-modified lipid A are required for hypo-osmotic stress tolerance in R. leguminosarum and Sinorhizobium meliloti (11. 24.
58 ), while an intact outer membrane and exopolysaccharides are necessary for tolerance to hyperosmotic stress (61 ). In addition, several surface polysaccharides, LPS, and many membrane proteins have all been shown to play essential roles in the development of a successful symbiosis (7. 16. 25. 41.
48. 59 ). Recently, rhizobial mutants harboring mutations in genes required for cell envelope development that are unable to grow on complex media have been identified (21. 58 ), such as the routinely used tryptone-yeast extract medium (TY), a peptide-rich medium composed of 5 g of tryptone, 3 g of yeast extract, and 0. 5 g of calcium chloride per liter of H 2 O (6 ).
Mutation of genes involved in synthesis of a very-long-chain fatty acid which is a component of the lipid A of LPS resulted in loss of growth on standard complex media in R. leguminosarum and S.
meliloti (15. 58 ). Homologs of the ChvI/ChvG two-component signal transduction system which regulates several key components of the cell envelope in rhizobia, are required for growth of R. leguminosarum. S. meliloti.
and Agrobacterium spp. on complex media (4. 17.
32 ). A mutation in a periplasmic protease gene, ctpA. which has been implicated in cell envelope development results in an inability of R. leguminosarum to grow on standard complex media, and the mutant forms large, spherical cells on solid TY after incubation for 24 h (22 ). All of these studies suggest a strong correlation between a fully functional cell envelope and growth of rhizobia on complex media.
To identify novel genes important for cell envelope structure and function in R. leguminosarum. we used Tn 5 transposon mutagenesis and screened for mutants unable to grow on solid complex TY.
The transposon mutagenesis screen led to the isolation of a mutant in which the Tn 5 insertion had disrupted the third gene of an operon consisting of genes annotated as encoding a moxR -like AAA + ATPase (RL3499), a conserved hypothetical protein (RL3500), and two large conserved transmembrane proteins (RL3501 and RL3502) (66 ). These genes are conserved among several alphaproteobacterial orders; however, to date they remain uncharacterized.
Using a variety of mutagenesis approaches, including single-gene in-frame deletion mutants and insertional polar mutants, we have demonstrated that the genes in this operon are important for cell envelope integrity and cell morphology. MATERIALS AND METHODS. Strains, media, and growth conditions.
Table 1 gives a list of strains and plasmids used in this study. Primer sequences are listed in Table S1 in the supplemental material. Escherichia coli strains were cultured using Luria-Bertani (LB) medium (45 ), which was supplemented as necessary with antibiotics at the following concentrations (μg ml −1 ): gentamicin, 15; ampicillin, 100; spectinomycin, 100; and tetracycline, 10. R. leguminosarum cells were cultured using tryptone-yeast extract medium (TY) (6 ) or Vincent's minimal medium with 10 mM mannitol (VMM) (60 ), supplemented as required with antibiotics at the following concentrations (μg ml −1 ): gentamicin, 30; neomycin, 100; tetracycline, 5; and streptomycin, 500.