Occurrence of Choline and Glycine Betaine Uptake and Metabolism in the Family Rhizobiaceae and Their Roles in Osmoprotection

Abstract

The role of glycine betaine and choline in osmoprotection of various Rhizobium, Sinorhizobium,Mesorhizobium, Agrobacterium, andBradyrhizobium reference strains which display a large variation in salt tolerance was investigated. When externally provided, both compounds enhanced the growth of Rhizobium tropici,Sinorhizobium meliloti, Sinorhizobium fredii,Rhizobium galegae, Agrobacterium tumefaciens,Mesorhizobium loti, and Mesorhizobium huakuii, demonstrating their utilization as osmoprotectants. However, both compounds were inefficient for the most salt-sensitive strains, such asRhizobium leguminosarum (all biovars), Agrobacterium rhizogenes, Rhizobium etli, and Bradyrhizobium japonicum. Except for B. japonicum, all strains exhibit transport activity for glycine betaine and choline. When the medium osmolarity was raised, choline uptake activity was inhibited, whereas glycine betaine uptake was either increased in R. leguminosarum and S. meliloti or, more surprisingly, reduced in R. tropici, S. fredii, and M. loti. The transport of glycine betaine was increased by growing the cells in the presence of the substrate. With the exception ofB. japonicum, all strains were able to use glycine betaine and choline as sole carbon and nitrogen sources. This catabolic function, reported for only a few soil bacteria, could increase competitiveness of rhizobial species in the rhizosphere. Choline dehydrogenase and betaine-aldehyde dehydrogenase activities were present in the cells of all strains with the exception of M. huakuii and B. japonicum. The main physiological role of glycine betaine in the family Rhizobiaceae seems to be as an energy source, while its contribution to osmoprotection is restricted to certain strains.

Phosphatidylcholine levels of peanut-nodulatingBradyrhizobiumsp. SEMIA 6144 affect cell size and motility

“…Although minor Pcs activity was detected, it was found that SEMIA 6144 is incapable of incorporating [ 14 C]choline from the medium (data not shown). This is consistent with a previous study that had shown that all the rhizobial strains tested, except B. japonicum, possess a choline uptake activity and can use choline as a carbon, nitrogen and energy source for growth (Boncompagni et al, 1999).…”

“…Recently, Hacker et al (2008) have reported the presence of multiple functional phospholipid N-methyltransferases (Pmts) exhibiting different substrate specificities in B. japonicum and proposed a model in which phosphatidylcholine biosynthesis is achieved mainly by the concerted action of PmtA and PmtX1. Although it has been reported that B. japonicum is unable to take up choline (Boncompagni et al, 1999), its genome contains a functional Pcs (Hacker et al, 2008) and some Pcs activity can be detected in cell extracts of B. japonicum (Martínez-Morales et al, 2003).…”

Characterization of  the quaternary amine transporters ofRhizobium leguminosarumbv.viciae3841

“…The absence of a BetS like system in R. leguminosarum may be important in the sensitivity of this species to NaCl stress. This sensitivity of all three biovars of R. leguminosarum to NaCl stress and the inability of choline and glycine betaine to protect against it has been observed previously (Boncompagni et al, 1999). In this study a much wider range of compatible solutes were tested but again none were effective.…”

Synthesis of phosphatidylcholine, a typical eukaryotic phospholipid, is necessary for full virulence of the intracellular bacterial parasite Brucella abortus

“…This is compatible with the idea that a moderately active PmtA is progressively taking over PC synthesis in vivo because choline becomes either unavailable in the Brucella vacuole or used for other purposes. Indeed, choline can be used to synthesize the osmoprotectant glycine betaine, and some α-2 Proteobacteria also use it as C and N source (Smith et al, 1988;Boncompagni et al, 1999). Again, the behaviour of the double mutant in mice is fully consistent with these possibilities and supports the interpretation that PC is necessary for B. abortus virulence.…”