Role of Symbiotic Auxotrophy in the Rhizobium-Legume Symbioses

Prell, Jürgen; Bourdès, Alexandre; Kumar, Sumit; Lodwig, E. M.; Hosie, Arthur H.F.; Kinghorn, Seonag; White, James P.; Poole, Philip S.

doi:10.1371/journal.pone.0013933

Cited by 57 publications

(53 citation statements)

References 37 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Upon the establishment of a functional symbiotic association, free-living Rhizobium bacteroids surrender their ability to synthesize the branched-chain amino acids (isoleucine, leucine, and valine) and become dependent on the host plant for supply of these nutrients, a phenomenon that is called "symbiotic auxotrophy" (2). Significantly, the supply of branched-chain amino acids to Rhizobium bacteroids provides a mechanism by which legume host plants regulate the development and persistence of Rhizobium bacteroids (2,34). Likewise, as a result of extensive genome erosion, Buchnera cannot synthesize seven nonessential amino acids (asparagine, aspartate, glutamate, glutamine, proline, serine, and tyrosine) (11) and therefore also can be classified as symbiotic auxotrophs.…”

Section: Discussionmentioning

confidence: 99%

Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts

Price

Feng

Baker

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

108

158

View full text Add to dashboard Cite

Endosymbiotic associations have played a major role in evolution. However, the molecular basis for the biochemical interdependence of these associations remains poorly understood. The aphid–Buchnera endosymbiosis provides a powerful system to elucidate how these symbioses are regulated. In aphids, the supply of essential amino acids depends on an ancient nutritional symbiotic association with the gamma-proteobacterium Buchnera aphidicola. Buchnera cells are densely packed in specialized aphid bacteriocyte cells. Here we confirm that five putative amino acid transporters are highly expressed and/or highly enriched in Acyrthosiphon pisum bacteriocyte tissues. When expressed in Xenopus laevis oocytes, two bacteriocyte amino acid transporters displayed significant levels of glutamine uptake, with transporter ACYPI001018, LOC100159667 (named here as Acyrthosiphon pisum glutamine transporter 1, ApGLNT1) functioning as the most active glutamine transporter. Transporter ApGLNT1 has narrow substrate selectivity, with high glutamine and low arginine transport capacity. Notably, ApGLNT1 has high binding affinity for arginine, and arginine acts as a competitive inhibitor for glutamine transport. Using immunocytochemistry, we show that ApGLNT1 is localized predominantly to the bacteriocyte plasma membrane, a location consistent with the transport of glutamine from A. pisum hemolymph to the bacteriocyte cytoplasm. On the basis of functional transport data and localization, we propose a substrate feedback inhibition model in which the accumulation of the essential amino acid arginine in A. pisum hemolymph reduces the transport of the precursor glutamine into bacteriocytes, thereby regulating amino acid biosynthesis in the bacteriocyte. Structural similarities in the arrangement of hosts and symbionts across endosymbiotic systems suggest that substrate feedback inhibition may be mechanistically important in other endosymbioses.

show abstract

Section: Discussionmentioning

confidence: 99%

Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts

Price

Feng

Baker

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

108

158

View full text Add to dashboard Cite

show abstract

“…In particular, the branched-chain amino acid import system (liv [for leucine-isoleucine-valine]) was required for establishing blood-stage infection in both screens. It is interesting in this context that other Rhizobiales drop biosynthesis of these particular amino acids during growth in bacteroids and then completely depend on their supply from the host plant ("symbiotic auxotrophy") (342,343). However, one enzyme of the branched-chain amino acid synthesis pathway was also essential for virulence in B. birtlesii (427), indicating that not only import but also biosynthesis of these amino acids is necessary at one point of the infection.…”

Section: Other Virulence Factorsmentioning

confidence: 99%

Intruders below the Radar: Molecular Pathogenesis of Bartonella spp

2012

View full text Add to dashboard Cite

SUMMARY Bartonella spp. are facultative intracellular pathogens that employ a unique stealth infection strategy comprising immune evasion and modulation, intimate interaction with nucleated cells, and intraerythrocytic persistence. Infections with Bartonella are ubiquitous among mammals, and many species can infect humans either as their natural host or incidentally as zoonotic pathogens. Upon inoculation into a naive host, the bartonellae first colonize a primary niche that is widely accepted to involve the manipulation of nucleated host cells, e.g., in the microvasculature. Consistently, in vitro research showed that Bartonella harbors an ample arsenal of virulence factors to modulate the response of such cells, gain entrance, and establish an intracellular niche. Subsequently, the bacteria are seeded into the bloodstream where they invade erythrocytes and give rise to a typically asymptomatic intraerythrocytic bacteremia. While this course of infection is characteristic for natural hosts, zoonotic infections or the infection of immunocompromised patients may alter the path of Bartonella and result in considerable morbidity. In this review we compile current knowledge on the molecular processes underlying both the infection strategy and pathogenesis of Bartonella and discuss their connection to the clinical presentation of human patients, which ranges from minor complaints to life-threatening disease.

show abstract

“…In contrast, aap/bra double mutants of S. meliloti did not significantly affect nitrogen fixation in alfalfa, another example of an indeterminate nodule host, even though amino acid transport levels were reduced to background levels (Prell et al 2010). The exact reason for this difference between the two genera of indeterminate-nodulating rhizobia is not known, but it may reflect the highly coordinated interaction between host plants and their respective symbionts.…”

Section: Amino Acid Cyclingmentioning

confidence: 90%

“…viciae and other indeterminate nodule bacteroids appear to depend on their host for branched-chain amino acid biosynthesis because they are terminally differentiated (see next section). To test whether or not this state of symbiotic auxotrophy is applicable to rhizobia that establish symbioses with determinate-nodule forming legumes, Prell et al (2010) constructed aap/bra double mutants of R. leguminosarum bv. phaseoli, which nodulates Phaseolus vulgaris.…”

Section: Amino Acid Cyclingmentioning

confidence: 99%

Molecular Signals and Receptors: Communication Between Nitrogen-Fixing Bacteria and Their Plant Hosts

Hirsch

Fujishige

2011

Biocommunication of Plants

View full text Add to dashboard Cite

Our understanding of the extent of communication taking place between the plant and its underground microbiome (rhizosphere microbes) as well as with other soil organisms has grown exponentially in the last decade. Much of this information has been obtained from studies of nitrogen-fixing organisms, particularly members of the family Rhizobiaceae (Alphaproteobacteria) that establish nodules on legume roots in which atmospheric nitrogen is converted to plant-utilizable forms. Signals exchanged among organisms in the rhizosphere via quorum sensing (QS) and the responses to these signals have been identified, but it is unclear how they influence the downstream stages of nodulation and nitrogen fixation. An exchange of signal molecules ensures that a high level of specificity takes place to optimize the nitrogenfixing interaction between host legume and symbiont. Chitin-related molecules appear to be the microbial currency for communication between the symbiotic partners in both mutualistic and pathogenic interactions. Exceptions to the paradigms based on the legume-Rhizobium interaction, including the discovery of Betaproteobacteria (now called beta-rhizobia) that nodulate and fix nitrogen with legumes and the lack of nodulation (nod) genes in certain alpha-rhizobia, particularly those that nodulate Aeschynomene and Arachis, bring into question the universality of some of the previous models. Moreover, new frontiers have opened that examine the coordination of information exchange that is needed for the induction and maintenance of nitrogen fixation and for bacteroid differentiation. Nevertheless, nitrogen-fixing organisms are just one small part of a highly interactive rhizosphere community. The challenge of the

show abstract

Role of Symbiotic Auxotrophy in the Rhizobium-Legume Symbioses

Cited by 57 publications

References 37 publications

Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts

Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts

Intruders below the Radar: Molecular Pathogenesis of Bartonella spp

Molecular Signals and Receptors: Communication Between Nitrogen-Fixing Bacteria and Their Plant Hosts

Contact Info

Product

Resources

About