Molecular Determinants of a Symbiotic Chronic Infection

Gibson, Katherine E.; Kobayashi, Hajime; Walker, Graham C.

doi:10.1146/annurev.genet.42.110807.091427

Cited by 325 publications

(282 citation statements)

References 191 publications

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“…Within the nodule cells, RNB differentiate into bacteroids, which reduce atmospheric nitrogen (N 2 ) to ammonia (Oldroyd and Downie 2008;Udvardi and Poole 2013). Rhizobial infection and nodule organogenesis require a coordinated exchange of molecular signals between the host and its symbiotic bacteria (Gibson et al 2008;Perret et al 2000).…”

Section: Introductionmentioning

confidence: 99%

Ribosomal protein biomarkers provide root nodule bacterial identification by MALDI-TOF MS

Ziegler

Pothier

Ardley

et al. 2015

Appl Microbiol Biotechnol

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Accurate identification of soil bacteria that form nitrogen-fixing associations with legume crops is challenging given the phylogenetic diversity of root nodule bacteria (RNB). The labor-intensive and time-consuming 16S ribosomal RNA (rRNA) sequencing and/or multilocus sequence analysis (MLSA) of conserved genes so far remain the favored molecular tools to characterize symbiotic bacteria. With the development of mass spectrometry (MS) as an alternative method to rapidly identify bacterial isolates, we recently showed that matrix-assisted laser desorption ionization (MALDI) time-of-flight (TOF) can accurately characterize RNB found inside plant nodules or grown in cultures. Here, we report on the development of a MALDI-TOF RNB-specific spectral database built on whole cell MS fingerprints of 116 strains representing the major rhizobial genera. In addition to this RNB-specific module, which was successfully tested on unknown field isolates, a subset of 13 ribosomal proteins extracted from genome data was found to be sufficient for the reliable identification of nodule isolates to rhizobial species as shown in the putatively ascribed ribosomal protein masses (PARPM) database. These results reveal that data gathered from genome sequences can be used to expand spectral libraries to aid the accurate identification of bacterial species by MALDI-TOF MS.

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Section: Introductionmentioning

confidence: 99%

Ribosomal protein biomarkers provide root nodule bacterial identification by MALDI-TOF MS

Ziegler

Pothier

Ardley

et al. 2015

Appl Microbiol Biotechnol

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“…Rhizobia elicit on legume roots -occasionally stems-the formation of specialized organs called nodules in which they fix nitrogen to the benefit of the plant. In most present symbioses rhizobia massively infect nodule cells forming intracellular structures called symbiosomes (Gibson et al, 2008;Ivanov et al, 2010), although infection processes regarded as more primitive are also encountered (Sprent, 2001). Intracellular accommodation of rhizobia was an evolutionary quantum leap in the rhizobiumlegume symbiosis as it boosted metabolic exchanges between the two partners while shielding internalized bacteria, called bacteroids, from plant defense reactions.…”

Section: Introductionmentioning

confidence: 99%

Experimental evolution of nodule intracellular infection in legume symbionts

et al. 2013

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Soil bacteria known as rhizobia are able to establish an endosymbiosis with legumes that takes place in neoformed nodules in which intracellularly hosted bacteria fix nitrogen. Intracellular accommodation that facilitates nutrient exchange between the two partners and protects bacteria from plant defense reactions has been a major evolutionary step towards mutualism. Yet the forces that drove the selection of the late event of intracellular infection during rhizobium evolution are unknown. To address this question, we took advantage of the previous conversion of the plant pathogen Ralstonia solanacearum into a legume-nodulating bacterium that infected nodules only extracellularly. We experimentally evolved this draft rhizobium into intracellular endosymbionts using serial cycles of legume-bacterium cocultures. The three derived lineages rapidly gained intracellular infection capacity, revealing that the legume is a highly selective environment for the evolution of this trait. From genome resequencing, we identified in each lineage a mutation responsible for the extracellular-intracellular transition. All three mutations target virulence regulators, strongly suggesting that several virulence-associated functions interfere with intracellular infection. We provide evidence that the adaptive mutations were selected for their positive effect on nodulation. Moreover, we showed that inactivation of the type three secretion system of R. solanacearum that initially allowed the ancestral draft rhizobium to nodulate, was also required to permit intracellular infection, suggesting a similar checkpoint for bacterial invasion at the early nodulation/root infection and late nodule cell entry levels. We discuss our findings with respect to the spread and maintenance of intracellular infection in rhizobial lineages during evolutionary times.

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“…rhizobia-legume | host-microbe interactions I nterspecies signaling is critical throughout the process that establishes the symbiosis between Medicago plant species and the nitrogen-fixing bacterium Sinorhizobium meliloti (1). Secretion of flavonoid molecules by plant roots signals the presence of a potential host to S. meliloti.…”

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confidence: 99%

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

Penterman

Abo

Nisco

et al. 2014

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

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The α-proteobacterium Sinorhizobium meliloti establishes a chronic intracellular infection during the symbiosis with its legume hosts. Within specialized host cells, S. meliloti differentiates into highly polyploid, enlarged nitrogen-fixing bacteroids. This differentiation is driven by host cells through the production of defensin-like peptides called "nodule-specific cysteine-rich" (NCR) peptides. Recent research has shown that synthesized NCR peptides exhibit antimicrobial activity at high concentrations but cause bacterial endoreduplication at sublethal concentrations. We leveraged synchronized S. meliloti populations to determine how treatment with a sublethal NCR peptide affects the cell cycle and physiology of bacteria at the molecular level. We found that at sublethal levels a representative NCR peptide specifically blocks cell division and antagonizes Z-ring function. Gene-expression profiling revealed that the cell division block was produced, in part, through the substantial transcriptional response elicited by sublethal NCR treatment that affected ∼15% of the genome. Expression of critical cell-cycle regulators, including ctrA, and cell division genes, including genes required for Z-ring function, were greatly attenuated in NCR-treated cells. In addition, our experiments identified important symbiosis functions and stress responses that are induced by sublethal levels of NCR peptides and other antimicrobial peptides. Several of these stress-response pathways also are found in related α-proteobacterial pathogens and might be used by S. meliloti to sense host cues during infection. Our data suggest a model in which, in addition to provoking stress responses, NCR peptides target intracellular regulatory pathways to drive S. meliloti endoreduplication and differentiation during symbiosis.rhizobia-legume | host-microbe interactions

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Molecular Determinants of a Symbiotic Chronic Infection

Cited by 325 publications

References 191 publications

Ribosomal protein biomarkers provide root nodule bacterial identification by MALDI-TOF MS

Ribosomal protein biomarkers provide root nodule bacterial identification by MALDI-TOF MS

Experimental evolution of nodule intracellular infection in legume symbionts

Host plant peptides elicit a transcriptional response to control theSinorhizobium meliloticell cycle during symbiosis

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