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Comparative genomic analysis of two-component regulatory proteins in Pseudomonas syringae.

ABSTRACT: Pseudomonas syringae is a widespread bacterial plant pathogen, and strains of P. syringae may be assigned to different pathovars based on host specificity among different plant species. The genomes of P. syringae pv. syringae (Psy) B728a, pv. tomato (Pto) DC3000 and pv. phaseolicola (Pph) 1448A have been recently sequenced providing a major resource for comparative genomic analysis. A mechanism commonly found in bacteria for signal transduction is the two-component system (TCS), which typically consists of a sensor histidine kinase (HK) and a response regulator (RR). P. syringae requires a complex array of TCS proteins to cope with diverse plant hosts, host responses, and environmental conditions.Based on the genomic data, pattern searches with Hidden Markov Model (HMM) profiles have been used to identify putative HKs and RRs. The genomes of Psy B728a, Pto DC3000 and Pph 1448A were found to contain a large number of genes encoding TCS proteins, and a core of complete TCS proteins were shared between these genomes: 30 putative TCS clusters, 11 orphan HKs, 33 orphan RRs, and 16 hybrid HKs. A close analysis of the distribution of genes encoding TCS proteins revealed important differences in TCS proteins among the three P. syringae pathovars.In this article we present a thorough analysis of the identification and distribution of TCS proteins among the sequenced genomes of P. syringae. We have identified differences in TCS proteins among the three P. syringae pathovars that may contribute to their diverse host ranges and association with plant hosts. The identification and analysis of the repertoire of TCS proteins in the genomes of P. syringae pathovars constitute a basis for future functional genomic studies of the signal transduction pathways in this important bacterial phytopathogen.

SUBMITTER: Lavin JL

PROVIDER: S-EPMC2222644 | biostudies-literature | 2007 Oct

REPOSITORIES: biostudies-literature

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Comparative genomic analysis of two-component regulatory proteins in Pseudomonas syringae.

Lavín José L JL Kiil Kristoffer K Resano Ohiana O Ussery David W DW Oguiza José A JA

BMC genomics 20071031

<h4>Background</h4>Pseudomonas syringae is a widespread bacterial plant pathogen, and strains of P. syringae may be assigned to different pathovars based on host specificity among different plant species. The genomes of P. syringae pv. syringae (Psy) B728a, pv. tomato (Pto) DC3000 and pv. phaseolicola (Pph) 1448A have been recently sequenced providing a major resource for comparative genomic analysis. A mechanism commonly found in bacteria for signal transduction is the two-component system (TCS ...[more]

PMID: 17971244

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Project description:CvsSR is a Ca2+-induced two-component system (TCS) in the plant pathogen Pseudomonas syringae pv. tomato DC3000. Here, we discovered that CvsSR is induced by Fe3+, Zn2+, and Cd2+ However, only supplementation of Ca2+ to medium resulted in rugose, opaque colonies in ΔcvsS and ΔcvsR strains. This phenotype corresponded to formation of calcium phosphate precipitation on the surface of ΔcvsS and ΔcvsR colonies. CvsSR regulated swarming motility in P. syringae pv. tomato in a Ca2+-dependent manner, but swarming behavior was not influenced by Fe3+, Zn2+, or Cd2+ We hypothesized that reduced swarming displayed by ΔcvsS and ΔcvsR strains was due to precipitation of calcium phosphate on the surface of ΔcvsS and ΔcvsR cells grown on agar medium supplemented with Ca2+ By reducing the initial pH or adding glucose to the medium, calcium precipitation was inhibited, and swarming was restored to ΔcvsS and ΔcvsR strains, suggesting that calcium precipitation influences swarming ability. Constitutive expression of a CvsSR-regulated carbonic anhydrase and a CvsSR-regulated putative sulfate major facilitator superfamily transporter in ΔcvsS and ΔcvsR strains inhibited formation of calcium precipitates and restored the ability of ΔcvsS and ΔcvsR bacteria to swarm. Lastly, we found that glucose inhibited Ca2+-based induction of CvsSR. Hence, CvsSR is a key regulator that controls calcium precipitation on the surface of bacterial cells.IMPORTANCE Bacteria are capable of precipitating and dissolving minerals. We previously reported the characterization of the two-component system CvsSR in the plant-pathogenic bacterium Pseudomonas syringae CvsSR responds to the presence of calcium and is important for causing disease. Here, we show that CvsSR controls the ability of the bacterium to prevent calcium phosphate precipitation on the surface of cells. We also identified a carbonic anhydrase and transporter that modulate formation of surface-associated calcium precipitates. Furthermore, our results demonstrate that the ability of the bacterium to swarm is controlled by the formation and dissolution of calcium precipitates on the surface of cells. Our study describes new mechanisms for microbially induced mineralization and provides insights into the role of mineral deposits on bacterial physiology. The discoveries may lead to new technological and environmental applications.

Project description:The pPT23A family of plasmids appears to be indigenous to the plant pathogen Pseudomonas syringae and these plasmids are widely distributed and widely transferred among pathovars of P. syringae and related species. pPT23A-family plasmids (PFPs) are sources of accessory genes for their hosts that can include genes important for virulence and epiphytic colonization of plant leaf surfaces. The occurrence of repeated sequences including duplicated insertion sequences on PFPs has made obtaining closed plasmid genome sequences difficult. Therefore, our objective was to obtain complete genome sequences from PFPs from divergent P. syringae pathovars and also from strains of P. syringae pv. syringae isolated from different hosts.The eight plasmids sequenced ranged in length from 61.6 to 73.8 kb and encoded from 65 to 83 annotated orfs. Virulence genes including type III secretion system effectors were encoded on two plasmids, and one of these, pPt0893-29 from P. syringae pv. tabaci, encoded a wide variety of putative virulence determinants. The PFPs from P. syringae pv. syringae mostly encoded genes of importance to ecological fitness including the rulAB determinant conferring tolerance to ultraviolet radiation. Heavy metal resistance genes encoding resistance to copper and arsenic were also present in a few plasmids. The discovery of part of the chromosomal genomic island GI6 from P. syringae pv. syringae B728a in two PFPs from two P. syringae pv. syringae hosts is further evidence of past intergenetic transfers between plasmid and chromosomal DNA. Phylogenetic analyses also revealed new subgroups of the pPT23A plasmid family and confirmed that plasmid phylogeny is incongruent with P. syringae pathovar or host of isolation. In addition, conserved genes among seven sequenced plasmids within the same phylogenetic group were limited to plasmid-specific functions including maintenance and transfer functions.Our sequence analysis further revealed that PFPs from P. syringae encode suites of accessory genes that are selected at species (universal distribution), pathovar (interpathovar distribution), and population levels (intrapathovar distribution). The conservation of type IV secretion systems encoding conjugation functions also presumably contributes to the distribution of these plasmids within P. syringae populations.

Project description:BackgroundPseudomonas syringae is an important plant pathogen, which could adapt many different environmental conditions. Under the nutrient-limited and other stress conditions, P. syringae produces nucleotide signal molecules, i.e., guanosine tetra/pentaphosphate ((p)ppGpp), to globally regulate gene expression. Previous studies showed that (p) ppGpp played an important role in regulating virulence factors in P. syringae pv. tomato DC3000 (PstDC3000) and P. syringae pv. syringae B728a (PssB728a). Here we present a comparative transcriptomic analysis to uncover the overall effects of (p)ppGpp-mediated stringent response in P. syringae.ResultsIn this study, we investigated global gene expression profiles of PstDC3000 and PssB728a and their corresponding (p)ppGpp0 mutants in hrp-inducing minimal medium (HMM) using RNA-seq. A total of 1886 and 1562 differentially expressed genes (DEGs) were uncovered between the (p)ppGpp0 mutants and the wild-type in PstDC3000 and PssB728a, respectively. Comparative transcriptomics identified 1613 common DEGs, as well as 444 and 293 unique DEGs in PstDC3000 and PssB728a, respectively. Functional cluster analysis revealed that (p) ppGpp positively regulated a variety of virulence-associated genes, including type III secretion system (T3SS), type VI secretion system (T6SS), cell motility, cell division, and alginate biosynthesis, while negatively regulated multiple basic physiological processes, including DNA replication, RNA processes, nucleotide biosynthesis, fatty acid metabolism, ribosome protein biosynthesis, and amino acid metabolism in both PstDC3000 and PssB728a. Furthermore, (p) ppGpp had divergent effects on other processes in PstDC3000 and PssB728a, including phytotoxin, nitrogen regulation and general secretion pathway (GSP).ConclusionIn this study, comparative transcriptomic analysis reveals common regulatory networks in both PstDC3000 and PssB728a mediated by (p) ppGpp in HMM. In both P. syringae systems, (p) ppGpp re-allocate cellular resources by suppressing multiple basic physiological activities and enhancing virulence gene expression, suggesting a balance between growth, survival and virulence. Our research is important in that due to similar global gene expression mediated by (p) ppGpp in both PstDC3000 and PssB728a, it is reasonable to propose that (p) ppGpp could be used as a target to develop novel control measures to fight against important plant bacterial diseases.

Dataset Information

Comparative genomic analysis of two-component regulatory proteins in Pseudomonas syringae.

Publications

Comparative genomic analysis of two-component regulatory proteins in Pseudomonas syringae.

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