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The complete genome sequence of Dickeya zeae EC1 reveals substantial divergence from other Dickeya strains and species.

ABSTRACT: Dickeya zeae is a bacterial species that infects monocotyledons and dicotyledons. Two antibiotic-like phytotoxins named zeamine and zeamine II were reported to play an important role in rice seed germination, and two genes associated with zeamines production, i.e., zmsA and zmsK, have been thoroughly characterized. However, other virulence factors and its molecular mechanisms of host specificity and pathogenesis are hardly known.The complete genome of D. zeae strain EC1 isolated from diseased rice plants was sequenced, annotated, and compared with the genomes of other Dickeya spp.. The pathogen contains a chromosome of 4,532,364 bp with 4,154 predicted protein-coding genes. Comparative genomics analysis indicates that D. zeae EC1 is most co-linear with D. chrysanthemi Ech1591, most conserved with D. zeae Ech586 and least similar to D. paradisiaca Ech703. Substantial genomic rearrangement was revealed by comparing EC1 with Ech586 and Ech703. Most virulence genes were well-conserved in Dickeya strains except Ech703. Significantly, the zms gene cluster involved in biosynthesis of zeamines, which were shown previously as key virulence determinants, is present in D. zeae strains isolated from rice, and some D. solani strains, but absent in other Dickeya species and the D. zeae strains isolated from other plants or sources. In addition, a DNA fragment containing 9 genes associated with fatty acid biosynthesis was found inserted in the fli gene cluster encoding flagellar biosynthesis of strain EC1 and other two rice isolates but not in other strains. This gene cluster shares a high protein similarity to the fatty acid genes from Pantoea ananatis.Our findings delineate the genetic background of D. zeae EC1, which infects both dicotyledons and monocotyledons, and suggest that D. zeae strains isolated from rice could be grouped into a distinct pathovar, i.e., D. zeae subsp. oryzae. In addition, the results of this study also unveiled that the zms gene cluster presented in the genomes of D. zeae rice isolates and D. solani strains, and the fatty acid genes inserted in the fli gene cluster of strain EC1 were likely derived from horizontal gene transfer during later stage of bacterial evolution.

SUBMITTER: Zhou J

PROVIDER: S-EPMC4522980 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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The complete genome sequence of Dickeya zeae EC1 reveals substantial divergence from other Dickeya strains and species.

Zhou Jianuan J Cheng Yingying Y Lv Mingfa M Liao Lisheng L Chen Yufan Y Gu Yanfang Y Liu Shiyin S Jiang Zide Z Xiong Yuanyan Y Zhang Lianhui L

BMC genomics 20150804

<h4>Background</h4>Dickeya zeae is a bacterial species that infects monocotyledons and dicotyledons. Two antibiotic-like phytotoxins named zeamine and zeamine II were reported to play an important role in rice seed germination, and two genes associated with zeamines production, i.e., zmsA and zmsK, have been thoroughly characterized. However, other virulence factors and its molecular mechanisms of host specificity and pathogenesis are hardly known.<h4>Results</h4>The complete genome of D. zeae s ...[more]

PMID: 26239726

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Project description:Dickeya zeae is an important and aggressive bacterial phytopathogen that can cause substantial economic losses in banana and rice plantations. We previously showed that c-di-GMP signaling proteins (cyclases/phosphodiesterases) in D. zeae strain EC1 play a significant role in the bacterial sessile-to-motile transition. To determine whether there is any synergistic effect among these c-di-GMP signaling proteins, we prepared a series of mutant strains by generating consecutive in-frame deletions of the genes encoding diguanylate cyclases (which make c-di-GMP) and phosphodiesterases (which break down c-di-GMP), respectively, using EC1 as a parental strain. The results showed that the complete deletion of all the putative diguanylate cyclases resulted in significantly increased bacterial motility and abrogated biofilm formation but did not appear to affect pathogenicity and virulence factor production. In contrast, the deletion of all the c-di-GMP phosphodiesterase genes disabled motility and prevented the invasion of EC1 into rice seeds. By measuring the c-di-GMP concentrations and swimming motility of all the mutants, we propose that c-di-GMP controlled swimming behavior through a multitiered program in a c-di-GMP concentration-dependent manner, which could be described as an L-shaped regression curve. These features are quite different from those that have been shown for other bacterial species such as Salmonella and Caulobacter crescentus Further analysis identified three c-di-GMP signaling proteins, i.e., PDE10355, DGC14945, and PDE14950, that play dominant roles in influencing the global c-di-GMP pool of strain EC1. The findings from this study highlight the complexity and plasticity of c-di-GMP regulatory circuits in different bacterial species.IMPORTANCEDickeya zeae is the etiological agent of bacterial foot rot disease, which can cause massive economic losses in banana and rice plantations. Genome sequence analysis showed that D. zeae strain EC1 contains multiple c-di-GMP turnover genes, but their roles and regulatory mechanisms in bacterial physiology and virulence remain vague. By generating consecutive in-frame deletion mutants of the genes encoding c-di-GMP biosynthesis and degradation, respectively, we analyzed the individual and collective impacts of these c-di-GMP metabolic genes on the c-di-GMP global pool, bacterial physiology, and virulence. The significance of our study is in identifying the mechanism of c-di-GMP signaling in strain EC1 more clearly, which expands the c-di-GMP regulating patterns in Gram-negative species. The methods and experimental designs in this research will provide a valuable reference for the exploration of the complex c-di-GMP regulation mechanisms in other bacteria.

Project description:Rice foot rot caused by Dickeya zeae is an important bacterial disease of rice worldwide. In this study, we identified a new strain EC2 from rice in Guangdong province, China. This strain differed from the previously identified strain from rice in its biochemical characteristics, pathogenicity, and genomic constituents. To explore genomic discrepancies between EC2 and previously identified strains from rice, a complete genome sequence of EC2 was obtained and used for comparative genomic analyses. The complete genome sequence of EC2 is 4,575,125 bp in length. EC2 was phylogenetically closest to previously identified Dickeya strains from rice, but not within their subgroup. In terms of secretion systems, genomic comparisons revealed that EC2 harbored only type I (T1SS), typeⅡ (T2SS), and type VI (T6SS) secretion systems. The flagella cluster of this strain possessed specific genomic characteristics like other D. zeae strains from Guangdong and from rice; within this locus, the genetic diversity among strains from rice was much lower than that of within strains from non-rice hosts. Unlike other strains from rice, EC2 lost the zeamine cluster, but retained the clustered regularly interspaced short palindromic repeats-1 (CRISPR-1) array. Compared to the other D. zeae strains containing both exopolysaccharide (EPS) and capsular polysaccharide (CPS) clusters, EC2 harbored only the CPS cluster, while the other strains from rice carried only the EPS cluster. Furthermore, we found strain MS1 from banana, carrying both EPS and CPS clusters, produced significantly more EPS than the strains from rice, and exhibited different biofilm-associated phenotypes. Comparative genomics analyses suggest EC2 likely evolved through a pathway different from the other D. zeae strains from rice, producing a new type of rice foot rot pathogen. These findings emphasize the emergence of a new type of D. zeae strain causing rice foot rot, an essential step in the early prevention of this rice bacterial disease.

Project description:Quorum quenching (QQ) is a novel, promising strategy that opens up a new perspective for controlling quorum-sensing (QS)-mediated bacterial pathogens. QQ is performed by interfering with population-sensing systems, such as by the inhibition of signal synthesis, catalysis of degrading enzymes, and modification of signals. In many Gram-negative pathogenic bacteria, a class of chemically conserved signaling molecules named N-acyl homoserine lactones (AHLs) have been widely studied. AHLs are involved in the modulation of virulence factors in various bacterial pathogens including Dickeya zeae. Dickeya zeae is the causal agent of plant-rot disease of bananas, rice, maize, potatoes, etc., causing enormous economic losses of crops. In this study, a highly efficient AHL-degrading bacterial strain W-7 was isolated from activated-sludge samples and identified as Pseudomonas nitroreducens. Strain W-7 revealed a superior ability to degrade N-(3-oxododecanoyl)-l-homoserine lactone (OdDHL) and completely degraded 0.2 mmol/L of OdDHL within 48 h. Gas chromatography-mass spectrometry (GC-MS) identified N-cyclohexyl-propanamide as the main intermediate metabolite during AHL biodegradation. A metabolic pathway for AHL in strain W-7 was proposed based on the chemical structure of AHL and intermediate products. In addition to the degradation of OdDHL, this strain was also found to be capable of degrading a wide range of AHLs including N-(3-oxohexanoyl)-l-homoserine lactone (OHHL), N-(3-oxooctanoyl)-l-homoserine lactone (OOHL), and N-hexanoyl-l-homoserine lactone (HHL). Moreover, the application of strain W-7 as a biocontrol agent could substantially attenuate the soft rot caused by D. zeae EC1 to suppress tissue maceration in various host plants. Similarly, the application of crude enzymes of strain W-7 significantly reduced the disease incidence and severity in host plants. These original findings unveil the biochemical aspects of a highly efficient AHL-degrading bacterial isolate and provide useful agents that exhibit great potential for the control of infectious diseases caused by AHL-dependent bacterial pathogens.

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The complete genome sequence of Dickeya zeae EC1 reveals substantial divergence from other Dickeya strains and species.

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The complete genome sequence of Dickeya zeae EC1 reveals substantial divergence from other Dickeya strains and species.

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