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The rice foot rot pathogen Dickeya zeae alters the in-field plant microbiome.

ABSTRACT: Studies on bacterial plant diseases have thus far been focused on the single bacterial species causing the disease, with very little attention given to the many other microorganisms present in the microbiome. This study intends to use pathobiome analysis of the rice foot rot disease, caused by Dickeya zeae, as a case study to investigate the effects of this bacterial pathogen to the total resident microbiome and to highlight possible interactions between the pathogen and the members of the community involved in the disease process. The microbiome of asymptomatic and the pathobiome of foot-rot symptomatic field-grown rice plants over two growing periods and belonging to two rice cultivars were determined via 16S rRNA gene amplicon sequencing. Results showed that the presence of D. zeae is associated with an alteration of the resident bacterial community in terms of species composition, abundance and richness, leading to the formation of microbial consortia linked to the disease state. Several bacterial species were significantly co-presented with the pathogen in the two growing periods suggesting that they could be involved in the disease process. Besides, culture-dependent isolation and in planta inoculation studies of a bacterial member of the pathobiome, identified as positive correlated with the pathogen in our in silico analysis, indicated that it benefits from the presence of D. zeae. A similar microbiome/pathobiome experiment was also performed in a symptomatically different rice disease evidencing that not all plant diseases have the same consequence/relationship with the plant microbiome. This study moves away from a pathogen-focused stance and goes towards a more ecological perception considering the effect of the entire microbial community which could be involved in the pathogenesis, persistence, transmission and evolution of plant pathogens.

SUBMITTER: Bez C

PROVIDER: S-EPMC9292192 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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: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.

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The rice foot rot pathogen Dickeya zeae alters the in-field plant microbiome.

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