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Biological and Molecular Characterization of a Jumbo Bacteriophage Infecting Plant Pathogenic Ralstonia solanacearum Species Complex Strains.

ABSTRACT: A jumbo phage infecting Ralstonia solanacearum species complex strains, designated RsoM2USA, was isolated from soil of a tomato field in Florida, United States, and belongs to the family Myoviridae. The phage has a long latent period of 270 min and completed its infection cycle in 360 min with a burst size of approximately 32 particles per cell. With a genome size of 343,806 bp, phage RsoM2USA is the largest Ralstonia-infecting phage sequenced and reported to date. Out of the 486 ORFs annotated for RsoM2USA, only 80 could be assigned putative functions in replication, transcription, translation including 44 tRNAs, and structure with the main structural proteins experimentally confirmed. Phylogenetic analyses placed RsoM2USA in the same clade as Xanthomonas phage XacN1, prompting a proposal of a new genus for the two jumbo phages. Jumbo phage RsoM2USA is a lytic phage and has a wide host range, infecting each of the three newly established Ralstonia species: R. solanacearum, R. pseudosolanacearum, and R. syzygii, and significantly reduced the virulence of its susceptible R. solanacearum strain RUN302 in tomato plants, suggesting that this jumbo phage has the potential to be developed into an effective control against diseases caused by R. solanacearum species complex strains.

SUBMITTER: Ahmad AA

PROVIDER: S-EPMC8504454 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:All the strains grouped under the species Ralstonia solanacearum represent a species complex responsible for many diseases on agricultural crops throughout the world. The strains have different lifestyles and host range. Here, we investigated whether specific metabolic pathways contribute to strain diversification. To this end, we carried out systematic comparisons on 11 strains representing the diversity of the species complex. We reconstructed the metabolic network of each strain from its genome sequence and looked for the metabolic pathways differentiating the different reconstructed networks and, by extension, the different strains. Finally, we conducted an experimental validation by determining the metabolic profile of each strain with the Biolog technology. Results revealed that the metabolism is conserved between strains, with a core metabolism composed of 82% of the pan-reactome. The three species composing the species complex could be distinguished according to the presence/absence of some metabolic pathways, in particular, one involving salicylic acid degradation. Phenotypic assays revealed that the trophic preferences on organic acids and several amino acids such as glutamine, glutamate, aspartate, and asparagine are conserved between strains. Finally, we generated mutants lacking the quorum-sensing-dependent regulator PhcA in four diverse strains, and we showed that the phcA-dependent trade-off between growth and production of virulence factors is conserved across the R. solanacearum species complex. IMPORTANCE Ralstonia solanacearum is one of the most important threats to plant health worldwide, causing disease on a very large range of agricultural crops such as tomato or potato. Behind the R. solanacearum name are hundreds of strains with different host range and lifestyle, classified into three species. Studying the differences between strains allows to better apprehend the biology of the pathogens and the specificity of some strains. None of the published genomic comparative studies have focused on the metabolism of the strains so far. We developed a new bioinformatic pipeline to build high-quality metabolic networks and used a combination of metabolic modeling and high-throughput phenotypic Biolog microplates to look for the metabolic differences between 11 strains across the three species. Our study revealed that genes encoding enzymes are overall conserved, with few variations between strains. However, more variations were observed when considering substrate usage. These variations probably result from regulation rather than the presence or absence of enzymes in the genome.

Project description:Following a request from the European Commission, the EFSA Panel on Plant Health performed a pest categorisation of the Ralstonia solanacearum species complex (RSSC), a distinguishable cosmopolitan group of bacterial plant pathogens (including R. solanacearum, Ralstonia pseudosolanacearum and two subspecies of Ralstonia syzygii) of the family Burkholderiaceae. The RSSC causes bacterial wilt in solanaceous crops, such as potato, tomato and pepper, but can also cause wilts in other important food crops such as fruit banana, plantain banana and cassava. The pest survives in the soil, and a number of weed species can also be infected by the pest, often asymptomatically. The RSSC is regulated in Council Directive 2000/29/EC (Annex IAII) (indicated by its former name R. solanacearum, as delimited by Yabuuchi et al.) as a harmful organism whose introduction into the EU is banned. In addition, Council Directive 1998/57/EC (amended by Commission Directive 2006/63/CE) concerns the measures to be taken within EU Member States (MS) against the RSSC to (a) detect it and determine its distribution, (b) prevent its occurrence and spread, and (c) control it with the aim of eradication. The pest is present in several EU MS, but in all cases with a restricted distribution and under official control. New phylotypes of the RSSC could enter the EU primarily via host plants for planting (including seed tubers). The pest could establish in the EU, as climatic conditions are favourable, hosts are common and the pathogen has high adaptability. Spread is mainly via plants for planting. Substantial crop losses in the EU would occur in the presence of RSSC epidemics. The RSSC is regarded as one of the world's most important phytopathogenic bacteria due to its broad geographical distribution, large host range, aggressiveness, genetic diversity and long persistence in soil and water. The list of hosts and commodities for which the pest is regulated is incomplete due to the high diversity of hosts and the lack of knowledge of the complete host range. Moreover, the comparative epidemiology of the different pathogen species has not yet been studied. The criteria assessed by the Panel for consideration of the RSSC as potential quarantine pest are met, while, for regulated non-quarantine pests, the criterion on the widespread presence in the EU is not met.

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Biological and Molecular Characterization of a Jumbo Bacteriophage Infecting Plant Pathogenic Ralstonia solanacearum Species Complex Strains.

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