Dataset Information

Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex.

ABSTRACT:

Background

Ralstonia solanacearum species complex (RSSC) strains are destructive plant pathogenic bacteria and the causative agents of bacterial wilt disease, infecting over 200 plant species worldwide. In addition to chromosomal genes, their virulence is mediated by mobile genetic elements including integrated DNA of bacteriophages, i.e., prophages, which may carry fitness-associated auxiliary genes or modulate host gene expression. Although experimental studies have characterised several prophages that shape RSSC virulence, the global diversity, distribution, and wider functional gene content of RSSC prophages are unknown. In this study, prophages were identified in a diverse collection of 192 RSSC draft genome assemblies originating from six continents.

Results

Prophages were identified bioinformatically and their diversity investigated using genetic distance measures, gene content, GC, and total length. Prophage distributions were characterised using metadata on RSSC strain geographic origin and lineage classification (phylotypes), and their functional gene content was assessed by identifying putative prophage-encoded auxiliary genes. In total, 313 intact prophages were identified, forming ten genetically distinct clusters. These included six prophage clusters with similarity to the Inoviridae, Myoviridae, and Siphoviridae phage families, and four uncharacterised clusters, possibly representing novel, previously undescribed phages. The prophages had broad geographical distributions, being present across multiple continents. However, they were generally host phylogenetic lineage-specific, and overall, prophage diversity was proportional to the genetic diversity of their hosts. The prophages contained many auxiliary genes involved in metabolism and virulence of both phage and bacteria.

Conclusions

Our results show that while RSSC prophages are highly diverse globally, they make lineage-specific contributions to the RSSC accessory genome, which could have resulted from shared coevolutionary history.

SUBMITTER: Greenrod STE

PROVIDER: S-EPMC9535894 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Publications

Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex.

Greenrod Samuel T E STE Stoycheva Martina M Elphinstone John J Friman Ville-Petri VP

BMC genomics 20221006 1

<h4>Background</h4>Ralstonia solanacearum species complex (RSSC) strains are destructive plant pathogenic bacteria and the causative agents of bacterial wilt disease, infecting over 200 plant species worldwide. In addition to chromosomal genes, their virulence is mediated by mobile genetic elements including integrated DNA of bacteriophages, i.e., prophages, which may carry fitness-associated auxiliary genes or modulate host gene expression. Although experimental studies have characterised sever ...[more]

PMID: 36199029

Similar Datasets

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.

Project description:BACKGROUND: The Ralstonia solanacearum species complex includes thousands of strains pathogenic to an unusually wide range of plant species. These globally dispersed and heterogeneous strains cause bacterial wilt diseases, which have major socio-economic impacts. Pathogenicity is an ancestral trait in R. solanacearum and strains with high genetic variation can be subdivided into four phylotypes, correlating to isolates from Asia (phylotype I), the Americas (phylotype IIA and IIB), Africa (phylotype III) and Indonesia (phylotype IV). Comparison of genome sequences strains representative of this phylogenetic diversity can help determine which traits allow this bacterium to be such a pathogen of so many different plant species and how the bacteria survive in many different habitats. RESULTS: The genomes of three tomato bacterial wilt pathogens, CFBP2957 (phy. IIA), CMR15 (phy. III) and PSI07 (phy. IV) were sequenced and manually annotated. These genomes were compared with those of three previously sequenced R. solanacearum strains: GMI1000 (tomato, phy. I), IPO1609 (potato, phy. IIB), and Molk2 (banana, phy. IIB). The major genomic features (size, G+C content, number of genes) were conserved across all of the six sequenced strains. Despite relatively high genetic distances (calculated from average nucleotide identity) and many genomic rearrangements, more than 60% of the genes of the megaplasmid and 70% of those on the chromosome are syntenic. The three new genomic sequences revealed the presence of several previously unknown traits, probably acquired by horizontal transfers, within the genomes of R. solanacearum, including a type IV secretion system, a rhi-type anti-mitotic toxin and two small plasmids. Genes involved in virulence appear to be evolving at a faster rate than the genome as a whole. CONCLUSIONS: Comparative analysis of genome sequences and gene content confirmed the differentiation of R. solanacearum species complex strains into four phylotypes. Genetic distances between strains, in conjunction with CGH analysis of a larger set of strains, revealed differences great enough to consider reclassification of the R. solanacearum species complex into three species. The data are still too fragmentary to link genomic classification and phenotypes, but these new genome sequences identify a pan-genome more representative of the diversity in the R. solanancearum species complex.

Project description:Epidemiological surveillance of plant pathogens based on genotyping methods is mandatory to improve disease management strategies. In the Southwest Indian Ocean (SWIO) islands, bacterial wilt (BW) caused by the Ralstonia solanacearum species complex (RSSC) is hampering the production of many sustainable and cash crops. To thoroughly analyze the genetic diversity of the RSSC in the SWIO, we performed a wide sampling survey (in Comoros, Mauritius, Reunion, Rodrigues, and Seychelles) that yielded 1,704 isolates from 129 plots, mainly from solanaceous crops. Classification of the isolates to the four major RSSC phylogenetic groups, named phylotypes, showed that 87% were phylotype I, representing the most prevalent strain in each of the SWIO islands. Additionally, 9.7% were phylotype II, and 3.3% were phylotype III; however, these isolates were found only in Reunion. Phylotype IV (2 isolates), known to be restricted to Indonesia-Australia-Japan, was reported in Mauritius, representing the first report of this group in the SWIO. Partial endoglucanase (egl) sequencing, based on the selection of 145 isolates covering the geographic and host diversity in the SWIO (also including strains from Mayotte and Madagascar), revealed 14 sequevars with Reunion and Mauritius displaying the highest sequevar diversity. Through a multilocus sequence analysis (MLSA) scheme based on the partial sequencing of 6 housekeeping genes (gdhA, gyrB, rplB, leuS, adk, and mutS) and 1 virulence-associated gene (egl), we inferred the phylogenetic relationships between these 145 SWIO isolates and 90 worldwide RSSC reference strains. Phylotype I was the most recombinogenic, although recombination events were detected among all phylotypes. A multilocus sequence typing (MLST) scheme identified 29 sequence types (STs) with variable geographic distributions in the SWIO. The outstanding epidemiologic feature was STI-13 (sequevar I-31), which was overrepresented in the SWIO and obviously reflected a lineage strongly adapted to the SWIO environment. A goeBURST analysis identified eight clonal complexes (CCs) including SWIO isolates, four CCs being geographically restricted to the SWIO, and four CCs being widespread beyond the SWIO. This work, which highlights notable genetic links between African and SWIO strains, provides a basis for the epidemiological surveillance of RSSC and will contribute to BW management in the SWIO.

Dataset Information

Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex.

Background

Results

Conclusions

Publications

Global diversity and distribution of prophages are lineage-specific within the Ralstonia solanacearum species complex.

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