Widespread distribution of prophages signaling the potential for adaptability and pathogenicity evolution of Ralstonia solanacearum species complex

Gonçalves, Osiel Silva; Souza, Flávia de Oliveira; Bruckner, Fernanda Prieto; Santana, Mateus Ferreira; Alfenas‐Zerbini, Poliane

doi:10.1016/j.ygeno.2021.02.011

Cited by 15 publications

(38 citation statements)

References 54 publications

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“…Here, we show that R. solanacearum prophages have broad geographical distributions, each being found in multiple continents, with continent-specificity only observed in two low abundance prophages. Whilst these findings contrast with analyses by Gonҫalves et al (41) which suggested that R. solanacearum prophages are continent-specific, this is likely due to previous studies relying on geographically unrepresentative publicly available genomes. For example, φRS551 and φRSA1 were previously thought to be exclusive to South America and Korea, respectively, yet we found that they were present in all six continents, with particularly high prevalence in Africa and Europe.…”

Section: Discussioncontrasting

confidence: 99%

“…While prophages are known to affect plant pathogen fitness by mediating host growth, competitiveness, and virulence (29)(30)(31)(32)(33)(34)(35)(36)(37)41,80), only very little is known about their diversity and distribution at the pangenome-level. In this study, we analysed the prophage content of the plant pathogenic R. solanacearum bacterium using a representative, global collection of new 192 draft genome assemblies.…”

Section: Discussionmentioning

confidence: 99%

“…The large diversity of the strains within the complex and the economic losses associated with the disease make RSSC a salient target for prophage pangenome analyses (34,53,54). While a recent study made a significant contribution on understanding RSSC prophages using publicly available R. solanacearum genomes (41), it had a sampling bias with low representation of strains originating from Africa and Europe, missing a subset of hosts which are cold-adapted (48). In our study, R. solanacearum prophages were investigated using a new representative collection of 192 R. solanacearum draft genome sequences.…”

Section: Introductionmentioning

confidence: 99%

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

Greenrod

Stoycheva

Elphinstone

et al. 2021

Preprint

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Ralstonia solanacearum is a destructive plant pathogenic bacterium and the causative agent of bacterial wilt disease, infecting over 200 plant species worldwide. In addition to chromosomal genes, its 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 R. solanacearum virulence, the global diversity, distribution, and wider functional gene content of R. solanacearum prophages is unknown. In this study, prophages were identified in a diverse collection of 192 R. solanacearum draft genome assemblies originating from six continents. Prophages were identified bioinformatically and their diversity investigated using genetic distance measures, gene content, GC, and total length. Prophage distribution was characterised using metadata on R. solanacearum geographic origin and lineage classification (phylotypes), and their functional gene content was assessed by identifying putative prophage-encoded auxiliary genes. In total, 343 intact prophages were identified, forming ten genetically distinct clusters. These included five prophage clusters belonging to the Inoviridae, Myoviridae, and Siphoviridae phage families, and five uncharacterised clusters, possibly representing novel, previously undescribed phages. The prophages had broad geographical distribution 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 a myriad of auxiliary genes involved in metabolism and virulence of both phage and bacteria. Our results show that while R. solanacearum prophages are highly diverse globally, they make lineage-specific contributions to the R. solanacearum accessory genome, which could result from shared coevolutionary history.

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Section: Discussioncontrasting

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Greenrod

Stoycheva

Elphinstone

et al. 2021

Preprint

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“…The copyright holder for this preprint this version posted November 9, 2021. ; https://doi.org/10.1101/2021.11.09.467789 doi: bioRxiv preprint publication reported that in the presence of CRISPR arrays, 27.9% of spacers from Ralstonia genomes targeted prophage elements (28). Overall, our study demonstrated the lack of CRISPR systems in Ralstonia from a low temperature environment, and further underpins that this genus might employ other strategies for defense against mobile genetic elements (43).…”

Section: Discussionmentioning

confidence: 61%

“…Here, we follow the hypothesis that Ralstonia spp. prophages, which are geographically widespread entities (28), as well as replicating and adsorbed bacteriophages (all types further referred to as "host-associated" phages) can be used to study dispersal across the Antarctic continent. Extracting prokaryotic genomes from low DNA samples including air or precipitation is challenging, as low input libraries (1 pg) can result in the absence of bins (26).…”

Section: Introductionmentioning

confidence: 99%

Host-associated phages disperse across the extraterrestrial analogue Antarctica

Rahlff

Bornemann

Lopatina

et al. 2021

Preprint

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Extreme Antarctic conditions provide one of the closest analogues of extraterrestrial environments. Since air and snow samples especially from polar regions yield DNA amounts in the lower picogram range, binning of prokaryotic genomes is challenging and renders studying the dispersal of biological entities across these environments difficult. Here, we hypothesized that dispersal of host-associated bacteriophages (adsorbed, replicating or prophages) across the Antarctic continent can be tracked via their genetic signatures and benefits our understanding of virus and host dispersal across long distances. Phage genome fragments (PGFs) reconstructed from surface snow metagenomes of three Antarctic stations were assigned to four host genomes, mainly Betaproteobacteria including Ralstonia spp. Betaproteobacteria of this genus have been found in Antarctic snow as well as on space-related equipment. We reconstructed the complete genome of a temperate phage with near-complete alignment to a prophage in the reference genome of Ralstonia pickettii 12D. PGFs from different stations were related to each other at the genus level and matched similar hosts. Metagenomic read mapping and nucleotide polymorphism analysis revealed a wide dispersal of highly identical PGFs, 13 of which appeared in seawater from the Western Antarctic Peninsula with up to 5538 km to the snow sampling stations. Our results suggest that host-associated phages, especially of Ralstonia sp. disperse over long distances despite harsh conditions of the Antarctic continent. Due to the additional identification of 14 phages associated with two R. pickettii draft genomes isolated from space equipment, we conclude implications for the spread of biological contaminants in extraterrestrial settings.ImportanceHost-associated phages of the bacterium Ralstonia identified in snow samples can be used to track microbial dispersal over thousands of kilometers across the Antarctic continent, which functions as an extraterrestrial analogue because of its harsh environmental conditions. Due to presence of this bacterial strain including genome-integrated prophages on space-related equipment, and the here demonstrated potential for dispersal of host-associated phages, our work has implications for Planetary Protection, a discipline in Astrobiology interested in preventing contamination of celestial bodies with alien biomolecules or forms of life.

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Genomic and Biological Characterization of Ralstonia solanacearum Inovirus Brazil 1, an Inovirus that Alters the Pathogenicity of the Phytopathogen Ralstonia pseudosolanacearum

et al. 2021

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Widespread distribution of prophages signaling the potential for adaptability and pathogenicity evolution of Ralstonia solanacearum species complex

Cited by 15 publications

References 54 publications

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

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

Host-associated phages disperse across the extraterrestrial analogue Antarctica

Genomic and Biological Characterization of Ralstonia solanacearum Inovirus Brazil 1, an Inovirus that Alters the Pathogenicity of the Phytopathogen Ralstonia pseudosolanacearum

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