Genomic Analysis Unveils the Pervasiveness and Diversity of Prophages Infecting Erwinia Species

Morgan, Túlio; Rezende, Rafael Reis de; Lima, Thamylles Thuany Mayrink; Souza, Flávia de Oliveira; Alfenas‐Zerbini, Poliane

doi:10.3390/pathogens12010044

Cited by 4 publications

(2 citation statements)

References 60 publications

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“…We find that there were, on average, 4 prophage-like elements encoded per genome across the 590 isolates of P. syringae, demonstrating the abundance of prophage-like elements in the genomes of these isolates (Figure 5). This average number is comparable to other phytopathogenic bacteria such as Erwinia amylovora, which also carries a panel of 4 prophage-like elements per genome (36). We further observed that the average number of prophage-like elements, phage defenses and effectors encoded within both the genome and the mobilome differs across the phylogroups.…”

Section: Discussionsupporting

confidence: 68%

“…For other plant-associated bacteria specifically, this number has been shown to be as high as 10 mechanisms for some Ralstonia and Xanthomonas isolates (34). In sharp contrast to other bacterial species (35,36), and even other Pseudomonads, CRISPR-Cas does not appear to be an important phage defense strategy in the P. syringae species complex (37,38). Instead, we demonstrated that P. syringae relies on other defense mechanisms, such as restriction enzymes and abortive infection strategies, to cope with phage predation.…”

Section: Discussionmentioning

confidence: 99%

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Evidence for the key roles of thePseudomonas syringaemobilome in shaping biotic interactions

Holtappels,

Rickus,

Morgan

et al. 2024

Preprint

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The mobilome, defined as the collection of mobile genetic elements within a bacterial genome, plays a critical role in the adaptation of bacteria to abiotic and biotic drivers. In particular, prophages have been reported to contribute to bacterial resistance to virulent bacteriophages, the competitive interaction of bacterial hosts within microbial communities, and in pathogenicity and virulence. It is therefore critical to better understand the role of prophages in distributing genes and functions within and among bacterial species to predict how bacteria adapt to their biotic environment.Pseudomonas syringaeoffers an ideal study system to ask these questions both because of its broad range of lifestyles (spanning from environmental growth to plant pathogens) and its high intraspecies diversity. To examine the role of the mobilome in this species complex, we compared 590 genomes available from public databases and annotated the defense mechanisms, effectors, and prophages in the genomes. We found that this species complex has an elaborate phage pandefensome consisting of 139 defense mechanisms. Host-associatedP. syringaeisolates were found to have both elaborate phage defensomes and effectoromes. Assessing taxonomical signatures of the observed prophages uncovered broad differences in the types and numbers of genes encoded by different phage families, emphasizing how the evolutionary advantages conferred to hosts will depend on the prophage composition and offering insight to how these genes might disperse within a community. Our study highlights the intimate association of phage families with their hosts and uncovers their key role in shaping ecology for this widespread species complex.Significance statementThe bacterial accessory genome, including the mobilome and prophages, plays a critical role in shaping bacterial adaptation to abiotic and biotic drivers. These prophages are widespread across bacterial taxa and likely maintained because of their evolutionary advantage. Our ability to predict how a bacterial population will evolve over time requires a better understanding of where key functional traits arrive. To address this question, we assessed prophage-encoded phage defenses and effector acrossPseudomonas syringae. We show that prophages carrying these genes belong to specific phage taxa with differences in the types of genes encoded. This emphasizes the evolutionary advantage of these prophages, offering a framework to uncover how these genes disperse within microbial communities and their role in pathogen evolution.

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Section: Discussionsupporting

confidence: 68%

Section: Discussionmentioning

confidence: 99%

Evidence for the key roles of thePseudomonas syringaemobilome in shaping biotic interactions

Holtappels,

Rickus,

Morgan

et al. 2024

Preprint

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Prediction and characterization of prophages of Stenotrophomonas maltophilia reveals a remarkable phylogenetic diversity of prophages

Fang,

Xu,

Shen

et al. 2023

Sci Rep

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Prophages, which enables bacterial hosts to acquire novel traits, and increase genetic variation and evolutionary innovation, are considered to be one of the greatest drivers of bacterial diversity and evolution. Stenotrophomonas maltophilia is widely distributed and one of the most important multidrug resistant bacteria in hospitals. However, the distribution and genetic diversity of S. maltophilia prophages have not been elucidated. In this study, putative prophages were predicted in S. maltophilia genomes by using virus prediction tools, and the genetic diversity and phylogeny of S. maltophilia and the prophages they harbor were further analyzed. A total of 356 prophage regions were predicted from 88 S. maltophilia genomes. Among them, 144 were intact prophages, but 77.09% of the intact prophages did not match any known phage sequences in the public database. The number of prophage carried by S. maltophilia is related to its host habitat and is an important factor affecting the size of the host genome, but it is not related to the genetic diversity of the prophage. The prediction of auxiliary genes encoded by prophage showed that antibiotic resistance genes was not predicted for any of the prophages except for one questionable prophage, while 53 virulence genes and 169 carbohydrate active enzymes were predicted from 11.24 and 44.1% prophages, respectively. Most of the prophages (72.29%) mediated horizontal gene transfer of S. maltophilia genome, but only involved in 6.25% of the horizontal gene transfer events. In addition, CRISPR prediction indicated 97.75% S. maltophilia strains contained the CRISPR-Cas system containing 818 spacer sequences. However, these spacer sequences did not match any known S. maltophilia phages, and only a few S. maltophilia prophages. Comparative genomic analysis revealed a highly conserved and syntenic organization with genomic rearrangement between the prophages and the known related S. maltophilia phages. Our results indicate a high prevalence and genetic diversity of prophages in the genome of S. maltophilia, as well as the presence of a large number of uncharacterized phages. It provides an important complement to understanding the diversity and biological characteristics of phages, as well as the interactions and evolution between bacteria and phages.

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Pangenomics to understand prophage dynamics in thePectobacteriumgenus and the radiating lineages ofP. Brasiliense

Pardeshi,

van Duivenbode,

Pel

et al. 2024

Preprint

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Bacterial pathogens of the genus Pectobacterium are responsible for soft rot and blackleg disease in a wide range of crops and have a global impact on food production. The emergence of new lineages and their competitive succession is frequently observed in Pectobacterium species, in particular in P. brasiliense. With a focus on one such recently emerged P. brasiliense lineage in the Netherlands that causes blackleg in potatoes, we studied genome evolution in this genus using a reference-free graph-based pangenome approach. We clustered 1,977,865 proteins from 454 Pectobacterium spp. genomes into 30,156 homology groups. The Pectobacterium genus pangenome is open and its growth is mainly contributed by the accessory genome. Bacteriophage genes were enriched in the accessory genome and contributed 16% of the pangenome. Blackleg-causing P. brasiliense isolates had increased genome size with high levels of prophage integration. To study the diversity and dynamics of these prophages across the pangenome, we developed an approach to trace prophages across genomes using pangenome homology group signatures. We identified lineage-specific as well as generalist bacteriophages infecting Pectobacterium species. Our results capture the ongoing dynamics of mobile genetic elements, even in the clonal lineages. The observed lineage-specific prophage dynamics provide mechanistic insights into Pectobacterium pangenome growth and contribution to the radiating lineages of P. brasiliense.

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Genomic Analysis Unveils the Pervasiveness and Diversity of Prophages Infecting Erwinia Species

Cited by 4 publications

References 60 publications

Evidence for the key roles of thePseudomonas syringaemobilome in shaping biotic interactions

Evidence for the key roles of thePseudomonas syringaemobilome in shaping biotic interactions

Prediction and characterization of prophages of Stenotrophomonas maltophilia reveals a remarkable phylogenetic diversity of prophages

Pangenomics to understand prophage dynamics in thePectobacteriumgenus and the radiating lineages ofP. Brasiliense

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