Biocontrol of bacterial wilt in tomato with a cocktail of lytic bacteriophages

Magar, Roniya Thapa; Kim, Hyo Jeong; Lee, Seon-Woo

doi:10.1007/s00253-022-11962-7

Cited by 11 publications

(5 citation statements)

References 45 publications

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“…While the phage densities were reduced by 51% in single phage cocktail application treatments (down to 4 × 10³ PFU g −1 soil), phage densities remained constantly high when applied repeatedly for three times (four orders of magnitude higher densities: 2.5 × 10⁷ PFU g − ¹ soil). The survival and persistence of phages in soils have previously been demonstrated to show notable declines to densities lower than 10⁶ PFU g⁻¹ soil ( 12 , 65 , 66 ). It is thus likely that repeated phage application frequency improved the efficacy of phage biocontrol by increasing phage densities and phage-bacteria encounter rates in the rhizosphere.…”

Section: Discussionmentioning

confidence: 99%

Phages enhance both phytopathogen density control and rhizosphere microbiome suppressiveness

Wang,

Huang

et al. 2024

mBio

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Bacteriophages, viruses that specifically target plant pathogenic bacteria, have emerged as a promising alternative to traditional agrochemicals. However, it remains unclear how phages should be applied to achieve efficient pathogen biocontrol and to what extent their efficacy is shaped by indirect interactions with the resident microbiota. Here, we tested if the phage biocontrol efficacy of Ralstonia solanacearum phytopathogenic bacterium can be improved by increasing the phage cocktail application frequency and if the phage efficacy is affected by pathogen-suppressing bacteria already present in the rhizosphere. We find that increasing phage application frequency improves R. solanacearum density control, leading to a clear reduction in bacterial wilt disease in both greenhouse and field experiments with tomato. The high phage application frequency also increased the diversity of resident rhizosphere microbiota and enriched several bacterial taxa that were associated with the reduction in pathogen densities. Interestingly, these taxa often belonged to Actinobacteria known for antibiotics production and soil suppressiveness. To test if they could have had secondary effects on R. solanacearum biocontrol, we isolated Actinobacteria from Nocardia and Streptomyces genera and tested their suppressiveness to the pathogen in vitro and in planta . We found that these taxa could clearly inhibit R. solanacearum growth and constrain bacterial wilt disease, especially when combined with the phage cocktail. Together, our findings unravel an undiscovered benefit of phage therapy, where phages trigger a second line of defense by the pathogen-suppressing bacteria that already exist in resident microbial communities. IMPORTANCE Ralstonia solanacearum is a highly destructive plant-pathogenic bacterium with the ability to cause bacterial wilt in several crucial crop plants. Given the limitations of conventional chemical control methods, the use of bacterial viruses (phages) has been explored as an alternative biological control strategy. In this study, we show that increasing the phage application frequency can improve the density control of R. solanacearum , leading to a significant reduction in bacterial wilt disease. Furthermore, we found that repeated phage application increased the diversity of rhizosphere microbiota and specifically enriched Actinobacterial taxa that showed synergistic pathogen suppression when combined with phages due to resource and interference competition. Together, our study unravels an undiscovered benefit of phages, where phages trigger a second line of defense by the pathogen-suppressing bacteria present in resident microbial communities. Phage therapies could, hence, potentially be tailored according to host microbiota composition to unlock the pre-existing benefits provided by resident microbiota.

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Section: Discussionmentioning

confidence: 99%

Phages enhance both phytopathogen density control and rhizosphere microbiome suppressiveness

Wang,

Huang

et al. 2024

mBio

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“…Across the diversity of RSSC-infective phages, most do not transport aux clusters (96,(98)(99)(100). Nevertheless, with growing interest in employing phages for control of bacterial plant pathogens (99,(101)(102)(103)(104)(105), it will remain important to evaluate candidate biocontrol agents for their ability to improve the ecological fitness of the pathogens.…”

Section: Discussionmentioning

confidence: 99%

A pangenomic atlas reveals that eco-evolutionary dynamics shape plant pathogen type VI secretion systems

Aoun,

Georgoulis,

Avalos

et al. 2023

Preprint

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Soil-borne Ralstonia solanacearum species complex (RSSC) bacteria disrupt rhizosphere and endophytic microbial communities as they invade roots and fatally wilt plants. RSSC pathogens secrete antimicrobial toxins using a type VI secretion system (T6SS). To investigate how evolution and ecology have shaped pathogen T6SS biology, we analyzed the T6SS gene content and architecture across the RSSC pangenome and their evolutionarily relatives. Our analysis reveals that two ecologically similar Burkholderiaceae taxa, xylem pathogenic RSSC bacteria and Acidovorax, have convergently evolved to wield large arsenals of T6SS toxins. To understand the mechanisms underlying genomic enrichment of T6SS toxins, we compiled an atlas of 1,069 auxiliary ("aux") T6SS toxin clusters across 99 high-quality RSSC genomes. We classified 25 types of aux clusters with toxins that predominantly target lipids, nucleic acids, or unknown cellular substrates. The aux clusters were in diverse genetic neighborhoods and had complex phylogenetic distributions, suggesting frequent horizontal gene flow. Phages and other mobile genetic elements account for most of the aux cluster acquisition on the chromosome but very little on the megaplasmid. Nevertheless, RSSC genomes were more enriched in aux clusters on the megaplasmid. Secondary replicons like megaplasmids often evolve more rapidly than the more evolutionarily stable chromosome. Although the single ancestral T6SS was broadly conserved in the RSSC, the T6SS was convergently lost in atypical lineages with vectored transmission. Overall, our data suggest dynamic interplay between the lifestyle of soil-transmitted RSSC lineages and the evolution of T6SSs with robust arsenals of toxins. This pangenomic atlas poises the RSSC as an emerging, tractable model to understand the role of the T6SS in shaping pathogen populations.

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“…As a result, there is a growing interest in utilizing phage-derived proteins, such as endolysins, for pathogen biocontrol (O’Flaherty et al 2009 ). Researchers have identified several techniques to enhance the efficacy of phage biocontrol, including optimizing the timing, frequency, and dosage of application (Iriarte et al 2007 , Cui et al 2019 , Li et al 2020 ), employing phages as multiphage cocktails (Alvarez et al 2019 , Wang et al 2019 , Rabiey et al 2020 , Thapa Magar et al 2022 ) or rationally combining phages with antibiotics (Torres-Barcelo and Hochberg 2016 , Torres-Barcelo et al 2016 ) or probiotics (Wang et al 2017 ). Several products have been developed and already made commercially available, including AgriPhage ™ and Erwiphage ™ (Grace et al 2021 ).…”

Section: Introductionmentioning

confidence: 99%

The role of rhizosphere phages in soil health

Wang,

Tang,

Yue

et al. 2024

FEMS Microbiology Ecology

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While the One Health framework has emphasized the importance of soil microbiomes for plant and human health, one of the most diverse and abundant groups—bacterial viruses, i.e. phages—has been mostly neglected. This perspective reviews the significance of phages for plant health in rhizosphere and explores their ecological and evolutionary impacts on soil ecosystems. We first summarize our current understanding of the diversity and ecological roles of phages in soil microbiomes in terms of nutrient cycling, top-down density regulation and pathogen suppression. We then consider how phages drive bacterial evolution in soils by promoting horizontal gene transfer, encoding auxiliary metabolic genes that increase host bacterial fitness and selecting for phage-resistant mutants with altered ecology due to trade-offs with pathogen competitiveness and virulence. Finally, we consider challenges and avenues for phage research in soil ecosystems and how to elucidate the significance of phages for microbial ecology and evolution and soil ecosystem functioning in the future. We conclude that similar to bacteria, phages likely play important roles in connecting different One Health compartments, affecting microbiome diversity and functions in soils. From the applied perspective, phages could offer novel approaches to modulate and optimize microbial and microbe-plant interactions to enhance soil health.

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Biocontrol of bacterial wilt in tomato with a cocktail of lytic bacteriophages

Cited by 11 publications

References 45 publications

Phages enhance both phytopathogen density control and rhizosphere microbiome suppressiveness

Phages enhance both phytopathogen density control and rhizosphere microbiome suppressiveness

A pangenomic atlas reveals that eco-evolutionary dynamics shape plant pathogen type VI secretion systems

The role of rhizosphere phages in soil health

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