Antibacterial synergy between a phage endolysin and citric acid against the Gram-negative kiwifruit pathogen Pseudomonas syringae pv. actinidiae

Horticultural diseases caused by bacterial pathogens provide an obstacle to crop production globally. Management of the infection of kiwifruit by the Gram-negative phytopathogen pv. ( ) currently includes copper and antibiotics. However, the emergence of bacterial resistance and a changing regulator...

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Published in:Applied and environmental microbiology 2024-03, Vol.90 (3), p.e0184623
Main Authors: Sisson, Hazel M, Fagerlund, Robert D, Jackson, Simon A, Briers, Yves, Warring, Suzanne L, Fineran, Peter C
Format: Article
Language:English
Subjects:
Acidification
Acids
Actinidia
Actinidia - microbiology
Anti-Bacterial Agents - pharmacology
Antibiotics
Antiinfectives and antibacterials
Antimicrobial agents
Bacteria
Bacteriophages
Cations
Citric acid
Copper
Crop production
Destabilization
Divalent cations
Electron microscopy
Endopeptidases
Enzymology and Protein Engineering
Gram-negative bacteria
Kiwifruit
Lipopolysaccharides
Lysis
Membranes
Offspring
Pathogens
Peptidoglycan
Peptidoglycans
Phages
Plant Diseases - microbiology
Plant Diseases - prevention & control
Progeny
Pseudomonas
Pseudomonas syringae
Scanning electron microscopy
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Summary:Horticultural diseases caused by bacterial pathogens provide an obstacle to crop production globally. Management of the infection of kiwifruit by the Gram-negative phytopathogen pv. ( ) currently includes copper and antibiotics. However, the emergence of bacterial resistance and a changing regulatory landscape are providing the impetus to develop environmentally sustainable antimicrobials. One potential strategy is the use of bacteriophage endolysins, which degrade peptidoglycan during normal phage replication, causing cell lysis and the release of new viral progeny. Exogenous use of endolysins as antimicrobials is impaired by the outer membrane of Gram-negative bacteria that provides an impermeable barrier and prevents endolysins from accessing their target peptidoglycan. Here, we describe the synergy between citric acid and a phage endolysin, which results in a reduction of viable below detection. We show that citric acid drives the destabilization of the outer membrane via acidification and sequestration of divalent cations from the lipopolysaccharide, which is followed by the degradation of the peptidoglycan by the endolysin. Scanning electron microscopy revealed clear morphological differences, indicating cell lysis following the endolysin-citric acid treatment. These results show the potential for citric acid-endolysin combinations as a possible antimicrobial approach in agricultural applications. The phytopathogen pv. ( ) causes major impacts to kiwifruit horticulture, and the current control strategies are heavily reliant on copper and antibiotics. The environmental impact and increasing resistance to these agrichemicals are driving interest in alternative antimicrobials including bacteriophage-derived therapies. In this study, we characterize the endolysin from the which infects . When combined with citric acid, this endolysin displays an impressive antibacterial synergy to reduce viable below the limit of detection. The use of citric acid as a synergistic agent with endolysins has not been extensively studied and has never been evaluated against a plant pathogen. We determined that the synergy involved a combination of the chelation activity of citric acid, acidic pH, and the specific activity of the ΦPsa374 endolysin. Our study highlights an exciting opportunity for alternative antimicrobials in agriculture.
ISSN:0099-2240
1098-5336
1098-5336
DOI:10.1128/aem.01846-23