Extracellular DNases of Ralstonia solanacearum modulate biofilms and facilitate bacterial wilt virulence

Tuan Minh Tran, April Macintyre, Devanshi Khokhani, Martha Hawes, Caitilyn Allen

Research output: Contribution to journalArticlepeer-review

19 Scopus citations

Abstract

Ralstonia solanacearum is a soil-borne vascular pathogen that colonizes plant xylem vessels, a flowing, low-nutrient habitat where biofilms could be adaptive. Ralstonia solanacearum forms biofilm in vitro, but it was not known if the pathogen benefits from biofilms during infection. Scanning electron microscopy revealed that during tomato infection, R. solanacearum forms biofilm-like masses in xylem vessels. These aggregates contain bacteria embedded in a matrix including chromatin-like fibres commonly observed in other bacterial biofilms. Chemical and enzymatic assays demonstrated that the bacterium releases extracellular DNA in culture and that DNA is an integral component of the biofilm matrix. An R. solanacearum mutant lacking the pathogen’s two extracellular nucleases (exDNases) formed non-spreading colonies and abnormally thick biofilms in vitro. The biofilms formed by the exDNase mutant in planta contained more and thicker fibres. This mutant was also reduced in virulence on tomato plants and did not spread in tomato stems as well as the wild-type strain, suggesting that these exDNases facilitate biofilm maturation and bacterial dispersal. To our knowledge, this is the first demonstration that R. solanacearum forms biofilms in plant xylem vessels, and the first documentation that plant pathogens use DNases to modulate their biofilm structure for systemic spread and virulence.

Original languageEnglish (US)
Pages (from-to)4103-4117
Number of pages15
JournalEnvironmental microbiology
Volume18
Issue number11
DOIs
StatePublished - Nov 1 2016
Externally publishedYes

Bibliographical note

Funding Information:
This research was supported by grants from the Vietnam Education Foundation, the National Science Foundation and the University of Wisconsin-Madison College of Agricultural and Life Sciences. The authors gratefully acknowledge Sarah Swanson, Department of Botany, for technical advice on confocal microscopy. We also thank Beth Dalsing, Tiffany Lowe- Power, Heidi Goodrich-Blair, Patricia McManus and Jeri Barak for critical review of the manuscript.

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