VarR controls colonization and virulence in the marine macroalgal pathogen Nautella italica R11

Abstract

There is increasing evidence to suggest that macroalgae (seaweeds) are susceptible to infectious disease. However, to date, little is known about the mechanisms that facilitate the colonization and virulence of microbial seaweed pathogens. One well-described example of a seaweed disease is the bleaching of the red alga Delisea pulchra, which can be caused by the bacterium Nautella italica R11, a member of the Roseobacter clade. This pathogen contains a unique luxR-type gene, varR, which we hypothesize controls its colonization and virulence. We show here that a varR knock-out strain is deficient in its ability to cause disease in D. pulchra and is defective in biofilm formation and attachment to a common algal polysaccharide. Moreover complementation of the varR gene in trans can restore these functions to the wild type levels. Proteomic analysis of bacterial cells in planktonic and biofilm growth highlight the potential importance of nitrogen scavenging, mobilization of energy reserves, and stress resistance in the biofilm lifestyle of N. italica R11. Moreover, we show that VarR regulates the expression of a specific subset of biofilm-associated proteins. Taken together these data suggest that VarR controls colonization and persistence of N. italica R11 on the surface of a macroalgal host and that it is an important regulator of virulence.

Transcriptional response of Nautella italica R11 towards its macroalgal host uncovers new mechanisms of host–pathogen interaction

“…N. italica R11 has been identified as a causative agent of bleaching disease in D. pulchra, yet there is a paucity of knowledge regarding the gene regulation and molecular mechanisms that mediate this host–pathogen interaction. In N. italica R11, the LuxR homolog VarR was previously shown to control phenotypes involved in biofilm formation and virulence (Gardiner, Fernandes et al., ). Further proteomic analysis demonstrated that VarR positively controls a range of proteins for surface colonization and biofilm maturation, such as signal transduction mechanisms, and genes for nutrient acquisition and metabolism (Gardiner, Fernandes et al., ).…”

“…An N. italica R11 raiR allelic replacement mutant (∆ raiR ) strain and complement (C∆ raiR ) strain were constructed using the Splicing by Overlap Extension PCR (SOE‐PCR) strategy coupled with biparental conjugation following the method of Gardiner, Fernandes et al. (). Briefly, a single homologous recombination event between the SOE‐PCR fragment and the genome of N. italica R11 generated the chloramphenicol‐resistant mutant strain, Δ raiR .…”

“…An infection assay of laboratory‐cultured D. pulchra was performed as described by Gardiner, Fernandes et al. () and Case et al. ().…”

“…One of the best studied models for disease in macroalgae is the mid‐thallus bleaching of the red macroalga, Delisea pulchra (Campbell, Harder, Nielsen, Kjelleberg, & Steinberg, ; Case et al., ; Fernandes et al., ; Gardiner, Fernandes et al., ; Gardiner, Thomas, & Egan, ; Harder, Campbell, Egan, & Steinberg, ). Bleaching disease in D. pulchra leads to reduced photosynthetic efficiency, decreased fecundity and a greater susceptibility to fouling and grazing pressures (Campbell, Vergés, & Steinberg, ).…”

“…Recent studies have demonstrated a role for the solo VarR transcriptional regulator in the control of a range of biofilm‐associated phenotypes that allow N . italica R11 to colonize and persist on the algal surface (Gardiner, Fernandes et al., ). However, to date, the role of the other N .…”