Pyomelanin produced by Vibrio cholerae confers resistance to predation by Acanthamoeba castellanii

Abstract

Protozoan predation is one of the main environmental factors constraining bacterial growth in aquatic environments, and thus has led to the evolution of a number of defence mechanisms that protect bacteria from predation. These mechanisms may also function as virulence factors in infection of animal and human hosts. Whole transcriptome shotgun sequencing of Vibrio cholerae biofilms during predation by the amoebae, Acanthamoeba castellanii, revealed that 131 transcripts were significantly differentially regulated when compared to the non-grazed control. Differentially regulated transcripts included those involved in biosynthetic and metabolic pathways. The transcripts of genes involved in tyrosine metabolism were down-regulated in the grazed population, which indicates that the tyrosine metabolic regulon may have a role in the response of V. cholerae biofilms to A. castellanii predation. Homogentisate 1, 2-dioxygenase (HGA) is the main intermediate of the normal L-tyrosine catabolic pathway which is known to auto-oxidize, leading to the formation of the pigment, pyomelanin. Indeed, a pigmented mutant, disrupted in hmgA, was more resistant to amoebae predation than the wild type. Increased grazing resistance was correlated with increased production of pyomelanin and thus reactive oxygen species (ROS), suggesting that ROS production is a defensive mechanism used by bacterial biofilms against predation by amoebae A. castellanii.

Dual Role of Mechanisms Involved in Resistance to Predation by Protozoa and Virulence to Humans

“…For example, production of pyomelanin plays a role in virulence factor expression and colonization by V. cholerae ( Valeru et al, 2009 ). Pyomelanin production in V. cholerae biofilm also leads to increased ROS levels, which promotes resistance to predation by A. castellanii ( Noorian et al, 2017 ).…”

Density-dependent resistance protects Legionella pneumophila from its own antimicrobial metabolite, HGA

“…Phenazine inhibitory activity is typically thought to come from redox cycling and the production of reactive oxygen species, including H 2 O 2 (Hassan and Fridovich, 1980; Cheluvappa et al, 2008). Oddly, HGA-melanin production has previously been implicated both in the production of (Noorian et al, 2017) and protection from (Keith et al, 2007; Orlandi et al, 2015) reactive oxygen species. The catalase experiments presented here have ruled out the production of extracellular H 2 O 2 as a possible mechanism behind HGA inhibition (Figure 3—figure supplement 1B–C).…”

Brought to you courtesy of the red, white, and blue–pigments of nontuberculous mycobacteria

“…To protect against oxidative stress, melanin from Burkholderia cenocepacia neutralizes reactive oxygen species (ROS) generated by the oxidative burst in host cells [20] . Melanin from V. cholerae increases ROS production, toxin and pilus expression, as well as enhances host colonization and protection from amoeba predation [4] , [21] . During chronic infections, Pseudomonas aeruginosa increases melanin production to resist oxidative stress [14] .…”