Temperature-Dependent Growth Modeling of Environmental and Clinical Legionella pneumophila Multilocus Variable-Number Tandem-Repeat Analysis (MLVA) Genotypes

Abstract

Legionella pneumophila causes waterborne infections resulting in severe pneumonia. High-resolution genotyping of L. pneumophila isolates can be achieved by multiple-locus variable-number tandem-repeat analysis (MLVA). Recently, we found that different MLVA genotypes of L. pneumophila dominated different sites in a small drinking-water network, with a genotype-related temperature and abundance regime. The present study focuses on understanding the temperature-depen dent growth kinetics of the genotypes that dominated the water network. Our aim was to model mathematically the influence of temperature on the growth kinetics of different environmental and clinical L. pneumophila genotypes and to compare it with the influence of their ecological niches. Environmental strains showed a distinct temperature preference, with significant differences among the growth kinetics of the three studied genotypes (Gt4, Gt6, and Gt15). Gt4 strains exhibited superior growth at lower temperatures (25 and 30°C), while Gt15 strains appeared to be best adapted to relatively higher temperatures (42 and 45°C). The temperature-dependent growth traits of the environmental genotypes were consistent with their distribution and temperature preferences in the water network. Clinical isolates exhibited significantly higher growth rates and reached higher maximal cell densities at 37°C and 42°C than the environmental strains. Further research on the growth preferences of L. pneumophila clinical and environmental genotypes will result in a better understanding of their ecological niches in drinking-water systems as well as in the human body.IMPORTANCE Legionella pneumophila is a waterborne pathogen that threatens humans in developed countries. The bacteria inhabit natural and man-made freshwater environments. Here we demonstrate that different environmental L. pneumophila genotypes have different temperature-dependent growth kinetics. Moreover, Legionella strains that belong to the same species but were isolated from environmental and clinical sources possess adaptations for growth at different temperatures. These growth preferences may influence the bacterial colonization at specific ecological niches within the drinking-water network. Adaptations for growth at human body temperatures may facilitate the abilities of some L. pneumophila strains to infect and cause illness in humans. Our findings may be used as a tool to improve Legionella monitoring in drinking-water networks. Risk assessment models for predicting the risk of legionellosis should take into account not only Legionella concentrations but also the temperature-dependent growth kinetics of the isolates.

Occurrence of culturableLegionella pneumophilain drinking water distribution systems

“…can also survive at temperatures below 20°C and even below freezing (Borella, Guerrieri, Marchesi, Bondi, & Messi, ). Sharaby et al () reported that environmental strains of L. pneumophila exhibited a superior capability for growth at lower temperatures (25 and 30°C) than did clinical strains. Moreover, as the virulence of L. pneumophila is temperature dependent, with maximum virulence between 37 and 42°C (Edelstein, Beer, & DeBoynton, ; Mauchline, James, Fitzgeorge, Dennis, & Keevil, ), the virulence of strains growing in drinking water systems needs to be evaluated.…”

Legionella Persistence in Manufactured Water Systems: Pasteurization Potentially Selecting for Thermal Tolerance

“…In contrast, at lower temperatures (25°C) the opposite was observed (Sharaby et al, 2017). The identified emergence of new disease-associate clones of L. pneumophila may, in part, be accelerated by selective pressures exerted by heat treatments for disinfection.…”

Virulence Traits of Environmental and Clinical Legionella pneumophila Multilocus Variable-Number Tandem-Repeat Analysis (MLVA) Genotypes

“…7 in reference 43). Recently, Sharaby et al (37) demonstrated that the distribution and temperature preferences of these environmental genotypes were consistent with their temperature-dependent growth traits. For clinical isolates, it was shown that they had significantly higher growth rates and reached higher maximal cell densities at 37°C and 42°C than the environmental strains (37).…”

“…Recently, Sharaby et al (37) demonstrated that the distribution and temperature preferences of these environmental genotypes were consistent with their temperature-dependent growth traits. For clinical isolates, it was shown that they had significantly higher growth rates and reached higher maximal cell densities at 37°C and 42°C than the environmental strains (37). These findings highlight the importance of studying and characterizing the physiological and virulence traits of different L. pneumophila genotypes in order to promote our understanding of the hazardous potential of pathogenic strains.…”

“…Since L. pneumophila reaches the human lungs via water aerosols, a thorough understanding of its ecology outside the human body and especially in drinking-water supply systems is important to enable design of efficient prevention measures (13,(37)(38)(39)(40). From an epidemiological point of view, genotyping is important for determining the sources and the transfer pathway of infections.…”