Unravelling the importance of the eukaryotic and bacterial communities and their relationship with Legionella spp. ecology in cooling towers: a complex network

<jats:title>Abstract</jats:title><jats:sec> <jats:title>Background</jats:title> <jats:p>Cooling towers are a major source of large community-associated outbreaks of Legionnaires’ disease, a severe pneumonia. This disease is contracted when inhaling aerosols that are contaminated with bacteria from the genus <jats:italic>Legionella</jats:italic>, most importantly <jats:italic>Legionella pneumophila</jats:italic>. How cooling towers support the growth of this bacterium is still not well understood. As <jats:italic>Legionella</jats:italic> species are intracellular parasites of protozoa, it is assumed that protozoan community in cooling towers play an important role in <jats:italic>Legionella</jats:italic> ecology and outbreaks. However, the exact mechanism of how the eukaryotic community contributes to <jats:italic>Legionella</jats:italic> ecology is still unclear. Therefore, we used <jats:italic>18S rRNA</jats:italic> gene amplicon sequencing to characterize the eukaryotic communities of 18 different cooling towers. The data from the eukaryotic community was then analysed with the bacterial community of the same towers in order to understand how each community could affect <jats:italic>Legionella</jats:italic> spp. ecology in cooling towers.</jats:p> </jats:sec><jats:sec> <jats:title>Results</jats:title> <jats:p>We identified several microbial groups in the cooling tower ecosystem associated with <jats:italic>Legionella</jats:italic> spp<jats:italic>.</jats:italic> that suggest the presence of a microbial loop in these systems. Dissolved organic carbon was shown to be a major factor in shaping the eukaryotic community and may be an important factor for <jats:italic>Legionella</jats:italic> ecology. Network analysis, based on co-occurrence, revealed that <jats:italic>Legionella</jats:italic> was correlated with a number of different organisms. Out of these, the bacterial genus <jats:italic>Brevundimonas</jats:italic> and the ciliate class <jats:italic>Oligohymenophorea</jats:italic> were shown, through in vitro experiments, to stimulate the growth of <jats:italic>L</jats:italic>. <jats:italic>pneumophila</jats:italic> through direct and indirect mechanisms.</jats:p> </jats:sec><jats:sec> <jats:title>Conclusion</jats:title> <jats:p>Our results suggest that <jats:italic>Legionella</jats:italic> ecology depends on the host community, including ciliates and on several groups of organisms that contribute to its survival and growth in the cooling tower ecosystem. These findings further support the idea that some cooling tower microbiomes may promote the survival and growth of <jats:italic>Legionella</jats:italic> better than others.</jats:p> </jats:sec>