Amoebae can promote the survival of <i>Francisella</i> species in the aquatic environment

Hennebique, Aurélie; Peyroux, Julien; Brunet, Camille D.; Martin, Amandine; Henry, Thomas; Knežević, Maša; Šantić, Marina; Boisset, Sandrine; Maurin, Max

doi:10.1080/22221751.2021.1885999

Cited by 12 publications

(14 citation statements)

References 29 publications

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“…Furthermore, using this isolate ( Fth A-271), we corroborate earlier findings showing that the culturability of Francisella over time in water is improved at lower (4°C) temperatures rather than at higher ones (RT, 22.5°C). Furthermore, using the amoeba Naegleria gruberi we here can confirm prior publications, demonstrating that Francisella is not able to multiply in amoebae ( Acanthamoeba castellanii , A. polyphaga , Vermamoeba vermiformis ) ( Buse et al, 2017 ; Hennebique et al, 2021 ). However, lower temperatures and the presence of amoeba increased the survival and the long-term culturability of the bacterium ( Abd et al, 2003 ; El-Etr et al, 2009 ; Duodu and Colquhoun, 2010 ; Verhoeven et al, 2010 ; Gilbert and Rose, 2012 ; Ozanic et al, 2016 ; Buse et al, 2017 ; Golovliov et al, 2021 ; Hennebique et al, 2021 ).…”

Section: Discussionsupporting

confidence: 88%

“…Furthermore, using the amoeba Naegleria gruberi we here can confirm prior publications, demonstrating that Francisella is not able to multiply in amoebae (Acanthamoeba castellanii, A. polyphaga, Vermamoeba vermiformis) (Buse et al, 2017;Hennebique et al, 2021). However, lower temperatures and the presence of amoeba increased the survival and the long-term culturability of the bacterium (Abd et al, 2003;El-Etr et al, 2009;Duodu and Colquhoun, 2010;Verhoeven et al, 2010;Gilbert and Rose, 2012;Ozanic et al, 2016;Buse et al, 2017;Golovliov et al, 2021;Hennebique et al, 2021). Therefore, we chose Fth A-271 WT strain to investigate its ability to form biofilms and to colonize and survive in a natural aquatic multispecies biofilm.…”

Section: Discussionsupporting

confidence: 88%

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Francisella tularensis subsp. holarctica wild-type is able to colonize natural aquatic ex vivo biofilms

Schaudinn

Rydzewski²,

Meister³

et al. 2023

Front. Microbiol.

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Biofilms are a matrix-associated lifestyle of microbial communities, often enabling survivability and persistence of such bacteria. The objective of this study was to investigate the survival of the wild-type strain A-271 of Francisella tularensis subsp. holarctica (Fth) in a natural aquatic ex vivo biofilm. To that purpose, we allowed Fth A-271 to produce its own biofilm on solid surfaces but also to colonize naturally formed biofilms from aquatic habitats, which were infected with Francisella in the laboratory. The survival rates of the bacteria in biofilms were compared to those of planktonic bacteria as a function of the employed culture condition. It could be shown by light- and electron microscopy that Fth is able to form a complex, matrix-associated biofilm. The biofilm form of Francisella showed longer cultivability on agar plates in natural water when compared to planktonic (free-living) bacteria. Be it as a part of the existing ex vivo biofilm or free-floating above as planktonic bacteria, more than 80% of Francisella were not only able to survive under these conditions for 28 days, but even managed to establish microcolonies and areas with their own exclusive biofilm architecture within the ex vivo biofilm. Here, we can demonstrate for the first time that a Francisella tularensis wild-type strain (Type B) is able to successfully colonize an aquatic multi-species ex vivo biofilm. It is worthwhile to speculate that Fth might become more persistent in the environment when it forms its own biofilm or integrates in an existing one. Multi-species biofilms have been shown to be more resistant against stress compared to single-species biofilms. This may have an important impact on the long-term survival of Francisella in aquatic habitats and infection cycles in nature.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionsupporting

confidence: 88%

Francisella tularensis subsp. holarctica wild-type is able to colonize natural aquatic ex vivo biofilms

Schaudinn

Rydzewski²,

Meister³

et al. 2023

Front. Microbiol.

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“…pneumophila, as well as numerous other bacteria, have shown the ability to enter and multiply in A. castellanii cells [16]. A recent study also showed that amoebae likely promote survival of some bacteria in aquatic environments [62]. After the life cycle in an amoeba, L. pneumophila becomes more resistant to destruction by pasteurization treatment compared to agar-grown bacteria.…”

Section: Discussionmentioning

confidence: 99%

Decreasing Pasteurization Treatment Efficiency against Amoeba-Grown Legionella pneumophila—Recognized Public Health Risk Factor

Knežević

Rončević

Lušić

et al. 2022

IJERPH

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Legionellae are gram-negative bacteria most commonly found in freshwater ecosystems and purpose-built water systems. In humans, the bacterium causes Legionnaires’ disease (LD) or a Pontiac fever. In this study, the different waters (drinking water, pool water, cooling towers) in which Legionella pneumophila has been isolated were studied to assess the possible risk of bacterial spreading in the population. The influence of physical and chemical parameters, and interactions with Acanthamoeba castellanii on L. pneumophila, were analyzed by Heterotrophic Plate Count, the Colony-forming units (CFU) methods, transmission electron microscopy (TEM), and Sequence-Based Typing (SBT) analysis. During the study period (2013–2019), a total of 1932 water samples were analyzed, with the average annual rate of Legionella-positive water samples of 8.9%, showing an increasing trend. The largest proportion of Legionella-positive samples was found in cooling towers and rehabilitation centers (33.9% and 33.3%, respectively). Among the isolates, L. pneumophila SGs 2–14 was the most commonly identified strain (76%). The survival of Legionella was enhanced in the samples with higher pH values, while higher electrical conductivity, nitrate, and free residual chlorine concentration significantly reduced the survival of Legionella. Our results show that growth in amoeba does not affect the allelic profile, phenotype, and morphology of the bacterium but environmental L. pneumophila becomes more resistant to pasteurization treatment.

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“…In our study, the DNA detection of the tularemia agent does not allow us to determine the detected bacteria’s infectivity. Several in vitro experimental studies have shown that F. tularensis can survive in water through interaction with amebae [ 30 , 31 , 32 , 33 ]. Acanthamoeba species were especially shown to promote Francisella sp.…”

Section: Discussionmentioning

confidence: 99%

Presence of Francisella tularensis subsp. holarctica DNA in the Aquatic Environment in France

et al. 2021

Self Cite

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In 2018, the incidence of tularemia increased twofold in the west of France, with many pneumonic forms, suggesting environmental sources of infection. We investigated the presence of Francisella tularensis subsp. holarctica and other Francisella species DNA in the natural aquatic environment of this geographic area. Two sampling campaigns, in July 2019 and January 2020, allowed the collection of 87 water samples. Using a combination of real-time PCR assays, we tested the presence of either Francisella sp., F. tularensis/F. novicida, and F. tularensis subsp. holarctica, the latter being the only tularemia agent in Europe. Among 57 water samples of the first campaign, 15 (26.3%) were positive for Francisella sp., nine (15.8%) for F. tularensis and/or F. novicida, and four (7.0%) for F. tularensis subsp. holarctica. Ratios were 25/30 (83.3%), 24/30 (80.0%), and 4/30 (13.3%) for the second campaign. Among the thirty sites sampled during the two campaigns, nine were positive both times for Francisella sp., seven for F. tularensis and/or F. novicida, and one for F. tularensis subsp. holarctica. Altogether, our study reveals a high prevalence of Francisella sp. DNA (including the tularemia agent) in the studied aquatic environment. This aquatic environment could therefore participate in the endemicity of tularemia in the west of France.

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Amoebae can promote the survival of Francisella species in the aquatic environment

Cited by 12 publications

References 29 publications

Francisella tularensis subsp. holarctica wild-type is able to colonize natural aquatic ex vivo biofilms

Francisella tularensis subsp. holarctica wild-type is able to colonize natural aquatic ex vivo biofilms

Decreasing Pasteurization Treatment Efficiency against Amoeba-Grown Legionella pneumophila—Recognized Public Health Risk Factor

Presence of Francisella tularensis subsp. holarctica DNA in the Aquatic Environment in France

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