Environmental Free-Living Amoebae Can Predate on Diverse Antibiotic-Resistant Human Pathogens

Abstract

We here sought to test the resistance of human pathogens to unaltered environmental free-living amoebae. Amoebae are ubiquitous eukaryotic microorganisms and important predators of bacteria. Environmental amoebae have also been proposed to serve both as potential reservoir and training ground for human pathogens. However, studies addressing their relationship with human pathogens often rely on a few domesticated amoebae selected to feed on rich medium, thereby possibly overestimating the resistance of pathogens to these predatory phagocytes. From an open-air composting site, we recovered over a hundred diverse amoebae able to feed on Acinetobacter baumannii and Klebsiella pneumoniae . In a standardized and quantitative assay for predation, the isolated amoebae showed a broad predation spectrum, killing clinical isolates of A. baumannii , K. pneumoniae , Pseudomonas aeruginosa and Staphylococcus aureus . Interestingly, A. baumannii , previously reported to resist predation by laboratory strains of Acanthamoeba , is efficiently consumed by closely related environmental amoebae. The isolated amoebae are capable of feeding on highly virulent carbapenem-resistant or methicillin-resistant clinical isolates. In conclusion, the natural environment is a rich source of amoebae with broad-spectrum bactericidal activities, including against antibiotic resistant isolates. Importance Free-living amoebae have been proposed to play in important role in hosting and disseminating various human pathogens. The resistance of human pathogens to predation by amoebae is often derived from in vitro experiments using model amoebae. We here sought to isolate environmental amoebae and test their predation on diverse human pathogens, with results that challenge conclusions based on model amoebae. We found that the natural environment is a rich source of diverse amoebae with broad-spectrum predatory activities against human pathogens, including highly virulent and antibiotic resistant clinical isolates.

Grazing preferences of three species of amoebae on cyanobacteria and green algae

“…Vermamoeba is much smaller than Cochliopodium or Vannella , and while it is clear that Vermamoeba is able to ingest filamentous cyanobacteria (Figures 1E and 7E,F), we were unable to observe the mechanism. Vermamoeba vermiformis grazes on bacteria (Bornier et al., 2021) and will phagocytize fungal conidia (Maisonneuve et al., 2016). However, the data in Table 1 are likely the first demonstration that this widespread species can successfully graze on both unicellular and filamentous cyanobacteria.…”

On the ecology ofAcinetobacter baumannii– jet stream rider and opportunist by nature

“…Alternatively, there might be (micro-)habitats where they are permanently established and from where they spread again at opportunity. Soil-dwelling amoebae should be considered potential hosts (12, 114). Since colonization rates of earthworms were found lower than those of ambient soil we do not consider earthworms as original reservoir although they might contribute to spread.…”

Phagotrophic protists preserve antibiotic-resistant opportunistic human pathogens in the vegetable phyllosphere

“…The significant positive association between phyllosphere phagotrophic protists (both the diversity and the relative abundance) and the abundance of the Top 4 HPMGs, and the highest explanation of the phagotrophic protists on the abundance of K. pneumoniae phoE and P. aeruginosa regA both indicated a strong connection between phyllosphere phagotrophic protists and OHPs. This strong connection can be partially explained by the selective predation of phagotrophic protists on various human pathogens, including K. pneumoniae , Pseudomonas aeruginosa , and Staphylococcus aureus [ 15 ]. Phagotrophic protists can also influence the colonization of OHPs via regulating nutrient exchange [ 88 ] or pathogen-suppressing secondary metabolite genes [ 89 ].…”

“…[ 13 , 14 ]. More than 100 diverse environmental amoebae were reported to reduce the number of OHPs such as Acinetobacter baumannii , Klebsiella pneumoniae, Pseudomonas aeruginosa , and Staphylococcus aureus [ 15 , 16 ] by phagocytosis, killing OHPs intracellularly with toxic materials such as copper and arsenic [ 17 ]. In response to predation stress, specific pathogens evolve virulence (e.g., Shiga toxin and Violacein) [ 18 – 21 ] or mental resistance (e.g., copper resistance) [ 22 ] to resist digestion or internal shuttling to the contractile vacuole to replicate before being exocytosed to the environment [ 23 ].…”