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Environmental Sequencing Fills the Gap Between Parasitic Haplosporidians and Free-living Giant Amoebae.

ABSTRACT: Class Ascetosporea (Rhizaria; Endomyxa) comprises many parasites of invertebrates. Within this group, recent group-specific environmental DNA (eDNA) studies have contributed to the establishment of the new order Mikrocytida, a new phylogeny and characterization of Paramyxida, and illuminated the diversity and distribution of haplosporidians. Here, we use general and lineage-specific PCR primers to investigate the phylogenetic "gap" between haplosporidians and their closest known free-living relatives, the testate amoeba Gromia and reticulate amoeba Filoreta. Within this gap are Paradinium spp. parasites of copepods, which we show to be highly diverse and widely distributed in planktonic and benthic samples. We reveal a robustly supported radiation of parasites, ENDO-3, comprised of Paradinium and three further clades (ENDO-3a, ENDO-3b and SPP). A further environmental group, ENDO-2, perhaps comprising several clades, branches between this radiation and the free-living amoebae. Early diverging haplosporidians were also amplified, often associated with bivalves or deep-sea samples. The general primer approach amplified an overlapping set of novel lineages within ENDO-3 and Haplosporida, whereas the group-specific primer strategy, targeted to amplify from the earliest known divergent haplosporidians to Gromia, generated greater sequence diversity across part of this phylogenetic range.

SUBMITTER: Ward GM

PROVIDER: S-EPMC6173291 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Here, we 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 as both potential reservoirs and training grounds for human pathogens. However, studies addressing their relationships with human pathogens often rely on a few domesticated amoebae that have been 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 100 diverse amoebae that were 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, which was previously reported to resist predation by laboratory strains of Acanthamoeba, was efficiently consumed by closely related environmental amoebae. The isolated amoebae were 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 an 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. Here, we sought to isolate environmental amoebae and to 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.

Dataset Information

Environmental Sequencing Fills the Gap Between Parasitic Haplosporidians and Free-living Giant Amoebae.

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