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Phagocytosis-like cell engulfment by a planctomycete bacterium.

ABSTRACT: Phagocytosis is a key eukaryotic feature, conserved from unicellular protists to animals, that enabled eukaryotes to feed on other organisms. It could also be a driving force behind endosymbiosis, a process by which α-proteobacteria and cyanobacteria evolved into mitochondria and plastids, respectively. Here we describe a planctomycete bacterium, 'Candidatus Uab amorphum', which is able to engulf other bacteria and small eukaryotic cells through a phagocytosis-like mechanism. Observations via light and electron microscopy suggest that this bacterium digests prey cells in specific compartments. With the possible exception of a gene encoding an actin-like protein, analysis of the 'Ca. Uab amorphum' genomic sequence does not reveal any genes homologous to eukaryotic phagocytosis genes, suggesting that cell engulfment in this microorganism is probably not homologous to eukaryotic phagocytosis. The discovery of this "phagotrophic" bacterium expands our understanding of the cellular complexity of prokaryotes, and may be relevant to the origin of eukaryotic cells.

SUBMITTER: Shiratori T

PROVIDER: S-EPMC6906331 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Phagocytosis-like cell engulfment by a planctomycete bacterium.

Shiratori Takashi T Suzuki Shigekatsu S Kakizawa Yukako Y Ishida Ken-Ichiro KI

Nature communications 20191211 1

Phagocytosis is a key eukaryotic feature, conserved from unicellular protists to animals, that enabled eukaryotes to feed on other organisms. It could also be a driving force behind endosymbiosis, a process by which α-proteobacteria and cyanobacteria evolved into mitochondria and plastids, respectively. Here we describe a planctomycete bacterium, 'Candidatus Uab amorphum', which is able to engulf other bacteria and small eukaryotic cells through a phagocytosis-like mechanism. Observations via li ...[more]

PMID: 31827088

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Project description:The unique cell biology presented by members of the phylum Planctomycetota has puzzled researchers ever since their discovery. Initially thought to have eukaryotic-like features, their traits are now recognized as exceptional but distinctly bacterial. However, recently discovered strains again added novel and stunning aspects to the planctomycetal cell biology-shapeshifting by members of the "Saltatorellus" clade to an extent that is unprecedented in any other bacterial phylum, and phagocytosis-like cell engulfment in the bacterium "Candidatus Uabimicrobium amorphum." These recent additions to the phylum Planctomycetota indicate hitherto unexplored members with unique cell biology, which we aimed to make accessible for further investigations. Targeting bacteria with features like "Ca. U. amorphum", we first studied both the morphology and behavior of this microorganism in more detail. While similar to eukaryotic amoeboid organisms at first sight, we found "Ca. U. amorphum" to be rather distinct in many regards. Presenting a detailed description of "Ca. U. amorphum," we furthermore found this organism to divide in a fashion that has never been described in any other organism. Employing the obtained knowledge, we isolated a second "bacterium of prey" from the harbor of Heligoland Island (North Sea, Germany). Our isolate shares key features with "Ca. U. amorphum": phagocytosis-like cell engulfment, surface-dependent motility, and the same novel mode of cell division. Being related to "Ca. U. amorphum" within genus thresholds, we propose the name "Ca. Uabimicrobium helgolandensis" for this strain.IMPORTANCE"Candidatus Uabimicrobium helgolandensis" HlEnr_7 adds to the explored bacterial biodiversity with its phagocytosis-like uptake of prey bacteria. Enrichment of this strain indicates that there might be "impossible" microbes out there, missed by metagenomic analyses. Such organisms have the potential to challenge our understanding of nature. For example, the origin of eukaryotes remains enigmatic, with a contentious debate surrounding both the mitochondrial host entity and the moment of uptake. Currently, favored models involve a proteobacterium as the mitochondrial progenitor and an Asgard archaeon as the fusion partner. Models in which a eukaryotic ancestor engulfed the mitochondrial ancestor via phagocytosis had been largely rejected due to bioenergetic constraints. Thus, the phagocytosis-like abilities of planctomycetal bacteria might influence the debate, demonstrating that prey engulfment is possible in a prokaryotic cellular framework.

Project description:BackgroundResearch on cell-in-cell (CIC) phenomena, including entosis, emperipolesis and cannibalism, and their biological implications has increased in recent years. Homotypic and heterotypic engulfment of various target cells by numerous types of host cells has been studied in vitro and in tissue sections. This work has identified proteins involved in the mechanism and uncovered evidence for CIC as a potential histopathologic predictive and prognostic marker in cancer. Our experimental study focused on non-professional phagocytosis of leukocytes.ResultsWe studied the engulfment of peripheral blood mononuclear cells isolated from healthy donors by counting CIC structures. Two non-tumorigenic cell lines (BEAS-2B, SBLF-9) and two tumour cell lines (BxPC3, ICNI) served as host cells. Immune cells were live-stained and either directly co-incubated or treated with irradiation or with conventional or microwave hyperthermia. Prior to co-incubation, we determined leukocyte viability for each batch via Annexin V-FITC/propidium iodide staining. All host cells engulfed their targets, with uptake rates ranging from 1.0% ± 0.5% in BxPC3 to 8.1% ± 5.0% in BEAS-2B. Engulfment rates of the cancer cell lines BxPC3 and ICNI (1.6% ± 0.2%) were similar to those of the primary fibroblasts SBLF-9 (1.4% ± 0.2%). We found a significant negative correlation between leukocyte viability and cell-in-cell formation rates. The engulfment rate rose when we increased the dose of radiotherapy and prolonged the impact time. Further, microwave hyperthermia induced higher leukocyte uptake than conventional hyperthermia. Using fluorescent immunocytochemistry to descriptively study the proteins involved, we detected ring-like formations of diverse proteins around the leukocytes, consisting, among others, of α-tubulin, integrin, myosin, F-actin, and vinculin. These results suggest the involvement of actomyosin contraction, cell-cell adhesion, and the α-tubulin cytoskeleton in the engulfment process.ConclusionsBoth non-tumorigenic and cancer cells can form heterotypic CIC structures by engulfing leukocytes. Decreased viability and changes caused by microwave and X-ray irradiation trigger non-professional phagocytosis.

Project description:Vascular endothelial cells act as gatekeepers that protect underlying tissue from blood-borne toxins and pathogens. Nevertheless, endothelial cells are able to internalize large fibrin clots and apoptotic debris from the bloodstream, although the precise mechanism of such phagocytosis-like uptake is unknown. We show that cultured primary human endothelial cells (HUVEC) internalize both pathogenic and non-pathogenic Listeria bacteria comparably, in a phagocytosis-like process. In contrast with previously studied host cell types, including intestinal epithelial cells and hepatocytes, we find that endothelial internalization of Listeria is independent of all known pathogenic bacterial surface proteins. Consequently, we exploited the internalization and intracellular replication of L. monocytogenes to identify distinct host cell factors that regulate phagocytosis-like uptake in HUVEC. Using siRNA screening and subsequent genetic and pharmacologic perturbations, we determined that endothelial infectivity was modulated by cytoskeletal proteins that normally modulate global architectural changes, including phosphoinositide-3-kinase, focal adhesions, and the small GTPase Rho. We found that Rho kinase (ROCK) is acutely necessary for adhesion of Listeria to endothelial cells, whereas the actin-nucleating formins FHOD1 and FMNL3 specifically regulate internalization of bacteria as well as inert beads, demonstrating that formins regulate endothelial phagocytosis-like uptake independent of the specific cargo. Finally, we found that neither ROCK nor formins were required for macrophage phagocytosis of L. monocytogenes, suggesting that endothelial cells have distinct requirements for bacterial internalization from those of classical professional phagocytes. Our results identify a novel pathway for L. monocytogenes uptake by human host cells, indicating that this wily pathogen can invade a variety of tissues by using a surprisingly diverse suite of distinct uptake mechanisms that operate differentially in different host cell types.

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Phagocytosis-like cell engulfment by a planctomycete bacterium.

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Phagocytosis-like cell engulfment by a planctomycete bacterium.

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