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Journal Articles FEMS Microbiology Reviews Year : 2022

The evolution and role of eukaryotic-like domains in environmental intracellular bacteria: the battle with a eukaryotic cell

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Abstract

One sentence summary: This review aims to dissect the evolutionary processes that may lead to an enrichment of eukaryotic-like proteins in environmental intracellular bacteria through continuous adaptation to multiple eukaryotic hosts. We reveal that chromatin and ubiquitin modulation functions, as well as adaptable tandem repeat domains, are crucial for their virulence in protozoa and accidentally also in humans. Intracellular pathogens that are able to thrive in different environments, such as Legionella spp. that preferentially live in protozoa in aquatic environments or environmental Chlamydiae that replicate either within protozoa or a range of animals, possess a plethora of cellular biology tools to influence their eukaryotic host. The host manipulation tools that evolved in the interaction with protozoa confer these bacteria the capacity to also infect phylogenetically distinct eukaryotic cells, such as macrophages, and thus they can also be human pathogens. To manipulate the host cell, bacteria use protein secretion systems and molecular effectors. Although these molecular effectors are encoded in bacteria, they are expressed and function in a eukaryotic context often mimicking or inhibiting eukaryotic proteins. Indeed, many of these effectors have eukaryotic-like domains. In this review, we propose that the main pathways that environmental intracellular bacteria need to subvert in order to establish the host eukaryotic cell as a replication niche are chromatin remodelling, ubiquitination signalling and modulation of protein–protein interactions via tandem repeat domains. We then provide mechanistic insight into how these proteins might have evolved. Finally, we highlight that in environmental intracellular bacteria the number of eukaryotic-like domains and proteins is considerably higher than in intracellular bacteria specialized to an isolated niche, such as obligate intracellular human pathogens. As mimics of eukaryotic proteins are critical components of host–pathogen interactions, this distribution of eukaryotic-like domains suggests that the environment has selected them.
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Dates and versions

pasteur-03913556 , version 1 (27-12-2022)

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Jessica Martyn, Laura Gomez-Valero, Carmen Buchrieser. The evolution and role of eukaryotic-like domains in environmental intracellular bacteria: the battle with a eukaryotic cell. FEMS Microbiology Reviews, 2022, 46 (4), ⟨10.1093/femsre/fuac012⟩. ⟨pasteur-03913556⟩
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