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Receptors Mediating Host-Microbiota Communication in the Metaorganism: The Invertebrate Perspective.

ABSTRACT: Multicellular organisms live in close association with a plethora of microorganism, which have a profound effect on multiple host functions. As such, the microbiota and its host form an intimate functional entity, termed the metaorganism or holobiont. But how does the metaorganism communicate? Which receptors recognize microbial signals, mediate the effect of the microbiota on host physiology or regulate microbiota composition and homeostasis? In this review we provide an overview on the function of different receptor classes in animal host-microbiota communication. We put a special focus on invertebrate hosts, including both traditional invertebrate models such as Drosophila melanogaster and Caenorhabditis elegans and "non-model" invertebrates in microbiota research. Finally, we highlight the potential of invertebrate systems in studying mechanism of host-microbiota interactions.

SUBMITTER: Dierking K

PROVIDER: S-EPMC7308585 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Receptors Mediating Host-Microbiota Communication in the Metaorganism: The Invertebrate Perspective.

Dierking Katja K Pita Lucía L

Frontiers in immunology 20200616

Multicellular organisms live in close association with a plethora of microorganism, which have a profound effect on multiple host functions. As such, the microbiota and its host form an intimate functional entity, termed the metaorganism or holobiont. But how does the metaorganism communicate? Which receptors recognize microbial signals, mediate the effect of the microbiota on host physiology or regulate microbiota composition and homeostasis? In this review we provide an overview on the functio ...[more]

PMID: 32612612

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Project description:For many decades, invertebrate immunity was believed to be non-adaptive, poorly specific, relying exclusively on sometimes multiple but germ-line encoded innate receptors and effectors. But recent studies performed in different invertebrate species have shaken this paradigm by providing evidence for various types of somatic adaptations at the level of putative immune receptors leading to an enlarged repertoire of recognition molecules. Fibrinogen Related Proteins (FREPs) from the mollusc Biomphalaria glabrata are an example of these putative immune receptors. They are known to be involved in reactions against trematode parasites. Following not yet well understood somatic mechanisms, the FREP repertoire varies considerably from one snail to another, showing a trend towards an individualization of the putative immune repertoire almost comparable to that described from vertebrate adaptive immune system. Nevertheless, their antigenic targets remain unknown. In this study, we show that a specific set of these highly variable FREPs from B. glabrata forms complexes with similarly highly polymorphic and individually variable mucin molecules from its specific trematode parasite S. mansoni (Schistosoma mansoni Polymorphic Mucins: SmPoMucs). This is the first evidence of the interaction between diversified immune receptors and antigenic variant in an invertebrate host/pathogen model. The same order of magnitude in the diversity of the parasite epitopes and the one of the FREP suggests co-evolutionary dynamics between host and parasite regarding this set of determinants that could explain population features like the compatibility polymorphism observed in B. glabrata/S. mansoni interaction. In addition, we identified a third partner associated with the FREPs/SmPoMucs in the immune complex: a Thioester containing Protein (TEP) belonging to a molecular category that plays a role in phagocytosis or encapsulation following recognition. The presence of this last partner in this immune complex argues in favor of the involvement of the formed complex in parasite recognition and elimination from the host.

Project description:Scavenger receptors are cell surface membrane-bound receptors that typically bind multiple ligands and promote the removal of endogenous proteins and pathogens. In this study, we characterized a novel scavenger receptor-like protein, namely, SpBark. SpBark was upregulated in hemocytes after challenges with bacteria, suggesting that it might be involved in antibacterial defense. SpBark is a type I transmembrane protein with four extracellular domains, including three scavenger receptor cysteine-rich domains (SRCRDs) and a C-type lectin domain (CTLD). Western blot assay showed that SpBark CTLD possessed a much stronger binding activity to tested microbes than the three SRCRDs. It also exhibited apparent binding activities to lipopolysaccharide (LPS) and acetylated low-density lipoprotein (ac-LDL), whereas the other SRCRDs showed much lower or no binding activities to these components. Agglutination activities were observed in the presence of Ca2+ by incubating microorganisms with SpBark CTLD instead of SRCRDs. These results suggested that SpBark CTLD was the major binding site for ac-LDL and LPS. Coating Vibrio parahemolyticus with SpBark CTLD promoted bacterial clearance in vivo. This finding indicated that SpBark might participate in the immune defenses against Gram-negative bacteria through a certain mechanism. The promotion of bacterial clearance by SpBark was further determined using SpBark-silenced crabs injected with V. parahemolyticus. SpBark knockdown by injection of SpBark dsRNA remarkably suppressed the clearance of bacteria in hemolymph. Meanwhile, it also severely restrained the phagocytosis of bacteria. This finding suggested that SpBark could modulate the phagocytosis of bacteria, and the promotion of bacterial clearance by SpBark was closely related to SpBark-mediated phagocytosis activity. The likely mechanism of bacterial clearance mediated by SpBark was as follows: SpBark acted as a pattern recognition receptor, which could sense and bind to LPS on the surface of invading bacteria with its CTLD in hemolymph. The binding to LPS made the bacteria adhere to the surface of hemocytes. This process would facilitate phagocytosis of the bacteria, resulting in their removal. This study provided new insights into the hemocyte phagocytosis mechanisms of invertebrates and the multiple biological functions of Bark proteins.

Dataset Information

Receptors Mediating Host-Microbiota Communication in the Metaorganism: The Invertebrate Perspective.

Publications

Receptors Mediating Host-Microbiota Communication in the Metaorganism: The Invertebrate Perspective.

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