Innate immunity in the simplest animals – placozoans

Abstract Background Innate immunity provides the core recognition system in animals for preventing infection, but also plays an important role in managing the relationship between an animal host and its symbiont. Most of our knowledge about innate immunity stems from a few animal model systems, but...

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Main Authors: Kai Kamm, Bernd Schierwater, Rob DeSalle
Format: Article
Language:English
Published: BMC 2019-01-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-018-5377-3
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author Kai Kamm
Bernd Schierwater
Rob DeSalle
author_facet Kai Kamm
Bernd Schierwater
Rob DeSalle
author_sort Kai Kamm
collection DOAJ
description Abstract Background Innate immunity provides the core recognition system in animals for preventing infection, but also plays an important role in managing the relationship between an animal host and its symbiont. Most of our knowledge about innate immunity stems from a few animal model systems, but substantial variation between metazoan phyla has been revealed by comparative genomic studies. The exploration of more taxa is still needed to better understand the evolution of immunity related mechanisms. Placozoans are morphologically the simplest organized metazoans and the association between these enigmatic animals and their rickettsial endosymbionts has recently been elucidated. Our analyses of the novel placozoan nuclear genome of Trichoplax sp. H2 and its associated rickettsial endosymbiont genome clearly pointed to a mutualistic and co-evolutionary relationship. This discovery raises the question of how the placozoan holobiont manages symbiosis and, conversely, how it defends against harmful microorganisms. In this study, we examined the annotated genome of Trichoplax sp. H2 for the presence of genes involved in innate immune recognition and downstream signaling. Results A rich repertoire of genes belonging to the Toll-like and NOD-like receptor pathways, to scavenger receptors and to secreted fibrinogen-related domain genes was identified in the genome of Trichoplax sp. H2. Nevertheless, the innate immunity related pathways in placozoans deviate in several instances from well investigated vertebrates and invertebrates. While true Toll- and NOD-like receptors are absent, the presence of many genes of the downstream signaling cascade suggests at least primordial Toll-like receptor signaling in Placozoa. An abundance of scavenger receptors, fibrinogen-related domain genes and Apaf-1 genes clearly constitutes an expansion of the immunity related gene repertoire specific to Placozoa. Conclusions The found wealth of immunity related genes present in Placozoa is surprising and quite striking in light of the extremely simple placozoan body plan and their sparse cell type makeup. Research is warranted to reveal how Placozoa utilize this immune repertoire to manage and maintain their associated microbiota as well as to fend-off pathogens.
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spelling doaj.art-db71ba22e54e4a5c8abfb081739b39262022-12-22T03:57:15ZengBMCBMC Genomics1471-21642019-01-0120111210.1186/s12864-018-5377-3Innate immunity in the simplest animals – placozoansKai Kamm0Bernd Schierwater1Rob DeSalle2ITZ Ecology and Evolution, University of Veterinary Medicine Hannover, FoundationITZ Ecology and Evolution, University of Veterinary Medicine Hannover, FoundationSackler Institute for Comparative Genomics and Division of Invertebrate Zoology, American Museum of Natural HistoryAbstract Background Innate immunity provides the core recognition system in animals for preventing infection, but also plays an important role in managing the relationship between an animal host and its symbiont. Most of our knowledge about innate immunity stems from a few animal model systems, but substantial variation between metazoan phyla has been revealed by comparative genomic studies. The exploration of more taxa is still needed to better understand the evolution of immunity related mechanisms. Placozoans are morphologically the simplest organized metazoans and the association between these enigmatic animals and their rickettsial endosymbionts has recently been elucidated. Our analyses of the novel placozoan nuclear genome of Trichoplax sp. H2 and its associated rickettsial endosymbiont genome clearly pointed to a mutualistic and co-evolutionary relationship. This discovery raises the question of how the placozoan holobiont manages symbiosis and, conversely, how it defends against harmful microorganisms. In this study, we examined the annotated genome of Trichoplax sp. H2 for the presence of genes involved in innate immune recognition and downstream signaling. Results A rich repertoire of genes belonging to the Toll-like and NOD-like receptor pathways, to scavenger receptors and to secreted fibrinogen-related domain genes was identified in the genome of Trichoplax sp. H2. Nevertheless, the innate immunity related pathways in placozoans deviate in several instances from well investigated vertebrates and invertebrates. While true Toll- and NOD-like receptors are absent, the presence of many genes of the downstream signaling cascade suggests at least primordial Toll-like receptor signaling in Placozoa. An abundance of scavenger receptors, fibrinogen-related domain genes and Apaf-1 genes clearly constitutes an expansion of the immunity related gene repertoire specific to Placozoa. Conclusions The found wealth of immunity related genes present in Placozoa is surprising and quite striking in light of the extremely simple placozoan body plan and their sparse cell type makeup. Research is warranted to reveal how Placozoa utilize this immune repertoire to manage and maintain their associated microbiota as well as to fend-off pathogens.http://link.springer.com/article/10.1186/s12864-018-5377-3Innate immunityPlacozoaTrichoplaxSymbiosisToll-like receptor pathwayNOD-like receptor pathway
spellingShingle Kai Kamm
Bernd Schierwater
Rob DeSalle
Innate immunity in the simplest animals – placozoans
BMC Genomics
Innate immunity
Placozoa
Trichoplax
Symbiosis
Toll-like receptor pathway
NOD-like receptor pathway
title Innate immunity in the simplest animals – placozoans
title_full Innate immunity in the simplest animals – placozoans
title_fullStr Innate immunity in the simplest animals – placozoans
title_full_unstemmed Innate immunity in the simplest animals – placozoans
title_short Innate immunity in the simplest animals – placozoans
title_sort innate immunity in the simplest animals placozoans
topic Innate immunity
Placozoa
Trichoplax
Symbiosis
Toll-like receptor pathway
NOD-like receptor pathway
url http://link.springer.com/article/10.1186/s12864-018-5377-3
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AT berndschierwater innateimmunityinthesimplestanimalsplacozoans
AT robdesalle innateimmunityinthesimplestanimalsplacozoans