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Invertebrate Immunity
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Invertebrate Immunity

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (30 November 2019) | Viewed by 24544

Special Issue Editors

Dr. Benjamin Gourbal

E-Mail Website1 Website2
Guest Editor
IHPE, University Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, 66860 Perpignan, France
Interests: comparative immunology; evolution of immunity; invertebrate innate immunity; Biomphalaria glabrata; Schistosoma mansoni; compatibility polymorphism; specificity; immune recognition; immune priming; innate immune memory; molecular mechanisms; trans-generational immune priming; comparative molecular approaches; transcriptomic; proteomic; epigenomic
Dr. Patrick Hanington

E-Mail Website
Guest Editor
School of Public Health, University of Alberta, Edmonton, AB, Canada
Interests: invertebrate immunity; parasitology; host-parasite interactions; parasite detection and monitoring; water; environmental health

Special Issue Information

Dear Colleagues,

All living organisms face biotic and abiotic stressors in their environments. Pathogens, for example, cause substantial deleterious effects on their hosts, and thus represent a major driving force for host evolution. Therefore, all living organisms have evolved defence systems capable of recognizing and controlling/containing and/or eliminating most of the pathogens encountered during their life. Efforts to escalate the diversity and availability of genomic resources have substantially increased our knowledge of the molecular basis of invertebrate immunity and presented an opportunity to improve our comprehension of invertebrate immune systems and host–pathogen evolution. The advent of “omic” approaches reconciles mechanisms with phenomena and paves the way to a better characterization of the molecular supports of innate immune processes and immunological memory in diverse model and non-model organisms. Deciphering the cellular and molecular basis of immune responses from an increasing variety of phylogenetically distant models sheds light on the nature, origin, and complexity of the evolutionary innovations of the immune responses of invertebrates.

The forthcoming Special Issue aims to provide an overview of recent topics on invertebrate immunity, with an emphasis on reviews and fundamental or applied studies that aim to decipher the dynamic molecular processes of invertebrate immune responses as they adapt and respond to pathogen and parasite challenges. Priority will be given to works that elucidate new immune mechanisms in invertebrates, challenging the commonly accepted paradigms in innate immunity, notably revealing recognition specificity, the complexity of innate immune responses, and adaptive-like mechanisms (priming/memory) and transfer protection to offspring.

Dr. Patrick Hanington
Dr. Benjamin Gourbal
Guest Editors

Manuscript Submission Information

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Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • Invertebrates
  • host–parasite interactions
  • ecology
  • evolution
  • innate immunity
  • immune priming
  • immune memory
  • trained immunity
  • trans-generational immunity

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Published Papers (7 papers)

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Research

13 pages, 3490 KiB  
Article
Shedding Light on the Antimicrobial Peptide Arsenal of Terrestrial Isopods: Focus on Armadillidins, a New Crustacean AMP Family
by Thomas Becking, Carine Delaunay, Richard Cordaux, Jean-Marc Berjeaud, Christine Braquart-Varnier and Julien Verdon
Genes 2020, 11(1), 93; https://doi.org/10.3390/genes11010093 - 14 Jan 2020
Cited by 11 | Viewed by 3704
Abstract
In crustaceans, antimicrobial peptides (AMPs) are clustered into four major groups according to their amino acid composition and structure: (1) single-domain peptides containing cysteine residues such as anti-lipopolysaccharide-factor (ALF), (2) multi-domain or chimeric AMPs such as crustins, (3) non-conventional AMPs, and (4) linear [...] Read more.
In crustaceans, antimicrobial peptides (AMPs) are clustered into four major groups according to their amino acid composition and structure: (1) single-domain peptides containing cysteine residues such as anti-lipopolysaccharide-factor (ALF), (2) multi-domain or chimeric AMPs such as crustins, (3) non-conventional AMPs, and (4) linear single-domain AMPs. The majority of AMPs has been described in commercially exploited crustaceans, particularly decapods living in aquatic environments (crab, shrimp, lobster, and crayfish). Here, we aimed at establishing the AMPs repertoire of terrestrial isopods (Oniscidea), an original suborder of crustaceans adapted to life outside of the aquatic environment. Using transcriptomic data from 21 species, we identified 110 ALF and 73 crustin sequences. We also characterized the full-length sequence of armadillidins from 17 species, similar to the AMP previously described in the terrestrial isopod Armadillidium vulgare. Furthermore, we tested the antimicrobial activity of three armadillidin peptides characterized from three distantly related species. This analysis revealed similar activity spectra against pathogens, despite extensive structural variation among the tested peptides. In addition to conventional crustacean AMPs, our work highlights armadillidins as a new and independent family of AMPs specific to the Oniscidea, thus opening new perspectives concerning the study of the immune system of terrestrial isopods. Full article
(This article belongs to the Special Issue Invertebrate Immunity)
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16 pages, 1985 KiB  
Article
A New Assessment of Thioester-Containing Proteins Diversity of the Freshwater Snail Biomphalaria glabrata
by David Duval, Remi Pichon, Damien Lassalle, Maud Laffitte, Benjamin Gourbal and Richard Galinier
Genes 2020, 11(1), 69; https://doi.org/10.3390/genes11010069 - 7 Jan 2020
Cited by 16 | Viewed by 4164
Abstract
Thioester-containing proteins (TEPs) superfamily is known to play important innate immune functions in a wide range of animal phyla. TEPs are involved in recognition, and in the direct or mediated killing of several invading organisms or pathogens. While several TEPs have been identified [...] Read more.
Thioester-containing proteins (TEPs) superfamily is known to play important innate immune functions in a wide range of animal phyla. TEPs are involved in recognition, and in the direct or mediated killing of several invading organisms or pathogens. While several TEPs have been identified in many invertebrates, only one TEP (named BgTEP) has been previously characterized in the freshwater snail, Biomphalaria glabrata. As the presence of a single member of that family is particularly intriguing, transcriptomic data and the recently published genome were used to explore the presence of other BgTEP related genes in B. glabrata. Ten other TEP members have been reported and classified into different subfamilies: Three complement-like factors (BgC3-1 to BgC3-3), one α-2-macroblobulin (BgA2M), two macroglobulin complement-related proteins (BgMCR1, BgMCR2), one CD109 (BgCD109), and three insect TEP (BgTEP2 to BgTEP4) in addition to the previously characterized BgTEP that we renamed BgTEP1. This is the first report on such a level of TEP diversity and of the presence of macroglobulin complement-related proteins (MCR) in mollusks. Gene structure analysis revealed alternative splicing in the highly variable region of three members (BgA2M, BgCD109, and BgTEP2) with a particularly unexpected diversity for BgTEP2. Finally, different gene expression profiles tend to indicate specific functions for such novel family members. Full article
(This article belongs to the Special Issue Invertebrate Immunity)
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17 pages, 3721 KiB  
Article
Glabralysins, Potential New β-Pore-Forming Toxin Family Members from the Schistosomiasis Vector Snail Biomphalaria glabrata
by Damien Lassalle, Guillaume Tetreau, Silvain Pinaud, Richard Galinier, Neil Crickmore, Benjamin Gourbal and David Duval
Genes 2020, 11(1), 65; https://doi.org/10.3390/genes11010065 - 7 Jan 2020
Cited by 8 | Viewed by 4346
Abstract
Biomphalaria glabrata is a freshwater Planorbidae snail. In its environment, this mollusk faces numerous microorganisms or pathogens, and has developed sophisticated innate immune mechanisms to survive. The mechanisms of recognition are quite well understood in Biomphalaria glabrata, but immune effectors have been [...] Read more.
Biomphalaria glabrata is a freshwater Planorbidae snail. In its environment, this mollusk faces numerous microorganisms or pathogens, and has developed sophisticated innate immune mechanisms to survive. The mechanisms of recognition are quite well understood in Biomphalaria glabrata, but immune effectors have been seldom described. In this study, we analyzed a new family of potential immune effectors and characterized five new genes that were named Glabralysins. The five Glabralysin genes showed different genomic structures and the high degree of amino acid identity between the Glabralysins, and the presence of the conserved ETX/MTX2 domain, support the hypothesis that they are pore-forming toxins. In addition, tertiary structure prediction confirms that they are structurally related to a subset of Cry toxins from Bacillus thuringiensis, including Cry23, Cry45, and Cry51. Finally, we investigated their gene expression profiles in snail tissues and demonstrated a mosaic transcription. We highlight the specificity in Glabralysin expression following immune stimulation with bacteria, yeast or trematode parasites. Interestingly, one Glabralysin was found to be expressed in immune-specialized hemocytes, and two others were induced following parasite exposure. Full article
(This article belongs to the Special Issue Invertebrate Immunity)
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12 pages, 1226 KiB  
Article
Biomphalaria glabrata Granulin Increases Resistance to Schistosoma mansoni Infection in Several Biomphalaria Species and Induces the Production of Reactive Oxygen Species by Haemocytes
by Jacob R. Hambrook, Abdullah A. Gharamah, Emmanuel A. Pila, Solomon Hussein and Patrick C. Hanington
Genes 2020, 11(1), 38; https://doi.org/10.3390/genes11010038 - 28 Dec 2019
Cited by 9 | Viewed by 2872
Abstract
Gastropod molluscs, which have co-evolved with parasitic digenean trematodes for millions of years, utilize circulating heamocytes as the primary method of containing and killing these invading parasites. In order to do so, they must generate suitable amounts of haemocytes that are properly armed [...] Read more.
Gastropod molluscs, which have co-evolved with parasitic digenean trematodes for millions of years, utilize circulating heamocytes as the primary method of containing and killing these invading parasites. In order to do so, they must generate suitable amounts of haemocytes that are properly armed to kill parasitic worms. One method by which they generate the haemocytes required to initiate the appropriate cell mediated immune response is via the production and post-translational processing of granulins. Granulins are an evolutionarily conserved family of growth factors present in the majority of eukaryotic life forms. In their pro-granulin form, they can elicit cellular replication and differentiation. The pro-granulins can be further processed by elastase to generate smaller granulin fragments that have been shown to functionally differ from the pro-granulin precursor. In this study, we demonstrate that in vivo addition of Biomphalaria glabrata pro-granulin (BgGRN) can reduce Schistosoma mansoni infection success in numerous Biomphalaria sp. when challenged with different S. mansoni strains. We also demonstrate that cleavage of BgGRN into individual granulin subunits by elastase results in the stimulation of haemocytes to produce reactive oxygen species. Full article
(This article belongs to the Special Issue Invertebrate Immunity)
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18 pages, 1880 KiB  
Article
Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor
by Clémentine Bernier, Céline Boidin-Wichlacz, Aurélie Tasiemski, Nina Hautekèete, François Massol and Virginie Cuvillier-Hot
Genes 2019, 10(12), 989; https://doi.org/10.3390/genes10120989 - 1 Dec 2019
Cited by 5 | Viewed by 2563
Abstract
Transgenerational immune priming (TGIP) is an intriguing form of parental care which leads to the plastic adjustment of the progeny’s immunity according to parental immune experience. Such parental effect has been described in several vertebrate and invertebrate taxa. However, very few empirical studies [...] Read more.
Transgenerational immune priming (TGIP) is an intriguing form of parental care which leads to the plastic adjustment of the progeny’s immunity according to parental immune experience. Such parental effect has been described in several vertebrate and invertebrate taxa. However, very few empirical studies have been conducted from the field, with natural host-parasite systems and real ecological settings, especially in invertebrates. We investigated TGIP in wild populations of the marine annelid Hediste diversicolor. Females laid eggs in a mud tube and thus shared the local microbial threats with the first developmental stages, thus meeting expectations for the evolution of TGIP. We evidenced that a maternal bacterial challenge led to the higher antibacterial defense of the produced oocytes, with higher efficiency in the case of Gram-positive bacterial challenge, pointing out a prevalent role of these bacteria in the evolutionary history of TGIP in this species. Underlying mechanisms might involve the antimicrobial peptide hedistin that was detected in the cytoplasm of oocytes and whose mRNAs were selectively stored in higher quantity in mature oocytes, after a maternal immune challenge. Finally, maternal immune transfer was significantly inhibited in females living in polluted areas, suggesting associated costs and the possible trade-off with female’s protection. Full article
(This article belongs to the Special Issue Invertebrate Immunity)
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22 pages, 5936 KiB  
Article
Cross-Kingdom Analysis of Diversity, Evolutionary History, and Site Selection within the Eukaryotic Macrophage Migration Inhibitory Factor Superfamily
by Claire Michelet, Etienne G. J. Danchin, Maelle Jaouannet, Jürgen Bernhagen, Ralph Panstruga, Karl-Heinz Kogel, Harald Keller and Christine Coustau
Genes 2019, 10(10), 740; https://doi.org/10.3390/genes10100740 - 24 Sep 2019
Cited by 17 | Viewed by 3571
Abstract
Macrophage migration inhibitory factors (MIF) are multifunctional proteins regulating major processes in mammals, including activation of innate immune responses. MIF proteins also play a role in innate immunity of invertebrate organisms or serve as virulence factors in parasitic organisms, raising the question of [...] Read more.
Macrophage migration inhibitory factors (MIF) are multifunctional proteins regulating major processes in mammals, including activation of innate immune responses. MIF proteins also play a role in innate immunity of invertebrate organisms or serve as virulence factors in parasitic organisms, raising the question of their evolutionary history. We performed a broad survey of MIF presence or absence and evolutionary relationships across 803 species of plants, fungi, protists, and animals, and explored a potential relation with the taxonomic status, the ecology, and the lifestyle of individual species. We show that MIF evolutionary history in eukaryotes is complex, involving probable ancestral duplications, multiple gene losses and recent clade-specific re-duplications. Intriguingly, MIFs seem to be essential and highly conserved with many sites under purifying selection in some kingdoms (e.g., plants), while in other kingdoms they appear more dispensable (e.g., in fungi) or present in several diverged variants (e.g., insects, nematodes), suggesting potential neofunctionalizations within the protein superfamily. Full article
(This article belongs to the Special Issue Invertebrate Immunity)
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13 pages, 593 KiB  
Article
The Challenge of the Sponge Suberites domuncula (Olivi, 1792) in the Presence of a Symbiotic Bacterium and a Pathogen Bacterium
by Gaël Le Pennec and Johan Gardères
Genes 2019, 10(7), 485; https://doi.org/10.3390/genes10070485 - 26 Jun 2019
Cited by 4 | Viewed by 2290
Abstract
Sponges, which are in close contact with numerous bacteria in prey/predator, symbiotic and pathogenic relationships, must provide an appropriate response in such situations. This starts with a discriminating recognition of the partner either by a physical contact or through secreted molecules or both. [...] Read more.
Sponges, which are in close contact with numerous bacteria in prey/predator, symbiotic and pathogenic relationships, must provide an appropriate response in such situations. This starts with a discriminating recognition of the partner either by a physical contact or through secreted molecules or both. We investigated the expression of the Toll-like receptor, Caspase 3/7, Tumor Necrosis Factor receptor-associated factor 6, Bcl-2 homology protein-2 and macrophage expressed genes of axenic sponge cells in the presence of a symbiotic bacterium (Endozoicomonas sp. Hex311), a pathogen bacterium (Pseudoalteromonas sp. 1A1), their exoproducts and lipopolysaccharides. The vast majority of answers are in line with what could be observed with the symbiotic bacterium. The pathogenic bacterium seems to profit from the eukaryotic cell: suppression of the production of the antibacterial compound, inhibition of the apoptosis caspase-dependent pathway, deregulation of bacterial recognition. This work contributes new scientific knowledge in the field of immunology and apoptosis in early branching metazoan harboring within its tissue and cells a large number of symbiotic bacteria. Full article
(This article belongs to the Special Issue Invertebrate Immunity)
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