A Unique Gene Module in Thermococcales Archaea Centered on a Hypervariable Protein Containing Immunoglobulin Domains

Molecular mechanisms involved in biological conflicts and self vs nonself recognition in archaea remain poorly characterized. We apply phylogenomic analysis to identify a hypervariable gene module that is widespread among Thermococcales. These loci consist of an upstream gene coding for a large protein containing several immunoglobulin (Ig) domains and unique combinations of downstream genes, some of which also contain Ig domains. In the large Ig domain containing protein, the C-terminal Ig domain sequence is hypervariable, apparently, as a result of recombination between genes from different Thermococcales. To reflect the hypervariability, we denote this gene module VARTIG (VARiable Thermococcales IG). The overall organization of the VARTIG modules is similar to the organization of Polymorphic Toxin Systems (PTS). Archaeal genomes outside Thermococcales encode a variety of Ig domain proteins, but no counterparts to VARTIG and no Ig domains with comparable levels of variability. The specific functions of VARTIG remain unknown but the identified features of this system imply three testable hypotheses: (i) involvement in inter-microbial conflicts analogous to PTS, (ii) role in innate immunity analogous to the vertebrate complement system, and (iii) function in self vs nonself discrimination analogous to the vertebrate Major Histocompatibility Complex. The latter two hypotheses seem to be of particular interest given the apparent analogy to the vertebrate immunity.

Cytoplasmic Mixing, Not Nuclear Coexistence, Can Explain Somatic Incompatibility in Basidiomycetes

Nonself recognition leading to somatic incompatibility (SI) is commonly used by mycologists to distinguish fungal individuals. Despite this, the process remains poorly understood in basidiomycetes as all current models of SI are based on genetic and molecular research in ascomycete fungi. Ascomycete fungi are mainly found in a monokaryotic stage, with a single type of haploid nuclei, and only briefly during mating do two genomes coexist in heterokaryotic cells. The sister phylum, Basidiomycota, differs in several relevant aspects. Basidiomycete fungi have an extended heterokaryotic stage, and SI is generally observed between heterokaryons instead of between homokaryons. Additionally, considerable nuclear migration occurs during a basidiomycete mating reaction, introducing a nucleus into a resident homokaryon with cytoplasmic mixing limited to the fused or neighboring cells. To accommodate these differences, we describe a basidiomycete model for nonself recognition using post-translational modification, based on a reader-writer system as found in other organisms. This post-translational modification combined with nuclear migration allows for the coexistence of two genomes in one individual while maintaining nonself recognition during all life stages. Somewhat surprisingly, this model predicts localized cell death during mating, which is consistent with previous observations but differs from the general assumptions of basidiomycete mating. This model will help guide future research into the mechanisms behind basidiomycete nonself recognition.

Nonself-recognition-based self-incompatibility can alternatively promote or prevent introgression

1SummaryTraditionally, we expect that self-incompatibility alleles (S-alleles), which prevent self-fertilization, should benefit from negative-frequency dependent selection and rise to high frequency when introduced to a new population through gene flow. However, the most taxonomically widespread form of self-incompatibility, the ribonuclease-based system ancestral to the core eudicots, functions through nonself-recognition, which drastically alters the process of S-allele diversification.We analyze a model of S-allele evolution in two populations connected by migration, focusing on comparisons among the fates of S-alleles originally unique to each population and those shared among populations.We find that both shared and unique S-alleles originating from the population with more unique S-alleles were usually fitter than S-alleles from the population with fewer. Resident S-alleles were often driven extinct and replaced by migrant S-alleles, though this outcome could be averted by pollen limitation or biased migration.Nonself-recognition-based self-incompatibility will usually either disfavor introgression of S-alleles or result in the whole-sale replacement of S-alleles from one population with those from another.

Amyloid Signaling in Filamentous Fungi and Bacteria

Amyloids are implicated in many protein misfolding diseases. Amyloid folds, however, also display a range of functional roles particularly in the microbial world. The templating ability of these folds endows them with specific properties allowing their self-propagation and protein-to-protein transmission in vivo. This property, the prion principle, is exploited by specific signaling pathways that use transmission of the amyloid fold as a way to convey information from a receptor to an effector protein. I describe here amyloid signaling pathways involving fungal nucleotide binding and oligomerization domain (NOD)-like receptors that were found to control nonself recognition and programmed cell death processes. Studies on these fungal amyloid signaling motifs stem from the characterization of the fungal [Het-s] prion protein and have led to the identification in fungi but also in multicellular bacteria of several distinct families of signaling motifs, one of which is related to RHIM [receptor-interacting protein (RIP) homotypic interaction motif], an amyloid motif regulating mammalian necroptosis.