Thousands of Pristionchus pacificus orphan genes were integrated into developmental networks that respond to diverse environmental microbiota

Abstract

Adaptation of organisms to environmental change may be facilitated by the creation of new genes. New genes without homologs in other lineages are known as taxonomically-restricted orphan genes and may result from divergence or de novo formation. Previously, we have extensively characterized the evolution and origin of such orphan genes in the nematode model organism Pristionchus pacificus. Here, we employ large-scale transcriptomics to establish potential functional associations and to measure the degree of transcriptional plasticity among orphan genes. Specifically, we analyzed 24 RNA-seq samples from adult P. pacificus worms raised on 24 different monoxenic bacterial cultures. Based on coexpression analysis, we identified 28 large modules that harbor 3,727 diplogastrid-specific orphan genes and that respond dynamically to different bacteria. These coexpression modules have distinct regulatory architecture and also exhibit differential expression patterns across development suggesting a link between bacterial response networks and development. Phylostratigraphy revealed a considerably high number of family- and even species-specific orphan genes in certain coexpression modules. This suggests that new genes are not attached randomly to existing cellular networks and that integration can happen very fast. Integrative analysis of protein domains, gene expression and ortholog data facilitated the assignments of biological labels for 22 coexpression modules with one of the largest, fast-evolving module being associated with spermatogenesis. In summary, this work presents the first functional annotation for thousands of P. pacificus orphan genes and reveals insights into their integration into environmentally responsive gene networks.

Starvation resistance in the nematode Pristionchus pacificus requires a conserved supplementary nuclear receptor

“…Taken together, this newly-established reference data of transcriptional responses to acute starvation constitutes an important resource for the research community which complements recent nutrigenomic advances [ 40 ] in P. pacificus. We predict that our findings will inform diverse future studies that may aim to investigate, for example, the physiological effects of different diets, metabolic rewiring under varying environmental conditions, or the evolution of molecular starvation-response machineries across nematodes.…”

“…WT = wild type. ( B ) Bar chart showing the overrepresented gene-age classes and co-expression networks (according to [ 40 ]) identified the two response clusters, relative to the genome. “Phylogenetically old genes” refers to those genes in the genome of P. pacificus that are not diplogastrid-specific orphan genes.…”

“…6 B). Additionally, we asked whether recently identified co-expression modules [ 40 ] were overrepresented among the SRGs. Indeed, genes belonging to various neuronal and oogenesis-related co-expression modules were strongly enriched amongst the up-regulated SRGs.…”

“…Additionally, we found numerous down-regulated genes to be members of a co-expression module associated with the epidermis (Fig. 6 B “cuticle 1” [ 40 ]), the site of long-term lipid storage [ 30 ]. Together with the observation that lipid anabolism is down-regulated during starvation, these data could suggest that adult P. pacificus individuals, when facing acute starvation, may undergo dramatic changes to their neural regulatory landscape which may, in turn, lead the worms to switch strategies from synthesizing and storing lipids to maintain their soma, to investing into egg production and ensuring population survival.…”

Characterization of the Pristionchus pacificus “epigenetic toolkit” reveals the evolutionary loss of the histone methyltransferase complex PRC2

“…However, there are more than 40 SET-containing genes, and it may be useful to filter this list for genes with similar structural domains as EZH2 (via structural approaches like AlphaFold) or increased positive selection correlating with the loss of PRC2 in the Pristionchus lineage. Though this uncharacterized methyltransferase is likely conserved in P. pacificus, P. exspectatus, and P. arcanus at minimum, another formal possibility is that the “PRC2 equivalent” is one of thousands of documented P. pacificus orphan genes ( Athanasouli et al . 2023 ).…”