Gene networks governing the response of a calcareous sponge to future
ocean conditions reveal lineage-specific XBP1 regulation of the
unfolded protein response
Abstract
Marine sponges are predicted to be winners in the future ocean due to
their exemplary adaptive capacity. However, while many sponge groups
exhibit tolerance to a wide range of environmental insults, calcifying
sponges may be more susceptible to thermo-acidic stress. To describe the
gene regulatory networks that govern the stress response of a calcareous
sponge, Leucetta chagosensis (class Calcarea, order Clathrinida),
individuals were subjected to warming and acidification conditions based
on the climate models for 2100. Transcriptome analysis and gene
co-expression network reconstruction revealed that the unfolded protein
response (UPR) was activated under thermo-acidic stress. Among the
upregulated genes were two lineage-specific homologs of X-box binding
protein 1 (XBP1), a transcription factor that activates the UPR.
Alternative dimerization between these XBP1 gene products suggests a
clathrinid-specific mechanism to reversibly sequester the transcription
factor into an inactive form, enabling the rapid regulation of pathways
linked to the UPR in clathrinid calcareous sponges. Our findings support
the idea that transcription factor duplication events may refine
evolutionarily conserved molecular pathways and contribute to ecological
success.