<i>Schistosoma mansoni</i> Mucin Gene (<i>Sm</i>PoMuc) Expression: Epigenetic Control to Shape Adaptation to a New Host

<div><p>The digenetic trematode <i>Schistosoma mansoni</i> is a human parasite that uses the mollusc <i>Biomphalaria glabrata</i> as intermediate host. Specific <i>S. mansoni</i> strains can infect efficiently only certain <i>B. glabrata</i> strains (compatible strain) while others are incompatible. Strain-specific differences in transcription of a conserved family of polymorphic mucins (<i>Sm</i>PoMucs) in <i>S. mansoni</i> are the principle determinants for this compatibility. In the present study, we investigated the bases of the control of <i>Sm</i>PoMuc expression that evolved to evade <i>B. glabrata</i> diversified antigen recognition molecules. We compared the DNA sequences and chromatin structure of <i>Sm</i>PoMuc promoters of two <i>S. mansoni</i> strains that are either compatible (C) or incompatible (IC) with a reference snail host. We reveal that although sequence differences are observed between active promoter regions of <i>Sm</i>PoMuc genes, the sequences of the promoters are not diverse and are conserved between IC and C strains, suggesting that genetics alone cannot explain the evolution of compatibility polymorphism. In contrast, promoters carry epigenetic marks that are significantly different between the C and IC strains. Moreover, we show that modifications of the structure of the chromatin of the parasite modify transcription of <i>Sm</i>PoMuc in the IC strain compared to the C strain and correlate with the presence of additional combinations of <i>Sm</i>PoMuc transcripts only observed in the IC phenotype. Our results indicate that transcription polymorphism of a gene family that is responsible for an important adaptive trait of the parasite is epigenetically encoded. These strain-specific epigenetic marks are heritable, but can change while the underlying genetic information remains stable. This suggests that epigenetic changes may be important for the early steps in the adaptation of pathogens to new hosts, and might be an initial step in adaptive evolution in general.</p>