Abstract
The digenetic trematode Schistosoma mansoni is a human parasite that uses the mollusc Biomphalaria glabrata as intermediate host. Specific S. mansoni strains can infect efficiently only certain B. glabrata strains (compatible strain) while others are incompatible. Strain-specific differences in transcription of a conserved family of polymorphic mucins (SmPoMucs) in S. mansoni are the principle determinants for this compatibility. In the present study, we investigated the bases of the control of SmPoMuc expression that evolved to evade B. glabrata diversified antigen recognition molecules. We compared the DNA sequences and chromatin structure of SmPoMuc promoters of two S. mansoni 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 SmPoMuc 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 SmPoMuc in the IC strain compared to the C strain and correlate with the presence of additional combinations of SmPoMuc 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.
Highlights
The interaction of hosts and parasites is one of the best-studied examples of evolution in a changing environment [1]
Transcription of SmPoMuc genes is different in IC and C strains of S. mansoni
SmPoMucs genes have a 59 region containing a variable number of tandem repeats, which have been previously called r1 and r2 [8]. r2 exclusively occurs in the group1 and 2 and the intermingled r1–r2 exclusively occurs in the subgroup 3.1, which is present in several copies with either the r1–r2 intermingled repeats or with r1
Summary
The interaction of hosts and parasites is one of the best-studied examples of evolution in a changing environment [1]. Their reciprocal antagonistic co-evolution can be illustrated by an arms race in which host and parasite develop mechanisms to circumvent counter-measures developed by their opponents [2], [3]. The phenomenon that some parasite strains are compatible with certain host strains but not with others (and vice versa) is called compatibility polymorphism. This phenomenon was described in the platyhelminth Schistosoma mansoni and its intermediate host, the mollusc Biomphalaria glabrata [5].
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