Genome‐wide DNA methylation signatures of infection status in Trinidadian guppies (Poecilia reticulata)

Abstract

Epigenetic modification, especially DNA methylation, can play an important role in mediating gene regulatory response to environmental stressors and may be a key process affecting phenotypic plasticity and adaptation. Parasites are potent stressors with profound physiological and ecological effects on their hosts, yet it remains unclear how parasites influence host methylation patterns. Here, we used a well-studied host-parasite system, the guppy Poecilia reticulata and its ectoparasitic monogenean Gyrodactylus turnbulli to gain mechanistic insight into the dynamics of DNA methylation in host-parasite interactions. To explore this, we quantitatively measured genome-wide DNA methylation in guppy skin tissue using reduced representation bisulphite sequencing and characterized differential methylation patterns in guppies during distinct phases of infection. We identified 365, 313, and 741 differentially methylated regions (DMRs) between infected and control fish in early infection, peak infection and recovery phases, respectively. The magnitude of the methylation difference was moderate in DMRs, with an average of 29% (early infection), 27% (peak infection) and 30% (recovery) differential methylation per DMR. Approximately 50% of DMRs overlapped with CpG islands, and over half of the DMRs overlapped with gene bodies, several of which encode proteins relevant to immune response. These findings provide the first evidence of an epigenetic signature of infection by ectoparasites and demonstrate the changing relationship between epigenetic variation and immune response in distinct phases of infection.

Museum epigenomics: characterizing cytosine methylation in historic museum specimens

“…Sequences with a read depth less than 10X were excluded following conservative guidelines for calling percent methylation (Ziller et al 2015). To account for PCR duplication, we also excluded positions with abnormally high coverage, defined as bases in the top 99.9th percentile of read depth for each individual (following Hu et al 2018). Because many loci were sequenced for each individual, we included specimen identity as a random intercept term in all models.…”

Local parasite pressures and host genotype modulate epigenetic diversity in a mixed‐mating fish

“…Several abiotic and biotic factors, including parasites (Hu et al, ; Norouzitallab et al, ) as well as stochastic epimutations (Leung et al, ), are known to influence DNA methylation variation. Our results showed that genome‐wide DNA methylation levels for all sampling sites were significantly influenced by parasite loads through the interaction with selfing lineage, suggesting a potential genotype‐by‐environment interaction on parasite responses.…”

“…Potamopyrgus snails, the oldest asexual lineages are restricted to populations where parasites are rare (Neiman, Jokela, & Lively, 2005 The long-term persistence of self-fertilizing organisms suggests that nongenetic mechanisms may play a role in regulating gene expression to cope with environmental change (Douhovnikoff & Dodd, 2015;Hu et al, 2018;Liebl et al, 2013;Shrey et al, 2012). However, recent studies indicate that DNA methylation is likely to interact with genotypes in a genotype-by-environment manner to generate plastic responses (Herman & Sultan, 2016).…”

“…Increasing evidence suggests that epigenetic mechanisms, including genome‐wide DNA methylation, are involved in host–pathogen interactions (Gómez‐Díaz, Jordà, Peinado, & Rivero, ; Hu, Pérez‐Jvostov, Blondel, & Barrett, ), but the mechanisms are better known in plants than in animals (Annacondia, Mageroy, & Martinez, ; Gómez‐Díaz et al, ; Hewezi, Pantalone, Bennett, Neal Stewart, & Jr., Burch‐Smith TM, ). Pathogenic infection in plants can result in hypomethylation of resistance‐related genes but in hypermethylation at genome‐wide level (Peng & Zhang, ).…”

Immune genes,IL1βandCasp9,show sexual dimorphic methylation patterns in the zebrafish gonads

“…In contrast, less data is found in fish. Recent findings in guppy ( Poecilia reticulate ) showed changes in DNA methylation dynamics after host–parasite interactions (Hu et al, 2018) and in Atlantic salmon ( Salmon salar ) showed that stress response together with immune challenges, altered transcriptome and methylome of the gills through immune responses (Uren Webster et al, 2018). In zebrafish, viral infections showed that histone modification was able to increase methylation levels of the gene promoters associated with innate immune response in head kidney, liver, spleen and heart (Medina-Gali et al, 2018).…”