Three genes involved in the oxidative burst are closely linked in the genome of the snail, Biomphalaria glabrata

Abstract

Allelic variation at the Cu–Zn superoxide dismutase (SOD1) locus has been shown to be associated with resistance of the snail, Biomphalaria glabrata, to infection by the trematode parasite, Schistosoma mansoni. SOD1 catalyses the production of hydrogen peroxide, a known cytotoxic component of the oxidative burst used in defence against pathogens. In our laboratory population of B. glabrata, the most resistant allele at SOD1 is over-expressed relative to the other two alleles. Because hydrogen peroxide also causes oxidative stress on host tissues, we hypothesised that over-expression of SOD1 might be compensated by epistatic interactions with other loci involved in oxidation–reduction (redox) pathways. Catalase, peroxiredoxins and glutathione peroxidases all degrade hydrogen peroxide. We tested whether alleles at each of these loci were in linkage disequilibrium with SOD1 in our population, as might be expected given strong epistatic selection. We found that SOD1, catalase (CAT) and a peroxiredoxin locus (PRX4) are in strong linkage disequilibrium in our population. We also found that these loci are tightly linked, within 1–2 cM of each other, which explains the high linkage disequilibrium. This result raises the possibility that there is a linked cluster of redox genes, and perhaps other defence-relevant genes, in the B. glabrata genome. Whether epistatic interactions for fitness actually exist among these loci still needs to be tested. However the close physical linkage among SOD1, PRX4 and CAT, and subsequent high disequilibrium, makes such interactions a plausible hypothesis.

Pathogen-associated molecular patterns activate expression of genes involved in cell proliferation, immunity and detoxification in the amebocyte-producing organ of the snail Biomphalaria glabrata

“…LPS has been found to up-regulate expression of Cu/Zn SOD in mice (Marikovsky et al, 2003) although we did not see a similar effect of LPS in the APO of B. glabrata . Previous studies have demonstrated that allelic variation at the Cu/Zn SOD locus plays an important role in susceptibility of B. glabrata to schistosome infection (Bender et al, 2007; Blouin et al, 2013; Goodall et al, 2006). Therefore, we compared our SOD nucleotide sequence (contig_1415_rc, 1364 bp) to the complete cDNA of Cu/Zn SOD1-B allele (GenBank accession number DQ239578; 3076bp) (Goodall et al, 2006).…”

Resistance of Biomphalaria glabrata 13-16-R1 snails to Schistosoma mansoni PR1 is a function of haemocyte abundance and constitutive levels of specific transcripts in haemocytes

“…Considerable advances have been made toward this goal (Bayne, 2009; Loker, 2010; Moné et al, 2010; Martins-Souza et al, 2011; Hanington et al, 2012; Mitta et al, 2012; Negrão-Corrêa et al, 2012; Blouin et al, 2013; Ittiprasert et al, 2013), yet for both the recognition and the effector phases of the snails’ defence responses, much remains to be learned. Among known facts are that snail size can influence infectivity rates: some strains of B. glabrata are susceptible as juveniles but resistant as adults (Richards et al, 1992), and larger snails exposed to S. mansoni have lower infection levels than smaller snails of the same age (Niemann and Lewis, 1990).…”

Identification and characterisation of functional expressed sequence tags-derived simple sequence repeat (eSSR) markers for genetic linkage mapping of Schistosoma mansoni juvenile resistance and susceptibility loci in Biomphalaria glabrata

“…3). From recent data showing tight linkage of gene loci associated with resistance, namely Cu–Zn superoxide dismutase (SOD), and two other genes (catalase and peroxiredoxin) of the oxidation–reduction pathway, it has been suggested there might be epistatic interactions with gene loci that are important for defense in the snail (Blouin et al, 2013). …”

“…LGs were determined using LOD thresholds ranging from 4.0 to 8.0. Map distances were calculated with the Kosambi mapping function (Blouin et al, 2013). …”