Yolk proteins of the schistosomiasis vector snail Biomphalaria glabrata revealed by multi-omics analysis

Abstract

Vitellogenesis is the most important process in animal reproduction, in which yolk proteins play a vital role. Among multiple yolk protein precursors, vitellogenin (Vtg) is a well-known major yolk protein (MYP) in most oviparous animals. However, the nature of MYP in the freshwater gastropod snail Biomphalaria glabrata remains elusive. In the current study, we applied bioinformatics, tissue-specific transcriptomics, ovotestis-targeted proteomics, and phylogenetics to investigate the large lipid transfer protein (LLTP) superfamily and ferritin-like family in B. glabrata. Four members of LLTP superfamily (BgVtg1, BgVtg2, BgApo1, and BgApo2), one yolk ferritin (Bg yolk ferritin), and four soma ferritins (Bg ferritin 1, 2, 3, and 4) were identified in B. glabrata genome. The proteomic analysis demonstrated that, among the putative yolk proteins, BgVtg1 was the yolk protein appearing in the highest amount in the ovotestis, followed by Bg yolk ferritin. RNAseq profile showed that the leading synthesis sites of BgVtg1 and Bg yolk ferritin are in the ovotestis (presumably follicle cells) and digestive gland, respectively. Phylogenetic analysis indicated that BgVtg1 is well clustered with Vtgs of other vertebrates and invertebrates. We conclude that, vitellogenin (BgVtg1), not yolk ferritin (Bg yolk ferritin), is the major yolk protein precursor in the schistosomiasis vector snail B. glabrata.

Different metazoan parasites, different transcriptomic responses, with new insights on parasitic castration by digenetic trematodes in the schistosome vector snail Biomphalaria glabrata

“…Additionally, genes associated with ovarian development in other molluscs were down-regulated in our snails at 2 or 8dpi with trematodes (Table S18 ), and other genes implicated in sexual differentiation [ 67 ] also showed a general pattern of down-regulation in our results (Table S18 ). Notable among the genes down-regulated were the major yolk proteins vitellogenin-4 (by all 3 parasites at 2 and 8dpi), vitellogenin A2 (by E. paraensei at 40dpi), and yolk ferritin (by S. mansoni at 8d and D. potomaca at 2d), the former two produced in the ovary and the latter in the digestive gland [ 68 ].…”