The Planorbid Snail Biomphalaria glabrata Expresses a Hemocyanin-Like Sequence in the Albumen Gland

Abstract

The parasitic flatworm Schistosoma mansoni, causative agent of human intestinal schistosomiasis in South America, relies importantly on the freshwater snail Biomphalaria glabrata as intermediate host to achieve development of cercariae that infect humans. The recommendation from the World Health Organization (WHO) to integrate snail control in efforts to counter schistosomiasis transmission provides impetus for in depth study of B. glabrata biology. Our analysis indicates that two distinct hemocyanin-like genes (hcl-1 and hcl-2) are present in B. glabrata, a snail that uses hemoglobin for oxygen transport. Characterization of BAC clones yielded the full length hcl-1 gene, which is comprised of three functional unit (FU) domains at the amino acid level. Database searches and in silico analyses identified the second hcl gene (hcl-2), composed of six FU domains. Both genes are unusual for lacking canonical residues and having fewer FU domains than typical molluscan hemocyanins that contain 7–8 FUs. Reverse transcription PCR demonstrated that Hcl-1 is expressed in a manner that correlates with reproductive maturity in the albumen gland (AG), an immune- and reproduction-relevant organ. Immune cross-reactivity with anti-keyhole limpet hemocyanin (α-KLH) antiserum and tandem-mass spectrometry validated the presence of Hcl-1 protein in the AG and egg mass fluid (EMF). The evolutionary conservation of hemocyanin-like sequences in B. glabrata in the presence of the oxygen carrier hemoglobin, combined with our results, suggest that the Hcl-1protein has a functional role in general and/or reproductive biology. Further investigations are needed to explore Hcl-1 as a potential target for snail control.

Giant African snail genomes provide insights into molluscan whole‐genome duplication and aquatic–terrestrial transition

“…Based on an analysis of orthologous genes and phylogenetics, haemocyanin genes were observed in all six species (including B. glabrata ), indicating that B. glabrata not only possesses haemoglobin genes but also possesses haemocyanin genes. However, the B. glabrata haemocyanin is composed of only six functional units, compared to eight functional units in the other five species, indicating some level of function loss (Lieb et al., 2006; Markl, 2013; Peña & Adema, 2016). Notably, there are four haemocyanin genes in both A. immaculata and A. fulica , which is twice as many as in any other Gastropoda species (Figure 5a).…”

A Targeted Capture Linkage Map Anchors the Genome of the Schistosomiasis Vector Snail, Biomphalaria glabrata

“…LD, linkage disequilibrium.aLarson et al (2014).bMitta et al (2005).cAdema et al (2017).dPila et al (2016b).eZhang and Coultas (2011).fBaričević et al (2015).gLéonard et al (2001).hTennessen et al (2015b).iPeña and Adema (2016).jTennessen et al (2015a).kAllan et al (2017).lPila et al (2016a).mGoodall et al (2006).nBlouin et al (2013).oGalinier et al (2013).pHannington et al (2012).qKnight et al (1999).…”

Hemocyanin of the caenogastropod Pomacea canaliculata exhibits evolutionary differences among gastropod clades

“…coding regions. This feature was described only in two, non-functional, hemocyanin-like genes from the albumen gland of the pulmonate Biomphalaria glabrata where intron gain in the ancestral Hc genes may have provided them with novel functions [43], as it is believed to occur in paralogous gene families during evolutionary transitions [44]. The PcH TEM micrographs showed the typical cylindrical structure organization of snail Hc in di, tri and tetra-decamers with an internal collar structure, being the di-and tri- decameric cylinders the most abundant ones.…”