Multiple strategies of schistosomes to meet their requirements in the intermediate snail host

Abstract

The results of the studies on our model combination Trichobilharzia ocellata-Lymnaea stagnalis, presented in this review, lead to the conclusion that schistosomes use multiple strategies to reach their goals, i.e. to propagate and to continue their life cycle. They have to escape from being attacked by the internal defence system (IDS) of the snail host and to profoundly affect the host's energy flow, of which reproduction and growth are the main determinants, for their own benefit. These physiological changes they establish mainly by interfering with the two regulatory systems in the snail host, the IDS and the neuroendocrine system (NES). Moreover, these two regulatory systems clearly interact with each other. Parasitic E\S products affect the host's IDS both in a direct and an indirect way. The neuropeptides or neuropeptide-like substances that are secreted by parasite glands into the host directly suppress haemocyte activity in the snail. The indirect effects include effects of (1) peptides from connective tissue cells and (2) neuropeptides from NES and\or IDS. Parasitic E\S products also induce the effects on energy flow in the host. These E\S products act either directly on a target, as shown for the inhibiting effect of the parasite on the development of the male copulation organ, or on the NES regulating reproductive activity, e.g. on gene expression. Indirect effects of E\S products on the NES (hormone-receptor interaction, electrical activity) are mediated by a factor from connective tissue cells, presumably belonging to the IDS. The physiological changes in the snail host are obviously of vital importance for the parasites, since they make use of different strategies to bring them about.

Avian Schistosomes and Outbreaks of Cercarial Dermatitis

“…Both molecules, produced in L. stagnalis by granular cells of connective tissue, are related to phagocytic activity of hemocytes. MDM enhances phagocytosis of hemocytes, and the expression of a corresponding gene for MDM is downregulated in L. stagnalis infected with T. szidati (159,161). In contrast, treatment of hemocytes with granularin decreases phagocytic activity, and the encoding gene is upregulated in parasitized snails (160,161).…”

“…In the snail host, avian schistosomes also interfere with metabolism, such as causing abnormal body growth, and endocrine functions, such as causing a reduction of egg laying (161). In L. stagnalis, these processes are regulated by neuroendocrine cells in the central nervous system (CNS) (162,163).…”

“…Other neuropeptides (FMRFamide-related peptides) are also upregulated during infection of L. stagnalis by T. szidati, and these peptides, via inhibition of neuroendocrine cells, may be responsible for the suppression of snail metabolism and reproduction (167). All these changes in infected snails may provide energy resources and space that can be exploited by the schistosomes for development (145,161).…”

Parasites: evolution’s neurobiologists

“…One plausible example of this is the effects of the schistosome parasite Tricholbilharzia ocellata on its snail host, Lymnaea stagnalis. The parasite secretes/excretes compounds that interfere with host immune function, allowing the survival of the parasite within the host (de Jong-Brink et al, 1997;de Jong-Brink et al, 2001). Infection also leads to a reduction in egg-laying in the snail, and the energy the host would have invested in reproduction is redirected to support parasitic growth (de Jong-Brink et al, 2001).…”

Disruption of amylase genes by RNA interference affects reproduction in the Pacific oyster Crassostrea gigas

“…Among these, neuropeptide Y or gonadotropin-releasing hormones act as a switch for nutritional status and reproduction, as demonstrated in vertebrates (e.g. Kalra and Kalra, 2004;Temple et al, 2003) and suggested in invertebrates (de Jong-Brink et al, 2001;Bigot et al, 2012Bigot et al, , 2014. Therefore, these neuropeptides represent a possible line of investigation into differences in reproductive strategy depending on modification in energy input from environmental and/or endogenous variations, whether natural or induced in the laboratory.…”