Characterization of hemolymph phenoloxidase activity in two Biomphalaria snail species and impact of Schistosoma mansoni infection

Clec’h, Winka Le; Anderson, Timothy J.; Chevalier, Frédéric D.

doi:10.1186/s13071-016-1319-6

Cited by 57 publications

(59 citation statements)

References 59 publications

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“…mansoni sporocysts, and the cercariae developing within them, express a diverse array of proteases, including elastases and leishmanolysins [24,37], with likely functions in disabling snail defenses, dissolution of snail tissues to provide living space, facilitating intrasnail migration of sporocysts and for packaging in cercariae which use them both for exiting the snail host and entering the mammalian definitive host. Protease inhibitors are also produced and likely counteract proteases that the snail expresses late in infection [24,38].…”

Section: Resultsmentioning

confidence: 99%

Transcriptional responses ofBiomphalaria pfeifferiandSchistosoma mansonifollowing exposure to niclosamide, with evidence for a synergistic effect on snails following exposure to both stressors

Buddenborg¹,

Kamel²,

Zhang³

et al. 2018

Preprint

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BackgroundSchistosomiasis is one of the world's most common NTDs. Successful control operations often target snail vectors with the molluscicide niclosamide. Little is known about how niclosamide affects snails, including for Biomphalaria pfeifferi, the most important vector for Schistosoma mansoni in Africa. We used Illumina technology to explore how field-derived B. pfeifferi, either uninfected or harboring cercariae-producing S. mansoni sporocysts, respond to a sublethal exposure of niclosamide. This study afforded the opportunity to determine if snails respond differently to biotic or abiotic stressors, and if they reserve unique responses for when presented with both stressors in combination. We also examined how sporocysts respond when their snail host is exposed to niclosamide. Principal FindingsCercariae-producing sporocysts within snails exposed to niclosamide express ~68% of the genes in the S. mansoni genome, as compared to 66% expressed by intramolluscan stages of S. mansoni in snails not exposed to niclosamide. Niclosamide does not disable sporocysts nor does it seem to provoke from them distinctive responses associated with detoxifying a xenobiotic. For B. pfeifferi, niclosamide treatment alone increases expression of several features not up-regulated in infected snails including particular cytochrome p450s and heat shock proteins, glutathione-S-transferases, antimicrobial factors like LBP/BPI and protease inhibitors, and also provokes strong down regulation of proteases. Exposure of infected snails to niclosamide resulted in numerous up-regulated responses associated with apoptosis along with down-regulated ribosomal and defense functions, indicative of a distinctive, compromised state not achieved with either stimulus alone. Conclusions/SignificanceThis study helps define the transcriptomic responses of an important and under-studied schistosome vector to S. mansoni sporocysts, to niclosamide, and to both in combination. It suggests the response of S. mansoni sporocysts to niclosamide is minimal and not reflective of a distinct repertoire of genes to handle xenobiotics while in the snail host. It also offers new insights for how niclosamide affects snails. AUTHOR'S SUMMARYSchistosomaisis control programs often employ the use of chemical molluscicides, such as niclosamide, to control the obligatory intermediate snail hosts. Despite its widespread use, we know little about how niclosamide affects snails like Biomphalaria pfeifferi, the most important vector Schistosoma mansoni in Africa. By sequencing the transcriptomes of uninfected and S. mansoni-infected B. pfeifferi exposed to niclosamide, we analyze the snail's response to both biotic and abiotic stressors. We can also examine the response of S. mansoni to niclosamide exposure during intramolluscan development. Biomphalaria pfeifferi snails exposed only to niclosamide showed unique up-regulation of stress and defense-related transcripts not seen in snails infected with a biotic, like S. mansoni infection, alone. Schistosoma mansoni-infected B. ...

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Section: Resultsmentioning

confidence: 99%

Transcriptional responses ofBiomphalaria pfeifferiandSchistosoma mansonifollowing exposure to niclosamide, with evidence for a synergistic effect on snails following exposure to both stressors

Buddenborg¹,

Kamel²,

Zhang³

et al. 2018

Preprint

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“…It is, for example, possible that some localized immune responses in the target tissue of the parasite (i.e. hepatopancreas/digestive gland) determine the infection success and that their levels differ from those in the hemolymph (Tzou et al, 2000;Pulpitel, Pernice, Simpson, & Ponton, 2015; but see Galinier et al, 2013). Localized responses could also be highly beneficial by reducing the energetic costs of immune activation and by limiting self-harm commonly associated with immune defense (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…The examined immune parameters are central in the immune system of invertebrates, including mollusks (e.g. Butt & Raftos, ; Hellio, Bado‐Nilles, Gagnaire, Renault, & Thomas‐Guyon, ; Le Clec'h, Anderson, & Chevalier, ; Mitta, Vandenbulcke, & Roch, ), and are known to respond to various immune elicitors (Seppälä & Leicht, ) as well as to be subject to natural selection in L. stagnalis (Langeloh et al., ). It is, however, important to note that the role of these traits in determining resistance against E. aconiatum is not known.…”

Section: Methodsmentioning

confidence: 99%

Relative importance of chemical attractiveness to parasites for susceptibility to trematode infection

Langeloh

Seppälä

2018

Ecology and Evolution

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While the host immune system is often considered the most important physiological mechanism against parasites, precontact mechanisms determining exposure to parasites may also affect infection dynamics. For instance, chemical cues released by hosts can attract parasite transmission stages. We used the freshwater snail Lymnaea stagnalis and its trematode parasite Echinoparyphium aconiatum to examine the role of host chemical attractiveness, physiological condition, and immune function in determining its susceptibility to infection. We assessed host attractiveness through parasite chemo‐orientation behavior; physiological condition through host body size, food consumption, and respiration rate; and immune function through two immune parameters (phenoloxidase‐like and antibacterial activity of hemolymph) at an individual level. We found that, although snails showed high variation in chemical attractiveness to E. aconiatum cercariae, this did not determine their overall susceptibility to infection. This was because large body size increased attractiveness, but also increased metabolic activity that reduced overall susceptibility. High metabolic rate indicates fast physiological processes, including immune activity. The examined immune traits, however, showed no association with susceptibility to infection. Our results indicate that postcontact mechanisms were more likely to determine snail susceptibility to infection than variation in attractiveness to parasites. These may include localized immune responses in the target tissue of the parasite. The lack of a relationship between food consumption and attractiveness to parasites contradicts earlier findings that show food deprivation reducing snail attractiveness. This suggests that, although variation in resource level over space and time can alter infection dynamics, variation in chemical attractiveness may not contribute to parasite‐induced fitness variation within populations when individuals experience similar environmental conditions.

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“…In week 7, 3 days after the last cercarial shedding, we collected hemolymph as described in Le Clec’h et al, 2016 [18] from all surviving snails infected with SmLE (HS) and SmBRE (LS), as well as from uninfected Bg26 controls maintained under the same conditions. We measured both laccase-like activity (phenoloxydase (PO) activity, known to be involved in invertebrate immunity) and the hemoglobin (protein carrying oxygen in B. glabrata hemolymph) rates in the hemolymph of each snail infected with SmLE (HS), SmBRE (LS) or uninfected control.…”

Section: Methodsmentioning

confidence: 99%

“…We measured the total laccase-like activity as described in Le Clec’h et al, 2016 [18]. In brief, we combined 10 µL of freshly collected hemolymph to 40 µL of cacodylate buffer and 40 µL of bovine trypsin (1mg/mL) in a 96-well optical plate (Corning).…”

Section: Methodsmentioning

confidence: 99%

Striking differences in virulence, transmission, and sporocyst growth dynamics between two schistosome populations

Clec’h

Diaz

Chevalier

et al. 2019

Preprint

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BackgroundParasite traits associated with transmission success, such as the number of infective stages released from the host, are expected to be optimized by natural selection. However, in the trematode parasite Schistosoma mansoni, a key transmission trait – the number of cercariae larvae shed from infected Biomphalaria spp. snails – varies significantly within and between different parasite populations and selection experiments demonstrate that this variation has a strong genetic basis. In this study, we compared the transmission strategies of two laboratory schistosome population and their consequences for their snail host.MethodsWe infected inbred Biomphalaria glabrata snails using two Schistosoma mansoni parasite populations (SmBRE and SmLE), both isolated from Brazil and maintained in the laboratory for decades. We compared life history traits of these two parasite populations by quantifying sporocyst growth within infected snails (assayed using qPCR), output of cercaria larvae, and impact on snail host physiological response (i.e. hemoglobin rate, laccase-like activity) and survival.ResultsWe identified striking differences in virulence and transmission between the two studied parasite populations. SmBRE (low shedder (LS) parasite population) sheds very low numbers of cercariae, and causes minimal impact on the snail physiological response (i.e. laccase-like activity, hemoglobin rate and snail survival). In contrast, SmLE (high shedder (HS) parasite population) sheds 8-fold more cercariae (mean ± se cercariae per shedding: 284±19 vs 2352±113), causes high snail mortality, and has strong impact on snail physiology. We found that HS sporocysts grow more rapidly inside the snail host, comprising up to 60% of cells within infected snails, compared to LS sporocysts which comprised up to 31%. Cercarial production is strongly correlated to the number of S. mansoni sporocyst cells present within the snail host tissue, although the proportion of sporocyst cells alone does not explain the low cercarial shedding of SmBRE.ConclusionsWe demonstrated the existence of alternative transmission strategies in the S. mansoni parasite consistent with trade-offs between parasite transmission and host survival: a “boom-bust” strategy characterized by high virulence, high transmission and short duration infections and a “slow and steady” strategy with low virulence, low transmission but long duration of snail host infections.

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Characterization of hemolymph phenoloxidase activity in two Biomphalaria snail species and impact of Schistosoma mansoni infection

Cited by 57 publications

References 59 publications

Transcriptional responses ofBiomphalaria pfeifferiandSchistosoma mansonifollowing exposure to niclosamide, with evidence for a synergistic effect on snails following exposure to both stressors

Transcriptional responses ofBiomphalaria pfeifferiandSchistosoma mansonifollowing exposure to niclosamide, with evidence for a synergistic effect on snails following exposure to both stressors

Relative importance of chemical attractiveness to parasites for susceptibility to trematode infection

Striking differences in virulence, transmission, and sporocyst growth dynamics between two schistosome populations

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