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Schematic representation of Pomacea canaliculata responses to different periods of estivation (7 and 45 days). Unknown mechanisms have been represented with a question mark.
Source publication
Long-term estivation (45 days) in the apple snail Pomacea canaliculata induces an increase of non-enzymatic antioxidants, such as uric acid and reduced glutathione (GSH), which constitutes an alternative to the adaptive physiological strategy of preparation for oxidative stress (POS). Here, we studied markers of oxidative stress damage, uric acid l...
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Methods
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Studies on oxidative stress physiology on molluscs to monitor the aquatic environment, influenced by pollutants and stressors are very limited in general and in Indian apple snails, P. globosa in particular. The main focus of the present study was to establish the baseline data on a redox regulatory system in P. globosa sampled across the Indian su...
Citations
... Past studies on the tolerance of the apple snail to air exposure have focused on physiology, biochemistry, and behavior 14 . Studies have been conducted to induce dormancy in apple snails by air exposure stress, observed behavioral changes and examined the peroxide and antioxidant contents 8,15 . The results of the study revealed that uric acid acts as a non-enzymatic antioxidant during dormancy in apple snails. ...
The apple snail, Pomacea canaliculata (Lamarck, 1819), a freshwater snail listed as a pernicious invasive alien species by the World Conservation Union (IUCN), has caused serious agricultural and ecological harm worldwide. This species has inflicted significant agricultural and ecological damage on a global scale. Under conditions of extreme environmental stress, the apple snail enters a state of dormancy and remains in this dormant phase until environmental conditions become favorable again, which serves as a crucial survival strategy. In our study, we subjected apple snails to 30 days of air-exposure stress followed by rehydration to reactivate them. Our objective was to elucidate the underlying mechanisms associated with drought tolerance, dormancy, and subsequent arousal based on transcriptomic analyses. The results indicated that the groups subjected to 5-, 15- and 30-day air-exposure stress treatments (DRY05, DRY15 and DRY30) exhibited a general down-regulation of metabolism-related pathways. These pathways included starch and sucrose metabolism, linoleic acid metabolism, glutathione metabolism and glycosaminoglycan degradation, compared with the control (CK). In addition, the weighted correlation network analysis (WGCNA) identified two critical pathways: toll-like receptor signaling pathway and adherens junction. The down-regulation of these pathways indicated a decrease in immune levels during dormancy in apple snails. This may further lead to the inhibition of apoptosis and a reduction in energy expenditure, thereby sustaining vital activities. The up-regulation of intercellular adhesion and immune-related pathways upon reawakening (RCY01) further substantiates the presence of this tolerance mechanism during dormancy in the apple snail. This study provides a reference for understanding the tolerance of apple snails to extreme environments, and provides a basic theory for apple snail biocontrol research.
... Past studies on the tolerance of the apple snail to air exposure have focused on physiology, biochemistry, and behavior 14 . Studies have been conducted to induce dormancy in apple snails by air exposure stress, observed behavioral changes and examined the peroxide and antioxidant contents 8, 15 . ...
The apple snail ( Pomacea canaliculata ), a freshwater snail listed as a pernicious invasive alien species by the World Conservation Union (IUCN), has caused serious agricultural and ecological harm worldwide. The species enters dormancy under extreme environmental stress and does not lift the dormant state until the environment is suitable, which is an important survival strategy. In order to investigate its survival mechanism under environmental stress conditions, the present study was carried out to investigate the response of apple snails to air exposure stress through air exposure stress treatment and transcriptome analysis, using apple snails living normally under water conditions as control (CK), and to excavate the relevant mechanisms regulating their drought tolerance, dormancy and arousal. The results showed that the 5-, 15- and 30-day air-exposure stress treatment groups (DRY05, DRY15 and DRY30) showed a general down-regulation of metabolism-related pathways, including starch and sucrose metabolism, linoleic acid metabolism, glutathione metabolism and glycosaminoglycan degradation, compared with the CK group. Moreover, Apoptosis, intercellular adhesion, insulin resistance, and immune status of apple snails were also significantly changed during dormancy. These changes help the apple snail to reduce energy expenditure and maintain vital activities. In addition, this study found that pathways related to cell cycle, immune signalling and intercellular adhesion were significantly affected when apple snails enter dormancy (DRY01) and arousal (RCY01). This study provides a reference for understanding the tolerance of apple snails to extreme environments, and provides a basic theory for apple snail biocontrol research.
... As such, redox signaling senses, adapts to and communicates changes in metabolism [31]. Consequently, numerous studies have explored how redox metabolism is influenced by or influences substantial shifts in metabolic rate, such as diapause [32,33], estivation [34][35][36], and hibernation [37][38][39], often observing the activation of endogenous antioxidants [29,40]. On the other hand, the metamorphosis of holometabolous insects is a phenomenon characterized by a decline and recovery of metabolism that, despite resembling other metabolic suppression situations, remains underexplored from a redox perspective. ...
Complete insect metamorphosis requires substantial metabolic and physiological adjustments. Although oxidative stress has been implicated in metamorphosis, details on redox metabolism during larva-to-pupa and pupa-to-adult remain scarce. This study explores redox metabolism during metamorphosis of a lepidopteran (Chlosyne lacinia), focusing on core metabolism, antioxidant systems and oxidative stress. The larva-to-pupa transition was characterized by increased lactate dehydrogenase and glutathione peroxidase (GPX) activities, coupled with depletion of reduced glutathione (GSH), high disulfide-to-total-glutathione ratio (GSSG/tGSH), and increased lipid peroxidation. As metamorphosis progressed, metabolic enzyme activities, citrate synthase and glucose 6-phosphate dehydrogenase increased, indicating heightened oxidative metabolism associated with adult development. Concurrently, GSH and GPX levels returned to larval levels and GSSG/tGSH reached its most reduced state right before adult emergence. Adult emergence was marked by a further increase in oxidative metabolism, accompanied by redox imbalance and enhanced antioxidant mechanisms. These findings highlight a fluctuation in redox balance throughout metamorphosis, with periods of oxidative eustress followed by compensatory antioxidant responses. This study is the first to identify concurrent changes in metabolism, antioxidants, redox balance and oxidative stress throughout metamorphosis. Our findings extend knowledge on redox metabolism adjustments and highlight redox adaptations and oxidative stress as natural components of complete insect metamorphosis.
... 55,56 Previous research has shown that apple snails exhibit increased activities of SOD (superoxide dismutase) and CAT (catalase) in their tissues after a short period (7 days) of dormancy. 57 In this study, the POD activity in P. canaliculata rapidly increased upon entering hibernation. However, after a longer period of acclimation (60 days), the POD activity decreased at 90th and 120th days compared with that at 60th day ( Fig. 6(h)). ...
BACKGROUND
The invasive freshwater snail Pomacea canaliculata is an agricultural pest with a certain level of tolerance to abiotic stress. After the harvest of late rice, the snails usually burrow themselves into the soil surface layers to overwinter and pose a renewed threat to rice production in the following year. Revealing the response of snails to environmental stresses is crucial for developing countermeasures to control their damage and spread.
RESULTS
In this study, we conducted a 120‐day in situ experiment during the winter to investigate the survival and physiological changes of hibernating snails in 0‐5 and 5‐10 cm soil depths, aiming to explore their overwintering strategies. Our results showed that 73.61%, 87.50%, and 90.28% of male, female, and juvenile snails survived after hibernation for 120 days in 0–10 cm soil depth, respectively. The differences in survival rates based on sex and size of snails potentially reflect the countermeasures of snails to rapidly reproduce after hibernation. Simultaneously, the hibernating snails exhibited the ability to maintain a certain level of body weight. During this period, the snails increased their antioxidant enzyme activities to cope with oxidative stress, and enhanced their lipid storage. The hibernation survival of snails was not significantly affected by different soil depths, indicating that they have the potential to hibernate into deeper soils. Furthermore, snails were capable of increasing their contents of bound water and glycerol to cope with sudden cold spells during hibernation.
CONCLUSION
Our findings emphasize the adaptive changes of P. canaliculata snails overwintering in paddy soils. In future studies, the vulnerabilities of P. canaliculata during hibernation (e.g. shell characteristics, nutrient reserves, and dehydration tolerance, etc.,) should be investigated to develop effective control methods for this period. © 2024 Society of Chemical Industry.
... For example, estivating pulmonate snails (Otala lactea) arouse rapidly, within 20 min to a few hours after an increase in relative humidity (Herreid, 1977). Arousal is associated with rapid (within 10 min) upregulation of enzymes associated with ATP synthesis and an increase in reactive oxygen species (Storey, 2001;Giraud-Billoud et al., 2022). Estivating cocooned frogs similarly arouse within an hour or so of being moistened (Withers, pers. ...
... It seems that B. tenagophila conforms to the general strategy of POS exhibited in various anoxia-and hypoxia-tolerant animals (Hermes-Lima et al., 1998Hermes-Lima and Zenteno-Savın, 2002). However, Giraud-Billoud et al. (2022) reported that the changes in the levels of uric acid and reduced glutathione (GSH) in the snail Pomacea canaliculata (Lamarck, 1819) during long-term aestivation might indicate a non-enzymatic antioxidants mechanism, alternative to POS. ...
... Hsp70 and Hsp90 may also act as molecular chaperones during summer dormancy, protecting the proteome and providing long-term metabolic stability [13,125]. In a recent study, Giraud-Billoud et al. found that FOXO expression was upregulated during aestivation, suggesting a potential role in POS strategies [126]. Similarly, Sun et al. investigated changes in the expression of enzymes and antioxidant genes in freshwater snails during aestivation and awakening using proteomic methods. ...
Aestivation is considered to be one of the “purest” hypometabolic states in nature, as it involves aerobic dormancy that can be induced and sustained without complex factors. Animals that undergo aestivation to protect themselves from environmental stressors such as high temperatures, droughts, and food shortages. However, this shift in body metabolism presents new challenges for survival, including oxidative stress upon awakening from aestivation, accumulation of toxic metabolites, changes in energy sources, adjustments to immune status, muscle atrophy due to prolonged immobility, and degeneration of internal organs due to prolonged food deprivation. In this review, we summarize the physiological and metabolic strategies, key regulatory factors, and networks utilized by aestivating animals to address the aforementioned components of aestivation. Furthermore, we present a comprehensive overview of the advancements made in aestivation research across major species, including amphibians, fish, reptiles, annelids, mollusks, and echinoderms, categorized according to their respective evolutionary positions. This approach offers a distinct perspective for comparative analysis, facilitating an understanding of the shared traits and unique features of aestivation across different groups of organisms.
... In P. canaliculata, the involvement of nitrogen compounds in the anti-oxidant response associated with the arousal from estivation has been documented in detail. In agreement with the observations from A. fulica, the P. canaliculata presented a complex pattern of anti-oxidant responses that involved enzymatic and non-enzymatic components which fluctuated in an organ-specific fashion, especially during the arousal [81]. The nitrogen compound uric acid is likely to play an important role in buffering the ROS concentration increase during the arousal [82]. ...
Reactive oxygen species (ROS) are volatile and short-lived molecules playing important roles in several physiological functions, including immunity and physiological adaptation to unsuitable environmental conditions. In an eco-immunological view, the energetic costs associated with an advantageous metabolic apparatus able to cope with wide changes in environmental parameters, e.g., temperature range, water salinity or drought, could be further balanced by the advantages that this apparatus may also represent in other situations, e.g., during the immune response. This review provides an overview of molluscs included in the IUCN list of the worst invasive species, highlighting how their relevant capacity to manage ROS production during physiologically challenging situations can also be advantageously employed during the immune response. Current evidence suggests that a relevant capacity to buffer ROS action and their damaging consequences is advantageous in the face of both environmental and immunological challenges, and this may represent a trait for potential invasiveness. This should be considered in order to obtain or update information when investigating the potential of the invasiveness of emerging alien species, and also in view of ongoing climate changes.
... Besides, U may deplete reduced glutathione, as was reported in isolated hepatocytes from laboratory rat (Rattus norvegicus, Pourahmad et al., 2011) and zebrafish (Danio rerio, Barillet et al., 2011). Given that the three elements produce an oxidative imbalance in the digestive gland of P. canaliculata, snails may effectively delay or attenuate lipid peroxidation and protein damage activating its cellular antioxidant machinery, as occurs against other environmental stressors such as low temperature, desiccation, or xenobiotics (Giraud-Billoud et al., 2011;Giraud-Billoud et al., 2013;Giraud-Billoud et al., 2018;Giraud-Billoud et al., 2022). In the next paragraphs, we discuss the importance and effectiveness of each antioxidant defense during oxidative imbalance. ...
... CAT is an antioxidant enzyme that catalyzes the reduction of intracellular H 2 O 2 to water and oxygen (Orbea et al., 2000), thus counteracting the activity of H 2 O 2 -generating oxidases. The role of CAT, as an enzymatic antioxidant protective mechanism in P. canaliculata, has recently been characterized in models of acute stress where reactivation after hypometabolism induced by estivation or hibernation is related to increases in its expression and activity (Sun et al., 2019;Giraud Billoud et al., 2022;Rodriguez et al., 2023). However, the enzymatic activity of CAT remains approximately constant (with some small variations in U-exposed snails), even though the nonenzymatic antioxidant defenses partially counteract RS and protein damage. ...
The freshwater gastropod Pomacea canaliculata fulfills the ideal conditions of a bioindicator species since its digestive gland bioconcentrates elements toxic for human and ecosystems health. The aim of this work was to study the balance between production of free radicals and antioxidant defenses, and the generation of oxidative damage in the digestive gland of this mollusk after exposure (96 h) to three elements with differential affinities for functional biological groups: mercury (5.5 μg/L of Hg⁺² as HgCl2), arsenic [500 μg/L of (AsO4)⁻³ as Na3AsO47H2O], or uranium [700 μg/L of (UO2)⁺² as UO2(CH2COOH)2]. Bioconcentration factors of Hg, As, and U were 25, 23, and 53, respectively. Snails exhibited a sustained increase of reactive species (RS), and protein and lipid damage. Lipid radicals increased between 72 and 96 h, respectively, in snails exposed to U and Hg while this parameter changed early (24 h) in As- exposed snails. Snails showed protein damage, reaching maximum values at different endpoints. This redox disbalance was partially compensated by non-enzymatic antioxidant defenses α-tocopherol (α-T), β-carotene (β-C), uric acid, metallothionein (MTs). Snails consumed α-T and β-C in an element-dependent manner. The digestive gland consumed rapidly uric acid and this molecule was not recovered at 96 h. Digestive gland showed a significant increase in MTs after elemental exposure at different endpoints. The enzymatic antioxidant defenses, represented by the catalase and glutathione-S-transferase activities, seems to be not necessary for the early stages of the oxidative process by metals. This work is the first attempt to elucidate cellular mechanisms involved in the tolerance of this gastropod to non-essential elements. The bioconcentration factors and changes in the oxidative status and damage confirm that this species can be used as a bioindicator species of metal pollution in freshwater bodies.
... Thus, animals comprised five groups: (1) control (active), (2) estivation (est), (3) arousal-est, (4) hibernation (hib), and (5) arousal-hib. Our laboratory has previously characterized the experimental inductions of activity-dormancy-arousal cycles [11][12][13]21]. ...
... The apple snail P. canaliculata shows notable adaptations, such as the possibility of estivating and hibernating to tolerate seasonal activity-dormancy-arousal cycles [10]. In this way, the POS strategy is used by this species to avoid damage to vital cellular components by free radicals in tissues [13,15]. Until now, in those gastropods where the use of the POS strategy has been described (i.e., reported ten species, [11][12][13][40][41][42][43][44][45][46][47][48][49][50][51][52][53][54]), the experimental tests have been carried out on tissue extracts, not taking into account the changes occurring in compounds and cells from the blood. ...
... In this way, the POS strategy is used by this species to avoid damage to vital cellular components by free radicals in tissues [13,15]. Until now, in those gastropods where the use of the POS strategy has been described (i.e., reported ten species, [11][12][13][40][41][42][43][44][45][46][47][48][49][50][51][52][53][54]), the experimental tests have been carried out on tissue extracts, not taking into account the changes occurring in compounds and cells from the blood. In this study, we described, for the first time in a freshwater gastropod under laboratory conditions of estivation and hibernation, modifications in blood compounds and antioxidants, and changes in the circulating hemocytes. ...
States of natural dormancy include estivation and hibernation. Ampullariids are exemplary because they undergo estivation when deprived of water or hibernation when exposed to very low temperatures. Regardless of the condition, ampullariids show increased endogenous antioxidant defenses, anticipating the expected respiratory burst during reoxygenation after reactivation, known as “Preparation for Oxidative Stress (POS)”. In this work, we tested the POS hypothesis for changes in the blood and hemocytes of the bimodal breather Pomacea canaliculata (Ampullariidae) induced at experimental estivation and hibernation. We described respiratory (hemocyanin, proteins, lactate), antioxidant (GSH, uric acid, SOD, CAT, GST), and immunological (hemocyte levels, ROS production) parameters. We showed that, although the protein level remains unchanged in all experimental groups, hemocyanin increases in response to estivation. Furthermore, lactate remains unchanged in challenged snails, suggesting an aerobic metabolism during short-term challenges. Blood uric acid increases during estivation and arousal from estivation or hibernation, supporting the previously proposed antioxidant role. Regarding hemocytes, we showed that the total population increases with all challenges, and granulocytes increase during hibernation. We further showed that hibernation affects ROS production by hemocytes, possibly through mitochondrial inhibition. This study contributed to the knowledge of the adaptive strategies of ampullariids to tolerate adverse environmental conditions.
