Marine organisms need to adapt in order to cope with the adverse effects of ocean acidification and warming. Transgenerational exposure to CO2 stress has been shown to enhance resilience to ocean acidification in offspring from a number of species. However, the molecular basis underlying such adaptive responses is currently unknown. Here, we compared the transcriptional profiles of two genetically distinct oyster breeding lines following transgenerational exposure to elevated CO2 in order to explore the molecular basis of acclimation or adaptation to ocean acidification in these organisms. The expression of key target genes associated with antioxidant defence, metabolism and the cytoskeleton was assessed in oysters exposed to elevated CO2 over three consecutive generations. This set of target genes was chosen specifically to test whether altered responsiveness of intracellular stress mechanisms contributes to the differential acclimation of oyster populations to climate stressors. Transgenerational exposure to elevated CO2 resulted in changes to both basal and inducible expression of those key target genes (e.g. ecSOD, catalase and peroxiredoxin 6), particularly in oysters derived from the disease-resistant, fast-growing B2 line. Exposure to CO2 stress over consecutive generations produced opposite and less evident effects on transcription in a second population that was derived from wild-type (nonselected) oysters. The analysis of key target genes revealed that the acute responses of oysters to CO2 stress appear to be affected by population-specific genetic and/or phenotypic traits and by the CO2 conditions to which their parents had been exposed. This supports the contention that the capacity for heritable change in response to ocean acidification varies between oyster breeding lines and is mediated by parental conditioning.
Antilipopolysaccharide factors (ALFs) have been described as highly cationic polypeptides with a broad spectrum of potent antimicrobial activities. In addition, ALFs have been shown to recognize LPS, a major component of the Gram-negative bacteria cell wall, through conserved amino acid residues exposed in the four-stranded β-sheet of their three dimensional structure. In penaeid shrimp, ALFs form a diverse family of antimicrobial peptides composed by three main variants, classified as ALF Groups A to C. Here, we identified a novel group of ALFs in shrimp (Group D ALFs), which corresponds to anionic polypeptides in which many residues of the LPS binding site are lacking. Both Group B (cationic) and Group D (anionic) shrimp ALFs were produced in a heterologous expression system. Group D ALFs were found to have impaired LPS-binding activities and only limited antimicrobial activity compared to Group B ALFs. Interestingly, all four ALF groups were shown to be simultaneously expressed in an individual shrimp and to follow different patterns of gene expression in response to a microbial infection. Group B was by far the more expressed of the ALF genes. From our results, nucleotide sequence variations in shrimp ALFs result in functional divergence, with significant differences in LPS-binding and antimicrobial activities. To our knowledge, this is the first functional characterization of the sequence diversity found in the ALF family.
Some populations of marine organisms appear to have inherent tolerance or the capacity for acclimation to stressful environmental conditions, including those associated with climate change. Sydney rock oysters from the B2 breeding line exhibit resilience to ocean acidification (OA) at the physiological level. To understand the molecular basis of this physiological resilience, we analysed the gill transcriptome of B2 oysters that had been exposed to near-future projected ocean pH over two consecutive generations. Our results suggest that the distinctive performance of B2 oysters in the face of OA is mediated by the selective expression of genes involved in multiple cellular processes. Subsequent high-throughput qPCR revealed that some of these transcriptional changes are exclusive to B2 oysters and so may be associated with their resilience to OA. The intracellular processes mediated by the differentially abundant genes primarily involve control of the cell cycle and maintenance of cellular homeostasis. These changes may enable B2 oysters to prevent apoptosis resulting from oxidative damage or to alleviate the effects of apoptosis through regulation of the cell cycle. Comparative analysis of the OA conditioning effects across sequential generations supported the contention that B2 and wild-type oysters have different trajectories of changing gene expression and responding to OA. Our findings reveal the broad set of molecular processes underlying transgenerational conditioning and potential resilience to OA in a marine calcifier. Identifying the mechanisms of stress resilience can uncover the intracellular basis for these organisms to survive and thrive in a rapidly changing ocean.
Infectious diseases represent the most serious threat to shrimp farming worldwide. Understanding the molecular mechanisms driving shrimp-pathogen interactions is necessary for developing strategies to control disease outbreaks in shrimp production systems. In the current study, we experimentally reproduced mortality events using standardized infections to characterize the hemocyte transcriptome response of the shrimp Litopenaeus vannamei succumbing to infectious diseases. By using a high-throughput microfluidic RT-qPCR approach, we identified molecular signatures in shrimp during lethal infections caused by the White Spot Syndrome Virus (WSSV) or the filamentous fungus Fusarium solani. We successfully identified gene expression signatures shared by both infections but also pathogen-specific gene responses. Interestingly, whereas lethal WSSV infection induced the expression of antiviral-related genes, the transcript abundance of many antimicrobial effectors was reduced by lethal F. solani infection. To our knowledge, this is the first report of the immune-gene repertoire of infected shrimp at the brink of death.
BackgroundThis study characterises the molecular processes altered by both elevated CO2 and increasing temperature in oysters. Differences in resilience of marine organisms against the environmental stressors associated with climate change will have significant implications for the sustainability of coastal ecosystems worldwide. Some evidence suggests that climate change resilience can differ between populations within a species. B2 oysters represent a unique genetic resource because of their capacity to better withstand the impacts of elevated CO2 at the physiological level, compared to non-selected oysters from the same species (Saccostrea glomerata). Here, we used proteomic and transcriptomic analysis of gill tissue to evaluate whether the differential response of B2 oysters to elevated CO2 also extends to increased temperature.ResultsSubstantial and distinctive effects on protein concentrations and gene expression were evident among B2 oysters responding to elevated CO2 or elevated temperature. The combination of both stressors also altered oyster gill proteomes and gene expression. However, the impacts of elevated CO2 and temperature were not additive or synergistic, and may be antagonistic.ConclusionsThe data suggest that the simultaneous exposure of CO2-resilient oysters to near-future projected ocean pH and temperature results in complex changes in molecular processes in order to prevent stress-induced cellular damage. The differential response of B2 oysters to the combined stressors also indicates that the addition of thermal stress may impair the resilience of these oysters to decreased pH. Overall, this study reveals the intracellular mechanisms that might enable marine calcifiers to endure the emergent, adverse seawater conditions resulting from climate change.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3818-z) contains supplementary material, which is available to authorized users.
The oyster's immune system is capable of adapting upon exposure to a pathogen-associated molecular pattern (PAMP) to have an enhanced secondary response against the same type of pathogen. This has been demonstrated using poly(I:C) to elicit an antiviral response in the Pacific oyster (Crassostrea gigas) against Ostreid herpesvirus (OsHV-1). Improved survival following exposure to poly(I:C) has been found in later life stages (within-generational immune priming) and in the next generation (transgenerational immune priming). The mechanism that the oyster uses to transfer immunity to the next generation is unknown. Here we show that oyster larvae have higher survival to OsHV-1 when their mothers, but not their fathers, are exposed to poly(I:C) prior to spawning. RNA-seq provided no evidence to suggest that parental exposure to poly(I:C) reconfigures antiviral gene expression in unchallenged larvae. We conclude that the improved survival of larvae might occur via maternal provisioning of antiviral compounds in the eggs. Highlights ► The molecular mechanism involved in transgenerational immune priming was investigated in the oyster, Crassostrea gigas.► Crassostrea gigas larvae have higher survival to OsHV-1 when their mothers, but not their fathers, are exposed to poly(I:C) prior to spawning. ► RNA-seq provided no evidence to suggest that parental exposure to poly(I:C) reconfigures antiviral gene expression in unchallenged larvae. ► Improved survival of C. gigas larvae might occur via maternal provisioning of antiviral compounds in the eggs.
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