Abstract
Emerging, infectious diseases in shrimp like acute hepatopancreatic necrosis disease (AHPND) caused by Vibrio parahaemolyticus and mortality caused by other Vibrio species such as Vibrio harveyi are worldwide related to huge economic losses in industrial shrimp production. As a strategy to prevent disease outbreaks, a plant-based phenolic compound could be used as a biocontrol agent. Here, using the brine shrimp (Artemia franciscana) as a model system, we showed that phloroglucinol treatment of the parental animals at early life stages resulted in transgenerational inherited increased resistance in their progeny against biotic stress, i.e., bacteria (V. parahaemolyticus AHPND strain and V. harveyi) and abiotic stress, i.e., lethal heat shock. Increased resistance was recorded in three subsequent generations. Innate immune-related gene expression profiles and potential epigenetic mechanisms were studied to discover the underlying protective mechanisms. Our results showed that phloroglucinol treatment of the brine shrimp parents significantly (P < 0.05) enhanced the expression of a core set of innate immune genes (DSCAM, proPO, PXN, HSP90, HSP70, and LGBP) in subsequent generations. We also demonstrated that epigenetic mechanisms such as DNA methylation, m6A RNA methylation, and histone acetylation and methylation (active chromatin marker i.e., H3K4Me3, H3K4me1, H3K27me1, H3 hyperacetylation, H3K14ac and repression marker, i.e., H3K27me3, H4 hypoacetylation) might play a role in regulation of gene expression leading toward the observed transgenerational inheritance of the resistant brine shrimp progenies. To our knowledge, this is the first report on transgenerational inheritance of a compound-induced robust protected phenotype in brine shrimp, particularly protected against AHPND caused by V. parahaemolyticus and vibriosis caused by V. harveyi. Results showed that epigenetic reprogramming is likely to play a role in the underlying mechanism.
Highlights
Vibriosis caused by Vibrio parahaemolyticus infects various shrimp species and causes acute hepatopancreatic necrosis disease (AHPND), initially named early mortality syndrome (EMS)
Age- and size-synchronized larvae were used, which were obtained by hatching the oviparous produced brine shrimp cysts under axenic conditions, allowing to challenge gnotobiotic First filial generation (F1)–Third filial generation (F3) larvae with bacteria being V. parahaemolyticus or V. harveyi
Our results showed that phloroglucinol treatment of parental brine shrimp (F0) at an early life stage increased the resistance of their progeny for three subsequent unexposed generations (F1, Second filial generation (F2), and F3) against a bacterial infection with V. parahaemolyticus or Vibrio harveyi at the end of the monitoring period
Summary
Vibriosis caused by Vibrio parahaemolyticus infects various shrimp species and causes acute hepatopancreatic necrosis disease (AHPND), initially named early mortality syndrome (EMS). V. harveyi is another pathogen from the Vibrionaceae family that causes substantial mortality by vibriosis and economic loss in shrimp aquaculture [1]. Both infections affect animal welfare and are economically devastating to the shrimp industry [2]. Shrimp production in affected regions has dropped to ∼60%, with up to 100% mortality and led to tremendous global losses estimated at more than $1 billion per year [3, 4]. In particular AHPND/EMS, many conventional approaches such as the use of antibiotics and disinfectants have been applied but had very little success. There is an urgent need to develop innovative disease preventive methods that support sustainable shrimp aquaculture
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