Abstract
Crassostrea hongkongensis (Hong Kong oyster) is an ecologically and economically valuable shellfish endemic to South/Southeast Asia. Due to ocean acidification and warming waters, they have become increasingly vulnerable to invading microbes including Vibrio parahaemolyticus, a significant foodborne human pathogen. In recent years, outbreaks of V. parahaemolyticus have emerged as a perennial phenomenon in parts of the world, necessitating to better understand the biology of host-pathogen interactions in this under-examined marine invertebrate. Although an immunologically relevant autophagy apparatus has been identified in Crassostrea gigas, an evolutionarily close mollusk cousin, the precise mechanistic details of C. hongkongensis autophagy during V. parahaemolyticus infection are still wanting. Here, we compellingly demonstrated that in vivo V. parahaemolyticus challenge robustly triggered autophagic signaling in C. hongkongensis hemocytes peaking at 6 h post-infection, which subsequently promoted bacterial clearance and dampened premature apoptosis. Simultaneously, a large surplus of adenosine monophosphate (AMP) and elevations in reactive oxygen species (ROS, specifically mitochondrial O2– and cellular H2O2) formation were observed post-infection. Extrinsically applied AMP and ROS could synergistically induce AMP-activated protein kinase (AMPK) phosphorylation to stimulate downstream autophagic events. V. parahaemolyticus infection-induced autophagy was pharmacologically shown to be AMPK-dependent in vivo. Overall, our results establish autophagy as a crucial arm of host defense against Vibrio infections in mollusks, and provide new insights into the underappreciated roles of ROS and AMP as co-regulators of autophagy.
Highlights
Climate change and anthropogenic degradation of coastal ecosystems in the past decades have a progressive and profound impact on pathogen distribution in marine hosts consumed within the human food chain (Baker-Austin et al, 2012; Vezzulli et al, 2016)
To characterize autophagy in hemocytes following bacterial infection, we set out to obtain temporally resolved profiles of mRNA expression of 14 autophagy-related genes in the hemocytes of C. hongkongensis challenged with V. parahaemolyticus
Changes in microtubule-associated protein light chain 3 (LC3)-I and LC3-II levels were observed by Western blot, following treatment with the autophagy inhibitor NH4Cl to test the functional integrity of autophagic pathway in C. hongkongensis hemocytes
Summary
Climate change and anthropogenic degradation of coastal ecosystems in the past decades have a progressive and profound impact on pathogen distribution in marine hosts consumed within the human food chain (Baker-Austin et al, 2012; Vezzulli et al, 2016). A case in point is the Hong Kong oyster (Crassostrea hongkongensis), an edible mollusk species with an aquaculture history of 700 years and an annual production exceeding 1.6 million tons (Lam and Morton, 2003). A sessile filter feeder of intertidal zones, C. hongkongensis subsists on filtering seawater replete with microorganisms and possesses an immune system that has co-evolved with several clinically significant marine pathogens. Coastal regions of the Pacific basin are increasingly prone to foodborne diseases caused by V. parahaemolyticus outbreaks (Nordstrom et al, 2007; Cheng et al, 2013; Wu et al, 2014). As a result of ocean acidification and warming waters, encroachment of V. parahaemolyticus is accelerated in shellfish harvesting areas, forcing some aquaculture industries to shut down (Marsha et al, 2018; Richards et al, 2019)
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