Recombinant PirA‐like toxin protects shrimp against challenge with <i>Vibrio parahaemolyticus</i>, the aetiological agent of acute hepatopancreatic necrosis disease

Roy

Behera

et al. 2021

Toxins

111

Shrimp, as a high-protein animal food commodity, are one of the fastest growing food producing sectors in the world. It has emerged as a highly traded seafood product, currently exceeding 8 MT of high value. However, disease outbreaks, which are considered as the primary cause of production loss in shrimp farming, have moved to the forefront in recent years and brought socio-economic and environmental unsustainability to the shrimp aquaculture industry. Acute hepatopancreatic necrosis disease (AHPND), caused by Vibrio spp., is a relatively new farmed penaeid shrimp bacterial disease. The shrimp production in AHPND affected regions has dropped to ~60%, and the disease has caused a global loss of USD 43 billion to the shrimp farming industry. The conventional approaches, such as antibiotics and disinfectants, often applied for the mitigation or cure of AHPND, have had limited success. Additionally, their usage has been associated with alteration of host gut microbiota and immunity and development of antibiotic resistance in bacterial pathogens. For example, the Mexico AHPND-causing V. parahaemolyticus strain (13-306D/4 and 13-511/A1) were reported to carry tetB gene coding for tetracycline resistance gene, and V. campbellii from China was found to carry multiple antibiotic resistance genes. As a consequence, there is an urgent need to thoroughly understand the virulence mechanism of AHPND-causing Vibrio spp. and develop novel management strategies to control AHPND in shrimp aquaculture, that will be crucially important to ensure food security in the future and offer economic stability to farmers. In this review, the most important findings of AHPND are highlighted, discussed and put in perspective, and some directions for future research are presented.

Section: Acute Hepatopancreatic Necrosis Disease (Ahpnd)—an Overviewmentioning

confidence: 99%

Acute Hepatopancreatic Necrosis Disease (AHPND): Virulence, Pathogenesis and Mitigation Strategies in Shrimp Aquaculture

Roy

Behera

et al. 2021

Toxins

111

“…There are few reports which suggest that the administration of bacterial toxins could serve as cross-protective antigens and provide protection against microbial infection. For instance, Campa-Cordona et al [ 71 ] reported that recombinant PirA-like toxin, when administered through bath immersion, enhances the immune response of shrimp, providing protection against AHPND-causing V. parahaemolyticus [ 71 ]. In another study, ToxA VP toxin, when administrated to Pacific red snapper Lutjanus peru was reported to positively affect the humoral immune response and upregulate the expression of immune genes that protects the red snapper from V. parahaemolyticus infection [ 72 , 73 ].…”

Section: Discussionmentioning

confidence: 99%

Do acute hepatopancreatic necrosis disease-causing PirAB ^VP toxins aggravate vibriosis?

Tran

Emerging Microbes & Infections

Bossier

2020

Gram-negative marine bacterium Vibrio parahaemolyticus is an important aquatic pathogen and has been demonstrated to be the causative agent of acute hepatopancreatic necrotic disease (AHPND) in shrimp aquaculture. The AHPND-causing V. parahaemolyticus strains contain a pVA1 plasmid encoding the binary PirA VP and PirB VP toxins, are the primary virulence factor that mediates AHPND and mortality in shrimp. Since PirAB VP toxins are secreted extracellularly, one can hypothesize that PirAB VP toxins would aggravate vibriosis in the aquatic environment. To address this, in vivo and in vitro experiments were conducted. Germ-free Artemia franciscana were co-challenged with PirAB VP toxins and 10 Vibrio spp. The in vivo results showed that PirAB VP toxin interact synergistically with MM30 (a quorum sensing AI-2 deficient mutant) and V. alginolyticus AQ13-91, aggravating vibriosis. However, co-challenge by PirAB VP toxins and V. campbellii LMG21363, V. parahaemolyticus CAIM170, V. proteolyticus LMG10942, and V. anguillarum NB10 worked antagonistically, increasing the survival of Artemia larvae. The in vitro results showed that the addition of PirAB VP toxins significantly modulated the production of the virulence factors of studied Vibrio spp. Yet these in vitro results did not help to explain the in vivo results. Hence it appears that PirAB VP toxins can aggravate vibriosis. However, the dynamics of interaction is strain dependent.

“…Acute hepatopancreatic necrosis disease (AHPND), earlier named as early mortality syndrome (EMS), has been particularly devastating in the cultivation of shrimp, causing massive mortality (up to 100%) within 20-30 days of post-larvae stocking [5,11,15]. Since the AHPND outbreak first appeared in China in 2009, it has spread to Vietnam (2010), Malaysia (2011), Thailand (2012), Mexico (2013), Philippines (2015), South America (2016), Australia (2016), Bangladesh (2019), and USA (2019) [7,8,[16][17][18][19].…”

Section: Discussionmentioning

confidence: 99%

“…The PirAB VP toxins are the primary virulence factor of AHPND-causing bacteria that mediates AHPND and mortality in shrimp [10]. The binary PirAB VP toxins mainly target the hepatopancreas (digestive gland) of shrimp and damage the R (resorptive), B (blister), F (fibrillar), and E (embryonic) cells, resulting in dysfunction and massive mortalities (up to 100%) within 20-30 days of shrimp post-larvae stocking [2,5,11]. Since the impact of these binary toxins are significant in shrimp aquaculture, more research attention is needed to unravel the toxin-mediated infection process at cellular level.…”

Section: Introductionmentioning

confidence: 99%

PirABVP Toxin Binds to Epithelial Cells of the Digestive Tract and Produce Pathognomonic AHPND Lesions in Germ-Free Brine Shrimp

Bels

Couck

et al. 2019

Toxins

Acute hepatopancreatic necrosis disease (AHPND), a newly emergent farmed penaeid shrimp bacterial disease originally known as early mortality syndrome (EMS), is causing havoc in the shrimp industry. The causative agent of AHPND was found to be a specific strain of bacteria, e.g., Vibrio and Shewanella sps., that contains pVA1 plasmid (63–70 kb) encoding the binary PirAVP and PirBVP toxins. The PirABVP and toxins are the primary virulence factors of AHPND-causing bacteria that mediates AHPND and mortality in shrimp. Hence, in this study using a germ-free brine shrimp model system, we evaluated the PirABVP toxin-mediated infection process at cellular level, including toxin attachment and subsequent toxin-induced damage to the digestive tract. The results showed that, PirABVP toxin binds to epithelial cells of the digestive tract of brine shrimp larvae and produces characteristic symptoms of AHPND. In the PirABVP-challenged brine shrimp larvae, shedding or sloughing of enterocytes in the midgut and hindgut regions was regularly visualized, and the intestinal lumen was filled with moderately electron-dense cells of variable shapes and sizes. In addition, the observed cellular debris in the intestinal lumen of the digestive tract was found to be of epithelial cell origin. The detailed morphology of the digestive tract demonstrates further that the PirABVP toxin challenge produces focal to extensive necrosis and damages epithelial cells in the midgut and hindgut regions, resulting in pyknosis, cell vacuolisation, and mitochondrial and rough endoplasmic reticulum (RER) damage to different degrees. Taken together, our study provides substantial evidence that PirABVP toxins bind to the digestive tract of brine shrimp larvae and seem to be responsible for generating characteristic AHPND lesions and damaging enterocytes in the midgut and hindgut regions.