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Soto-Rodriguez, S.; Lozano-Olvera, R.; Ramos-Clamont Montfort, G.; Zenteno, E.; Sánchez Salgado, J.L.; , . PirAB from Vibrio parahaemolyticus and AHPND in Shrimp. Encyclopedia. Available online: https://encyclopedia.pub/entry/21956 (accessed on 10 July 2025).
Soto-Rodriguez S, Lozano-Olvera R, Ramos-Clamont Montfort G, Zenteno E, Sánchez Salgado JL,  . PirAB from Vibrio parahaemolyticus and AHPND in Shrimp. Encyclopedia. Available at: https://encyclopedia.pub/entry/21956. Accessed July 10, 2025.
Soto-Rodriguez, Sonia, Rodolfo Lozano-Olvera, Gabriela Ramos-Clamont Montfort, Edgar Zenteno, Jose Luis Sánchez Salgado,  . "PirAB from Vibrio parahaemolyticus and AHPND in Shrimp" Encyclopedia, https://encyclopedia.pub/entry/21956 (accessed July 10, 2025).
Soto-Rodriguez, S., Lozano-Olvera, R., Ramos-Clamont Montfort, G., Zenteno, E., Sánchez Salgado, J.L., & , . (2022, April 19). PirAB from Vibrio parahaemolyticus and AHPND in Shrimp. In Encyclopedia. https://encyclopedia.pub/entry/21956
Soto-Rodriguez, Sonia, et al. "PirAB from Vibrio parahaemolyticus and AHPND in Shrimp." Encyclopedia. Web. 19 April, 2022.
PirAB from Vibrio parahaemolyticus and AHPND in Shrimp
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This entry is adapted from the peer-reviewed paper 10.3390/toxins14040243

PirAB is a potent toxin which can causes 100% mortality in shrimp, the toxin produce masive sloughing of the epithelial cells of the shrimp hepatopancreas, kown as acute hepatopancreatic necrosis diseaseas (AHPND) in diseased penaeid shirmp. This toxin is produced by specific strains of Vibrio parahaemolyticus, which harbors a plasmid of ~70 kbp (pVA1) containing the pirAVp and pirBVp genes that encode PirAB toxin. 

 

PirAB AHPND shrimp microbiota change inhibitors PirAB receptors virulence plasmid

1. Virulence Plasmid of Vibrio parahaemolyticus AHPND

Acute hepatopancreatic necrosis disease (AHPND) is mainly caused by Vp, which harbors a plasmid of ~70 kbp (pVA1) containing the pirAVp and pirBVp genes that encode the delta-endotoxin responsible for the typical lesions in shrimp Hp [1][2]. The genomes of pVA1-harboring Vp revealed a large pan genome with high genetic diversity grouped into three main clades and specific structural differences, in addition to the instability of the pirABVp region of the pVA1 plasmid [3]. The structural differences found in pVA1 are likely due to the horizontal propagation of the plasmid to other Vibrio species [4], such as V. harveyi [5][6], V. campbellii [6], V. owensii [6], and V. punensis [7]. These processes might result in the appearance of new pathogenic AHPND strains, which would pose a major threat to the shrimp industry. Likewise, this variability in structural elements could eventually influence their niche adaptation ability, growth behavior, and virulence/pathogenesis.
Recently, Aguilar-Rendón et al. [8] found large variability of the plasmid copy number (7 to 121 copies) per bacterial cell of Vp AHPND strains analyzed by qPCR [9][10], although it has been reported that virulence does not depend on the copy number of pirAVp/pirBVp genes [11]. To date, no clear evidence of their role in AHPND has been found. It using a shotgun metagenomics approach on bottom seawater with P. vannamei inoculated with two Vp AHPND strains registered more than one copy of pVA1 per bacterial cell (1.9 to 13.5 copies per bacterial cell) throughout the experimental infection period [12]. The copy number of the virulent plasmid was not dependent on the degree of virulence of the Vp AHPND strain but rather on bacterial density (Figure 1). Nonetheless, it has been evaluated the variability in the plasmid copy number per bacterial cell in relation to the degree of virulence or bacterial density and how this may influence AHPND pathogenesis.
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Figure 1. Bacterial density of the bottom seawater and virulent plasmid copy (pVA1) number of moderate virulence Vibrio parahaemolyticus strain M0607 and high virulent V. parahaemolyticus strain M0904 during experimental infections at 105 CFU mL−1.

2. Factors That Could Induce or Inhibit Toxin Production

2.1. Quorum Sensing

Quorum sensing (QS) is a cell-to-cell signaling mechanism in response to an increased bacterial cell population [13]. Bacterial QS produce, release, and recognize molecular autoinducers (AIs) that bind to surface bacterial receptors, triggering signal transduction cascades that alter the expression of genes related with survival and infection factors, such as sporulation, luminescence, biofilm formation, and virulence [14]. The QS mechanism is widely distributed in Vibrionaceae members, with the acyl-homoserine lactones (AHLs) being among the more common AIs. For example, AHLs have been implicated in the signaling mechanisms that activate the production of luciferase in V. fischeri [13]. In addition, V. harveyi produces and responds to three other AIs: (1) HAI-1, [N-(3- hydroxy butyryl)-homoserine lactone], an intra-species AI; (2) CAI-1, [(Z)-3-aminoundec-2- en-4one], which is restricted to the Vibrio genera; and (3) the inter-species AI-2 [(2S,4S)-2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran-borate]. These three AIs act in parallel to regulate over 600 target genes through complex signaling cascades [13][15]. The capacity of Vibrionaceae for “sensing self” and “sensing others” allows for both competition and cooperation in complex microbial communities [16].
Virulence gene expression regulated by QS has been studied extensively in V. harveyi and may serve as a basis for understanding the QS mechanisms in Vp given that this pathogen contains the central conserved components of the QS pathway known in V. harveyi [17]. For example, a LuxT homolog of V. harveyi, SwrT, activates genes that encode for translocation across surfaces and swarming and is lateral-flagella-driven in Vp [18][19]. In addition, V. harveyi and presumably Vp produce three types of AIs, namely auto inducer 2 (AI-2), harveyi auto inducer 1 (HAI1), and cholerae auto inducer 1 (CAI1), which are recognized by the surface membrane receptors LuxP/LuxQ, LuxN, and CqsS, respectively [20]. In a preliminary one, [21] showed that the production of PirABVp binary toxin is regulated by the AI-2 QS process. They tested the effect of a cell-free supernatant from V. harveyi containing AI-2 (CFS-VH) on an AHPND-causing Vp strain. The AI-2-containing supernatant accelerated the production time and yield of both PirAVp and PirBVp toxins, whereas the application of the furanone [(5Z)-4-bromo5-(bromomethylene)-2(5H)-furanone] AI-2 antagonist delayed AHPND toxin production or secretion. It opens new perspectives on QS mechanisms in Vp and on possible treatments and management strategies to control AHPND infection in shrimp culture. Interestingly, AI-2 is synthetized by numerous bacterial species and can facilitate inter-species cell–cell signaling [22], resulting in changes of Vp behavior in complex microbial communities.

2.2. Environmental Factors

Bacterial adaptation and survival depend on the capacity to properly respond to changes in internal and external environments. The survival of Vibrio spp. in marine environments depends on carbon and energy sources, dissolved oxygen, water pH, salinity, temperature, and starvation [23]. In particular, changes in temperature due to global warming are a growing concern for aquaculture due to the increased risk of Vp-induced diseases. Environmental stress can increase horizontal gene transfer mechanisms in AHPND-causing Vp strains, promoting their growth [24][25] and increasing the risk of AHPND outbreaks and disease dispersion in tropical zones. Recently, the effect of temperature shifts on pirAVp and pirBVp gene expression of the AHPND-Vp AAHMRU04 strain isolated from white shrimp exhibiting clinical signs of AHPND was evaluated [26]. Bacteria were grown at 30 °C for 24 h and subsequently exposed to a set of different temperature trials for 4 days. The pirAVp and pirBVp genes were induced when the temperature shifted from high (26–32 °C) to low (22–28 °C) [26].
The relationship between salinity and AHPND in P. vannamei was studied by [27]. Pathogen-free shrimp cultures (5, 10, 15, and 20 g L−1 of NaCl) were challenged with a Vp AHPND broth. In all salinity treatments, Vp AHPND caused infection in shrimp as confirmed by histological damage and the presence of pirABVp toxin genes by PCR analysis. However, cumulative mortality was different, showing higher survival in shrimp maintained at lower salinities. Since Vp reproduces more efficiently in high salinity environments, it is likely that a greater amount of PirABVp toxin was produced, resulting in a higher cumulative mortality in P. vannamei when maintained under these conditions. However, different patterns were observed when challenging P. vannamei growing under different salinity conditions with the Vp AHPND strain E9 [28]. Mortality was higher at lower salinities and a positive correlation was present with the expression of the pirAVp gene. Although more experiments are needed to determine the influence of salinity on the expression of pirABVp, these experiments corroborate that the toxin can be expressed at different salinities [29] and that the management of salinity in shrimp culture can be an important factor to control Vp infectivity.
Another environmental factor that has been known with regard to the production of the PirABvp binary toxin is related to fluid shear and the hydrodynamic forces acting on Vp due to either natural influences or the use of aquaculture equipment to enhance shrimp productivity, such as blowers or aerators [30]. To this end, the effect of shaking conditions on the AHPND-causing Vp M0904 was known [31]. At a constant agitation of 110 rpm, bacteria developed cellular aggregates together with levan (branched polymeric fructans)-containing biofilm formations and acquired tolerance against antimicrobial agents (kanamycin, ampicillin, rifampicin, and tetracycline), possibly due to high biofilm production. In addition, a significant decrease was observed not only in PirAVp/PirBVp toxin production but also in the virulence of Vp M0904 to Artemia and Macrobrachium larvae. Increasing the shaking speed to 120 rpm produced an increase in PirAVp/PirBVp toxin production, the virulence of Vp M0904 to Artemia and Macrobrachium larvae, and the expression of polar flagellin (flaA), polar flagellin-specific chaperone (fliS), and chemotaxis protein (CheR). This type provides valuable information for understanding the behavior of Vp AHPND in aquaculture environments [31].

2.3. Biofilm Formation

The formation of bacterial biofilms represents one of the most important survival mechanisms, attachment, as well as host colonization strategies of bacteria [32]. This phenomenon is influenced by abiotic and biotic factors regulated by QS [33]. ToxR is an important virulence regulator implicated in the synthesis of Vp biofilms that also controls the expression of the virulence factors found in human pathogenic Vp, including thermostable direct hemolysin (TDH), TDH-related hemolysin (TRH), and T3SS [34][35]. The expression of these factors is regulated by QS through the production of and responses to AI-2 [33][36][37]. Under these conditions, biofilm and toxin production appear to be simultaneous activities.
Information on the relationship between biofilm formation and the production of PirABvp binary toxin in Vp AHPND is lacking. The only one to address this issue is that of [31], which observed an inverse relationship between the production of biofilms and that of the PirABVp toxin. This behavior refers to the formation of abiotic films in response to fluid shear and hydrodynamic forces. However, the regulation, growth kinetics, and characteristics of Vp AHPND biofilms in the host and their relationships with PirABvp toxin production remain uncharacterized.

3. Search for Membrane Receptors of PirAVp and PirBVp

3.1. Biological Activities of the PirAVp and PirBVp Subunits

Bacterial protein toxins, like PirABVp, are molecular self-governing virulence factors that target specific host cells, triggering different damaging processes involved in the disease of the infected organism. The binding of bacterial toxins to plasma cell surface receptors is an essential first step for shrimp intoxication. Knowing the structures of these receptors can further the understanding of the infection mechanisms with the aim of preventing host disease by blocking the toxin–receptor interaction using a mimetic antagonist [38]. The PirAVp/PirBVp toxin induces cell damage in the shrimp Hp, although it is not seen in other organs, and is considered a shrimp-specific toxin [39]. Moreover, it seems that PirAVp/PirBVp receptors will be found exclusively in this organ [40]. Recently, it has been observed that the B Subunit of the PirABVp toxin is an amino sugar-specific lectin-like, and it is able to recognize glycoproteins on the epithelium of the Hp, suggesting its participation in AHPND pathogenesis [41][42]. Nevertheless, the PirAVp/PirBVp binding model complex requires clarification and further information is needed.
It is known that PirAVp and PirBVp form a heterodimeric complex that binds to receptors located on the cells of the shrimp Hp [40][43]. However, the precise nature of the toxin receptors is still not known. Lee et al. [2] suggested that PirABVp structure is homologous to the insecticidal Photorhabdus insect-related (Pir) binary toxin, and in silico analysis showed that the PirAVp and PirBVp toxins possess similar structures to the functional domains of the pore-forming Bacillus thuringiensis Cry toxins [2][40]. The structural alignment of both toxins indicates that the PirAVp subunit is similar to the lectin-like recognition domain III of B. huringiensis toxin, whereas PirBVp corresponds to the pore-forming I and II domains [2][40][44][45]. In this context, the initial interaction of the PirAVp/PirBVp toxins would be through lectin-carbohydrate recognition between PirAVp and the glycans exposed on the surface of the plasma membrane of Hp cells [40]. Structural features and molecular docking of the PirAVp subunit show a potential sugar-binding cavity for glycans containing the N-Acetylgalactosamine (GalNac) molecule, whereas the PirBVp subunit structure contains a C-terminal receptor domain similar to Cry domain II for protein–protein ligand interactions and an N-terminal consistent with other membrane pore-forming toxins, including Cry domain I [2][44]. In addition, Hao et al. [39] analyzed the distribution and homology of PirABVp-like proteins in other bacterial species and showed that at least seven bacterial taxa harbor complete or partial pirAB genes, including Alcaligenes, Photorhabdus, Pectobacterium carotovorum, Vibrio, Xenorhabdus, Yersinia, and Shewanella violacea. All examined PirB proteins examined by Hao et al. [39] showed typical B. thuringiensis Cry structure formed by several α-helix bundles in the N-terminal of PirB and a coup of parallel or anti-parallel β-sheets in the C-terminal of PirBVp.
However, the protein structure in the receptor binding sites of compared PirB proposed by Lin et al. [40] reflected an evolutionary divergence in the amino acid sequences (for more details, see Hao et al. [39]). The conformation and the direction of Loop 2 of PirB are unique in V. parahaemolyticus, thus PirBVp might target a specific receptor in the cell membrane. In addition, the predicted structures of PirA toxins also showed remarkable differences in ligand-binding sites. These structural variations could largely influence the recognition events of PirABVp. It was proposed that PirABVp forms a heterotetrametric complex containing four PirAVp subunits and four PirBVp subunits [40] and that PirBVp first recognizes glycosaminoglycan molecules as mucin-like or beta-hexosaminidase where the Gal(β1–3/1–4)GlcNAc(α1–2) sequence is essential for PirBVp recognition in the hepatopancreatic membrane [42] (Figure 2). The role of the PirA subunit might be stabilizing the complex for a better binding to the possible receptor molecule on the shrimp hepatopancreatic epithelial cells [40]. A complete understanding of the receptor binding mechanisms of PirA/PirB toxins is essential in order to elucidate the toxin mechanism.
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Figure 2. Proposed PirABVp binding scheme. The PirAVp/PirBVp heterotetrametric complex first uses PirBVp-lectin to recognize and bind with glycosaminoglycan molecules; meanwhile, PirAVp stabilizes the complex. Then the complex probably binds to the receptor molecules on the membrane of the hepatopancreatic epithelial cells of shrimp to trigger the massive sloughing of these cells.
Recent ones have suggested that the regions of interaction of PirABVp are different than those of insecticidal toxins. From the extracellular products (ECPs) of Vp, a heterotetrametric complex of 250 kDa has been purified, which contains four PirAVp and four PirBVp subunits. The PirBVp subunit was confirmed to show lectin-like activity and the recognition of mucin-like O-glycosidic structures in the shrimp Hp that may act as receptors for toxin binding, while PirAVp did not present this activity [41]. Lectin activity has been suggested due to its ability to interact specifically with oligosaccharides and glycoproteins such as mucin, but further structural assays will confirm the participation of the lectin effect in the pathogenesis of Vp AHPND.
The PirABVp complex seems to be necessary to induce AHPND signs. The mechanism of action of the entire toxin during the AHPND disease process remains to be determined. However, experiments conducted with the recombinant proteins rPirAVp and rPirBVp showed that only the PirABVp complex and rPirBVp displayed Mg2+ or Ca2+ independent hemagglutinating activity (HA) toward rat red cells, whereas rPirAVp was not able to agglutinate erythrocytes from several animal species [41].
In a first attempt to determine the sugar specificity of the putative PirBVp lectin-like, subsequent competition experiments were conducted using a wide battery of monosaccharides, disaccharides, and glycoproteins. The PirBVp subunit binds to a glycoconjugate glycan moiety containing amino sugars [41]. Further experiments conducted by the same group showed the existence of different glycan receptors for PirBVp, and in particular a mucin-like receptor located at the surface membrane of the cell Hp and an internal hexosaminidase glycoprotein receptor that is possibly involved in toxin-related cell damage to shrimp tissues [42]. Beta-hexosaminidase (β-N-acetyl hexosaminidase) is a ubiquitous lysosomal enzyme with multiple roles in protein glycosylation and synthesis and glycoconjugate metabolism [46]. This glycoprotein plays an important role in arthropod molting and chitin degradation and in the defense system of P. vannamei against parasites [47][48]. Extracellular beta-hexosaminidases secreted by eukaryotes occur as dimers and possess N-glycosidically-linked glycans with oligomannosidic and complex-type glycan structures [49][50]. The possibility that PirBVp could recognize N-linked oligosaccharides expressed by endosomal or secreted beta-hexosaminidase, which would allow for an increased pathogenesis of Vp in crustaceans, cannot be excluded.
Previous data suggest putative lectin-like PirBVp subunit activity [41][42] that contrasts with the functions of domains I and II proposed for the Cry toxin and with the proposed function of the PirAVp subunit given that it has not been possible to verify that this subunit can recognize carbohydrates in the experiments conducted to date. In light of this, the PirAVp subunit could play an initial stabilizing role, allowing PirBVp to bind with higher affinity to the glycan receptors located at the surface of Hp cells.

3.2. Expression of Mucin-like O-Glycosidic Structures in Shrimp

O-glycans are critical for the development and proper functioning of multicellular organisms. Mucin-type glycans are widely found on the cell surfaces and secreted glycoconjugates of invertebrates [51]. These O-glycans may serve as receptor-binding sites for a variety of pathogenic bacteria and their toxins [52]. A small unit of P. vannamei hemocyanin had O-glycans that were closely associated with agglutination activity toward Vibrio fluvialis, V. alginolyticus, and V. parahaemolyticus [53][54].
A mucin-like peritrophin-like gene from fleshy shrimp (Fenneropenaeus chinensis) is able to bind to Gram-negative bacteria [55], while another mucin-like peritrophin-like gene from the shrimp Exopalaemon carinicauda is involved in white spot syndrome viral infections [56]. In addition, a mucin-like peritrophin has been implicated in V. harveyi infection in the black tiger shrimp P. monodon [57]. Abiotic characteristics, such as decreases in temperature and changes in diet, increase the expression of several mucin-like proteins in P. vannamei [58][59][60]. These modifications could be related to the pathologic development of Vibrio infection, increasing the number of binding targets in the shrimp digestive system. Searching for possible receptors for the lectin-like PirBVp [42] has yielded evidence of some correspondence with a mucin-like protein expressed in the shrimp Hp of P. vannamei. These  are the beginning of a better understanding of the infection mechanisms of Vp in shrimp.

3.3. Receptor on Shrimp Hemocytes

The PirABVp toxin is known to mainly target the epithelial cells of shrimp Hp tubules. In addition. Moreover, the dysregulation of apoptosis-related genes in Vp AHPND-challenged P. vannamei hemocytes suggests that Vp AHPND induces apoptosis in hemocytes [61]. In the transcriptome of Vp AHPND-challenged P. vannamei, an aminopeptidases N1 (LvAPN1) gene was identified [62]. DNA sequence analysis of the LvAPN1 gene showed a putative C-terminal transmembrane domain and various putative N- and O-glycosylation sites. The expression of LvAPN1 increases in hemocytes after challenging P. vannamei with either Vp AHPND or the partially purified Vp AHPND toxins. Silencing of LvAPN1 significantly reduced LvAPN1 transcription levels in the stomach, Hp, and hemocytes and increased the survival of adult P. vannamei that were challenged with the partially purified Vp AHPND toxins. These observations suggest the putative role of LvAPN1 as a PirABVp toxin receptor located on the hemocyte surface [62].
Other putative carbohydrate receptors for the PirABVp toxin could be located in the surface of P. vannamei hemocytes, as these cells express a plethora of glycoconjugates. Using commercial lectins with different carbohydrate specificities, the presence of carbohydrate moieties containing mainly N-acetyl-glucosamine (GlcNAc) and N-acetylneuraminic acid (sialic acid) was demonstrated [63]. In another, these carbohydrates were recognized by the rPirBVp subunit [41].

4. Search of Potential Inhibitors of the PirABVp Toxin

Understanding the structural biology of PirABVp is essential for finding or developing antiadhesive agents or receptor analogs that could prevent adhesion and subsequent cell entry of the toxin, thus inhibiting its activity. In particular, it is important to decipher the roles and structural features of complex carbohydrates that serve as toxin receptors. According  to the group, the PirB subunit presents lectin-like activity, and its adhesion can be inhibited in the presence of fucosylated glycans and by those that contain N-acetyl glucosamine [41][42].
In addition to glycans, peptides that can interact with PirABVp are also needed. Computational tools like molecular docking can play an important role in the search for antiadhesive peptides or in the design of antiadhesive peptide analogs through the creation of precise structural models of peptide-toxin complexes and the calculation of binding free energies [64][65]. The search for bifunctional peptides that can be used to improve shrimp growth while at the same time protecting them from the PirABVp toxin is also important. For example, oilseed peptides have been found to contribute to improved shrimp health and growth performance when used as feed ingredients [66]. In silico one have revealed six dual-target peptides from different oilseed proteins capable of interfering with the formation of the PirAVp/PirBVp complex. Such peptides (1139–2977 Da in mass and 10–28 residues in length) are possible candidates for the future development of peptide-based anti-AHPND agents [65].

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Subjects: Microbiology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Sonia Soto-Rodriguez
,
Rodolfo Lozano-Olvera
,
Gabriela Ramos-Clamont Montfort
,
Edgar Zenteno
,
Jose Luis Sánchez Salgado
,
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