Specific Molecular Signatures for Type II Crustins in Penaeid Shrimp Uncovered by the Identification of Crustin-Like Antimicrobial Peptides in Litopenaeus vannamei

Abstract

Crustins form a large family of antimicrobial peptides (AMPs) in crustaceans composed of four sub-groups (Types I-IV). Type II crustins (Type IIa or “Crustins” and Type IIb or “Crustin-like”) possess a typical hydrophobic N-terminal region and are by far the most representative sub-group found in penaeid shrimp. To gain insight into the molecular diversity of Type II crustins in penaeids, we identified and characterized a Type IIb crustin in Litopenaeus vannamei (Crustin-like Lv) and compared Type II crustins at both molecular and transcriptional levels. Although L. vannamei Type II crustins (Crustin Lv and Crustin-like Lv) are encoded by separate genes, they showed a similar tissue distribution (hemocytes and gills) and transcriptional response to the shrimp pathogens Vibrio harveyi and White spot syndrome virus (WSSV). As Crustin Lv, Crustin-like Lv transcripts were found to be present early in development, suggesting a maternal contribution to shrimp progeny. Altogether, our in silico and transcriptional data allowed to conclude that (1) each sub-type displays a specific amino acid signature at the C-terminal end holding both the cysteine-rich region and the whey acidic protein (WAP) domain, and that (2) shrimp Type II crustins evolved from a common ancestral gene that conserved a similar pattern of transcriptional regulation.

Antimicrobial Peptides and Ectosymbiotic Relationships: Involvement of a Novel Type IIa Crustin in the Life Cycle of a Deep-Sea Vent Shrimp

“…Although unusual, the presence of Type IIa crustins has been reported for other decapod crustaceans from the Pleocyemata suborder (59,60). On the other hand, Type IIb crustins were only described in penaeid shrimp species (46).…”

“…Comparatively, crustin members from Types III and IV are composed of one and two WAP domains, respectively, and are devoid of any other domains. Interestingly, while Type I crustins are widely distributed across decapod crustaceans (Pleocyemata and Dendrobranchiata), Type II crustins (Sub-Types IIa and IIb) are mainly present in penaeid shrimps (Dendrobranchiata) (46).…”

Identification of Multigene Biomarker for Shrimp White Feces Syndrome by Full-Length Transcriptome Sequencing

“…Unlike ALFs, the antibacterial activities of PENs are essentially directed against Gram-positive bacteria (Destoumieux et al, 1999). Crustins form a large family of antimicrobial peptides, exhibiting protease inhibitory properties and regulatory functions in bacterial growth to all microbes (Barreto et al, 2018). The C-MnSOD and lysozymes are immune effector proteins that have antibacterial activities (Niu et al, 2018).…”

“…The nodes with the greatest number of neighbors were identified (Table 3), which could be considered significant hubs of the network. Some important keystone genes, such as ALF-D, CrustinA and Lvserpin (Nigou et al, 2013;Liu et al, 2014;Barreto et al, 2018), have been reported to play central roles in antimicrobial activities. PCoA was performed to determine the transcript profiles across groups.…”

Massive Gene Expansion and Sequence Diversification Is Associated with Diverse Tissue Distribution, Regulation and Antimicrobial Properties of Anti-Lipopolysaccharide Factors in Shrimp

“…Instead, the expression of ALFs from Groups A, B, D and G was quite similar to that observed for other shrimp AMPs that are exclusively produced by hemocytes [ 16 ]. On the one hand, the expression of ALFs early in development could be the result of maternal transmission [ 16 , 22 ] but, on the other hand, those transcripts might originate from other shrimp tissues. Interestingly, in different species, including L. vannamei , the expression of ALFs from Groups C and F was mainly detected in other tissues (digestive system, gills, eyestalk) than in the circulating hemocytes [ 17 , 18 , 19 ].…”