Global mRNA and miRNA Analysis Reveal Key Processes in the Initial Response to Infection with WSSV in the Pacific Whiteleg Shrimp

Abstract

White Spot Disease (WSD) presents a major barrier to penaeid shrimp production. Mechanisms underlying White Spot Syndrome Virus (WSSV) susceptibility in penaeids are poorly understood due to limited information related to early infection. We investigated mRNA and miRNA transcription in Penaeus vannamei over 36 h following infection. Over this time course, 6192 transcripts and 27 miRNAs were differentially expressed—with limited differential expression from 3–12 h post injection (hpi) and a more significant transcriptional response associated with the onset of disease symptoms (24 hpi). During early infection, regulated processes included cytoskeletal remodelling and alterations in phagocytic activity that may assist WSSV entry and translocation, novel miRNA-induced metabolic shifts, and the downregulation of ATP-dependent proton transporter subunits that may impair cellular recycling. During later infection, uncoupling of the electron transport chain may drive cellular dysfunction and lead to high mortalities in infected penaeids. We propose that post-transcriptional silencing of the immune priming gene Dscam (downregulated following infections) by a novel shrimp miRNA (Pva-pmiR-78; upregulated) as a potential mechanism preventing future recognition of WSSV that may be suppressed in surviving shrimp. Our findings improve our understanding of WSD pathogenesis in P. vannamei and provide potential avenues for future development of prophylactics and treatments.

Resistance to white spot syndrome virus in the European shore crab is associated with suppressed virion trafficking and heightened immune responses

“…The average proportion of sequences that were WSSV-derived in these six crabs was 4.7% (± 2.9, one standard deviation). In contrast, viral transcripts in highly susceptible P. vannamei were first observed at 3 h and increased from 0.3% to approximately 40% of expressed transcripts in the first 24h following infection ( 8 ).…”

“…These groups were injected with either saline solution or WSSV-infected shrimp homogenate for the disease trial and the gills of 8 crabs were sampled from saline and WSSV-injected treatment groups at 0, 6, 12, 24, 48, 168, 336 and 672 hours and snap frozen for transcriptome sequencing. The lower panel illustrates the equivalent time course experiment in the susceptible shrimp ( P. vannamei ) reported in a previously published WSSV-exposure dataset utilised for comparison ( 8 ).…”

“…To enable comparisons between datasets for resistant C. maenas and susceptible P. vannamei analyses of C. maenas mRNA and miRNA sequencing datasets were conducted as closely as possible to that described previously for P. vannamei ( 8 ). A detailed account of the transcriptome analysis is detailed in Supplementary Figure 1 .…”

“…Transcriptional changes, enriched KEGG pathways and gene ontology (GO) terms following WSSV challenge were identified and interactions of these transcripts with differentially expressed regulatory miRNAs were predicted. Comparison of the molecular responses of C. maenas (as a resistant species) to the molecular mechanisms underpinning disease progression in the highly susceptible P. vannamei was undertaken using a previously published dataset ( 8 ), in which global mRNA and miRNA transcription was investigated over the initial 36 hours following experimental WSSV infection. Our data demonstrate that the molecular responses of C. maenas to WSSV are distinct to those identified in P. vannamei and offer insights into the temporal differences that can be found between resistant and susceptible hosts infected with WSSV.…”

Metabolic reprogramming in crustaceans: A vital immune and environmental response strategy

“…japonicus 49 and Pacific oysters Crassostrea gigas , 50 indicating that viruses can exploit VDAC. Recently, Millard et al revealed that in addition to cytoskeleton remodelling and changes in phagocytic activity that aids entry and translocation of WSSV, miRNA‐induced metabolic shifts also occur, indicating that miRNA‐induced metabolites participate in host–viral interactions 51 …”