Divergent proteomics response of Apostichopus japonicus suffering from skin ulceration syndrome and pathogen infection.

Skin ulceration syndrome (SUS) of sea cucumber is a common and serious disease that affects the stable development of Apostichopus japonicus in the culture industry. The part of sea cucumber that suffers from major injury and is directly observed is the body wall, in which protein variations should be the most direct evidence of the disease. To understand the response mechanisms of A. japonicus in SUS progression, we investigated protein changes in the body wall of diseased A. japonicus induced by Vibrio splendidus and individuals with natural diseases by isobaric tags for relative and absolute quantification (iTRAQ). About 119 proteins were identified in the two iTRAQ groups. A comparison of the protein expression profiles among two SUS conditions revealed that the mode of action induced by V. splendidus (Vs-SUS) was completely different from those in individuals with natural disease (ND-SUS). Most of the differentially expressed proteins (DEPs) (33 in 37 DEPs) were significantly depressed in the Vs-SUS group. Only 13 proteins in 27 DEPs showed similar trend to those in the ND-SUS group. Many important proteins involved in major intercellular signaling pathways associated with SUS disease were identified based on the KEGG and GO database search. Many proteins were located in the mitochondria and mainly involved in the oxidative stress pathway. Glutathione metabolism pathway was associated with reactive oxygen (ROS) production in the ND-SUS group. In the Vs-group, most of the proteins were concentrated in the cytoplasm and were related to immunity and extracellular matrix stability. In the ND-SUS group, the activity of key enzymes (CAT, GPx) that eliminate mitochondrial ROS production and structural stable protein (HSP60, HSP10) decreased, whereas those of complement proteins (C3, C3-2) that promoted ROS production was upregulated. This finding supported that oxidative damage caused by ROS might be the main effector for SUS in the ND-SUS group. The challenge with V. splendidus led to the breakdown of the defense capability of sea cucumber and suppressed the expression of immune-related proteins, such as C-type lectin, caspase, STAT, and cystatin. The downregulation of TIMP led to MMP1 overexpression. Members of the MMP family could directly degrade the extracellular matrix, which may be the main reason for the cell matrix degradation and induced SUS disease in the Vs-SUS group. Hence, ROS and extracellular matrix degradation enzymes could play important roles in the formation of SUS in sea cucumber. Results provide insights into the complex molecular mechanism of SUS in sea cucumber.