Environmental factors promote pathogen-induced skin ulceration syndrome outbreak by readjusting the hindgut microbiome of Apostichopus japonicus

Abstract

The synergistic effect of pathogen infection and environmental change cause a disease outbreak in many marine animals, including skin ulceration syndrome (SUS) in sea cucumber (Apostichopus japonicus). Emerging evidence has also linked the important roles of gut microbiota in influencing disease among invertebrates. However, the connection between them is largely unknown. Here, we first conducted Illumina sequencing of the bacterial 16S rRNA gene to investigate the common alteration of the hindgut microbiota in SUS-diseased sea cucumber under four different stress conditions (high temperature, mechanical damage, nitrite-N, and ammonium) combined with Vibrio splendidus exposure. Results showed that the abundances of Firmicutes, Actinobacteria, and Deltaproteobacteria in each environmental stress group were lower, and the gut microbial diversity profoundly declined. The mechanical damage group had the lowest decrease compared among the environmental stress groups. Under environmental stress, a significant increase in keystone species, especially Flavobacteriaceae, Pelagimonas, Vibrio splendidus, Vibrio cyclitrophicus, and Bacillus cereus, was also detected. At the same time, the abundance of V. splendidus was higher in the four environmental stress groups than in the V. splendidus immersion group. The abundance of V. splendidus was the highest in the mechanical damage group. Kyoto Encyclopedia of Genes and Genomes analysis indicated that immune system and cell communication (focal adhesion, tight junction, and adherens junction) pathways significantly decreased in each stress group. Our results confirmed that complex environmental factors destroy intestinal flora and provided a global understanding of the environmental factors that induce disease in sea cucumber.