Multi-omics analysis reveals the pathobiome-host interactions in the bleaching disease of the seaweed Saccharina japonica.

backgroundThe emerging concept of the pathobiome has revolutionized our understanding of disease etiology by emphasizing the complex interactions between multiple pathogens and their hosts during disease progression. Although significant advancements have been made in characterizing the pathobiome in human, animal, and plant diseases, the pathobiome associated with seaweed diseases remains unexplored. Saccharina japonica, a commercially important farmed seaweed, has increasingly suffered from bleaching disease during its nursery stage, severely compromising the supply of healthy sporelings and sea field cultivation. Despite its significant economic consequences, the pathobiome associated with this bleaching disease and its interactions with the host remain unclear, posing a major challenge for disease control.

resultsThrough multi-omics and meta-omics analyses, we identified the pathobiome associated with bleaching disease in S. japonica and elucidated its interactions with the host. The pathobiome is dominated by the core taxa Bin_7 (Glaciecola sp.), Bin_12 (Arenicella sp. 017854775), and Bin_22 (Arenicella sp.), which employ virulence mechanisms such as chemotaxis, motility, and toxin secretion to initiate infection. In response, the host S. japonica activates a multifaceted defense, including mechanisms like cell wall strengthening, reactive oxygen species bursts, and antibiotic production to combat the invading pathobiome. To counteract these host defenses, the core pathobiome taxa upregulate genes associated with antioxidant enzymes and antibiotic resistance, enabling their establishment and persistence within the host.

conclusionsThis study provides the first analysis of the pathobiome in seaweed diseases. By identifying the core taxa of the pathobiome, their virulence mechanisms, and the host defense responses, we elucidate the pathobiome-host interactions underlying S. japonica bleaching disease. These findings significantly advance our understanding of the pathobiome in seaweed diseases and lay the groundwork for developing targeted strategies to control the bleaching disease in seaweed aquaculture. Video Abstract.