Efficient inactivation of harmful algae K. mikimotoi by a novel algicidal bacterium via a rare direct contact pathway: Performances and mechanisms

Abstract

Harmful algal blooms (HABs) caused by Karenia mikimotoi have posed great threats to marine ecosystems, and algal inactivation by symbiotic bacteria has been recognized as environmental benign methods for controlling HABs. However, the identified algicidal bacteria for K. mikimotoi is limited and exclusively based on indirect algicidal pathways, which may cause secondary pollution due to releasing toxic algicidal agents. In this study, a novel strain of algicidal bacteria Tenacibaculum sp. GD3 was isolated from the phycosphere of K. mikimotoi. The bacterial strain GD3 could achieve 92.6 % of inactivation efficiency against K. mikimotoi within 8 h of co-culturing period, which outperformed those in existing literatures reported so far. The algicidal mechanisms were revealed to be a rare direct cell-to-cell contact pathway, and the GD3 could grow by utilizing metabolites from K. mikimotoi, exhibiting excellent bacterial adaptability in the phycosphere. Cell morphology changes were monitored by live cell imaging system combined with SEM and TEM observations, which showed that the GD3 was first attached to the algal cell membrane, followed by lipid peroxidation and lysis of membrane protein. Oxidative stress responses were induced as reveled by up-regulation of intracellular ROSs and antioxidant enzyme activity. Photosynthetic parameters including rETRmax, Fv/Fm, YII and NPQ were reduced, and expression of functional genes involved in decomposition of chlorophyll and cell wall was significantly suppressed. Moreover, the intracellular release profile and acute toxicity assessment indicated that the GD3 could also detoxify the K. mikimotoi cultures and the released biomolecules would not cause adverse effect to marine environment. This study not only provides a novel algicidal bacterium against K. mikimotoi via a rare direct mode, but also helps to better understand the algicidal mechanisms at physiological and genetic level, thus moving forward the areas of HABs control by microbiological strategies.