Algicidal mechanism of Raoultella ornithinolytica against Microcystis aeruginosa: Antioxidant response, photosynthetic system damage and microcystin degradation

Abstract

Water eutrophication caused by harmful algal blooms (HABs) occurs worldwide. It causes huge economic losses and has serious and potentially life-threatening effects on human health. In this study, the bacterium Raoultella sp. S1 with high algicidal efficiency against the harmful algae Microcystis aeruginosa was isolated from eutrophic water. The results showed that Raoultella sp. S1 initially flocculated the algae, causing the cells to sediment within 180 min and then secreted soluble algicidal substances that killed the algal cells completely within 72 h. The algicidal activity was stable across the temperature range −85.0 to 85.0 °C and across the pH range 3.00–11.00. Scanning electron microscopy (SEM) revealed the crumpling and fragmentation of cells algal cells during the flocculation and lysis stages. The antioxidant system was activated under conditions of oxidative stress, causing the increased antioxidant enzymes activities. Meanwhile, the oxidative stress response triggered by the algicidal substances markedly increased the malondialdehyde (MDA) and glutathione (GSH) content. We investigated the content of Chl-a and the relative expression levels of genes related to photosynthesis, verifying that the algicidal compounds attack the photosynthetic system by degrading the photosynthetic pigment and inhibiting the expression of key genes. Also, the results of photosynthetic efficiency and relative electric transport rate confirmed that the photosynthetic system in algal cells was severely damaged within 24 h. The algicidal effect of Raoultella sp. S1 against Microcystis aeruginosa was evaluated by analyzing the physiological response and photosynthetic system impairment of the algal cells. The concentration of microcystin-LR (MC-LR) slightly increased during the process of algal cells ruptured, and then decreased below its initial level due to the biodegradation of Raoultella sp. S1. To further investigate the algicidal mechanism of Raoultella sp. S1, the main components in the cell-free supernatant was analyzed by UHPLC-TOF-MS. Several low-molecular-weight organic acids might be responsible for the algicidal activity of Raoultella sp. S1. It is concluded that Raoultella sp. S1 has the potential to control Microcystis aeruginosa blooms.