Panoptic elucidation of algicidal mechanism of Raoultella sp. S1 against the Microcystis aeruginosa by TMT quantitative proteomics

Abstract

Harmful algal blooms (HABs) due to eutrophication are becoming a serious ecological disaster worldwide, threatening human health and the optimal balance of aquatic ecosystems. The traditional approaches to eradicate HABs yield several drawbacks in practical application, while microbial algicidal technology is garnering mounting recognition due to its high efficiency, eco-friendliness, and low cost. In our previous study, we isolated a bacterium strain Raoultella sp. S1 from eutrophic water with high efficiency of algicidal properties. This study further investigated the flocculation and inactivation efficiency of S1 on Microcystis aeruginosa at different eutrophic stages by customizing the algal cell densities. The supernatant extract of S1 strain exhibited remarkable flocculation and inactivation effects against low (1 × 106 cell/mL)and medium (2.7 × 106 cell/mL)concentrations of algal cells, but unexceptional for higher densities. The results further revealed that algal cells at low and medium counts manifested a more apparent antioxidant defense response, while the photosynthetic efficiency and relative electron transport rate were considerably reduced within 24 h. TEM observations confirmed the disruption of thylakoid membranes and cell structure of algal cells by algicidal substances. Moreover, TMT proteomics revealed alterations in protein metabolic pathways of algal cells during the flocculation and lysis stages at the molecular biological level. This signified that the disruption of the photosynthetic system is the core algicidal mechanism of S1 supernatant. In contrast, the photosynthetic metabolic pathways in the HABs were significantly upregulated, increasing the energy supply for the NADPH dehydrogenation process and the upregulation of ATPases in oxidative phosphorylation. Insufficient energy provided by NADPH resulted in a dwindled electron transport rate, stagnation of carbon fixation in dark reactions, and blockage of light energy conversion into chemical energy. Nonetheless, carbohydrate metabolism (gluconeogenesis and glycolysis) proteins were down-regulated and hampered DNA replication and repair. This study aided in unveiling the bacterial management of eutrophication by Raoultella sp. S1 and further arrayed the proteomic mechanism of algal apoptosis.