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

Jialin Shi; Wanjun Wang; Fan Wang; Shien Lei; Shaobin Shao; Chao Wang; Guiying Li; Taicheng An

doi:10.1016/j.scitotenv.2023.164401

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

Sci Total Environ. 2023 Sep 20:892:164401. doi: 10.1016/j.scitotenv.2023.164401. Epub 2023 May 27.

Authors

Jialin Shi¹, Wanjun Wang², Fan Wang¹, Shien Lei¹, Shaobin Shao¹, Chao Wang¹, Guiying Li¹, Taicheng An¹

Affiliations

¹ Guangdong Key Laboratory of Environmental Catalysis and Health Risk Control, Guangdong Hong Kong-Macao Joint Laboratory for Contaminants Exposure and Health, Institute of Environmental Health and Pollution Control, Guangdong University of Technology, Guangzhou 510006, China; Guangzhou Key Laboratory Environmental Catalysis and Pollution Control, Key Laboratory of City Cluster Environmental Safety and Green development, School of Environmental Science and Engineering, Guangdong University of Technology, Guangzhou 510006, China.
² Guangdong Key Laboratory of Environmental Catalysis and Health Risk Control, Guangdong Hong Kong-Macao Joint Laboratory for Contaminants Exposure and Health, Institute of Environmental Health and Pollution Control, Guangdong University of Technology, Guangzhou 510006, China; Guangzhou Key Laboratory Environmental Catalysis and Pollution Control, Key Laboratory of City Cluster Environmental Safety and Green development, School of Environmental Science and Engineering, Guangdong University of Technology, Guangzhou 510006, China. Electronic address: wanjun@gdut.edu.cn.

PMID: 37247737
DOI: 10.1016/j.scitotenv.2023.164401

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 rETR_max, F_v/F_m, 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.

Keywords: Algicidal efficiency; Direct contact; Karenia mikimotoi; Physiological response; Tenacibaculum.

MeSH terms

Antioxidants / pharmacology
Bacteria
Dinoflagellida* / physiology
Ecosystem*
Harmful Algal Bloom
Photosynthesis

Substances

Antioxidants