Dissolved organic carbon spurs bacterial-algal competition and phosphorus-paucity adaptation: Boosting Microcystis' phosphorus uptake capacity

Tingting Li; Longqian Xu; Wenxuan Li; Chengxian Wang; Karina Yew-Hoong Gin; Xiaoli Chai; Boran Wu

doi:10.1016/j.watres.2024.121465

Dissolved organic carbon spurs bacterial-algal competition and phosphorus-paucity adaptation: Boosting Microcystis' phosphorus uptake capacity

Water Res. 2024 May 15:255:121465. doi: 10.1016/j.watres.2024.121465. Epub 2024 Mar 13.

Authors

Tingting Li¹, Longqian Xu¹, Wenxuan Li², Chengxian Wang¹, Karina Yew-Hoong Gin³, Xiaoli Chai⁴, Boran Wu⁵

Affiliations

¹ State Key Laboratory of Pollution Control and Resource Reuse, College of Environmental Science and Engineering, Tongji University, 1239 Siping Road, Shanghai, 200092, China.
² State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing, 100012, China; State Environmental Protection Key Laboratory of Ecological Effect and Risk Assessment of Chemicals, Chinese Research Academy of Environmental Sciences, Beijing, 100012, China.
³ NUS Environmental Research Institute, National University of Singapore, 1 Create Way, #15-02, Singapore, 138602, Singapore.
⁴ State Key Laboratory of Pollution Control and Resource Reuse, College of Environmental Science and Engineering, Tongji University, 1239 Siping Road, Shanghai, 200092, China; Shanghai Institute of Pollution Control and Ecological Security, Shanghai, 200092, China.
⁵ State Key Laboratory of Pollution Control and Resource Reuse, College of Environmental Science and Engineering, Tongji University, 1239 Siping Road, Shanghai, 200092, China; Shanghai Institute of Pollution Control and Ecological Security, Shanghai, 200092, China. Electronic address: boranwu@tongji.edu.cn.

PMID: 38569356
DOI: 10.1016/j.watres.2024.121465

Abstract

Dissolved organic carbon (DOC) can alter the availability of background nutrients by affecting the proliferation of heterotrophic bacteria, which exerts a notable influence on algal growth and metabolism. However, the mechanism of how allochthonous DOC (aDOC) precipitates shifts in bacterial-algal interactions and modulates the occurrence of cyanobacteria blooms remains inadequately elucidated. Therefore, this study investigated the relationship between bacteria and algae under aDOC stimulation. We found that excess aDOC triggered the breakdown and reestablishment of the equilibrium between Microcystis and heterotrophic bacteria. The rapid proliferation of heterotrophic bacteria led to a dramatic decrease in soluble phosphorus and thereby resulted in the inhibition of the Microcystis growth. When the available DOC was depleted, the rapid death of heterotrophic bacteria released large amounts of dissolved phosphorus, which provided sufficient nutrients for the recovery of Microcystis. Notably, Microcystis rejuvenated and showed higher cell density compared to the carbon-absent group. This phenomenon can be ascribed that Microcystis regulated the compositions of extracellular polymeric substances (EPS) and the expression of relevant proteins to adapt to a nutrient-limited environment. Using time of flight secondary ion mass spectrometry (TOF-SIM) and proteomic analysis, we observed an enhancement of the signal of organic matter and metal ions associated with P complexation in EPS. Moreover, Microcystis upregulated proteins related to organic phosphorus transformation to increase the availability of phosphorus in various forms. In summary, this study emphasized the role of DOC in algal blooms, revealing the underestimated enhancement of Microcystis nutrient utilization through DOC-induced heterotrophic competition and providing valuable insights into eutrophication management and control.

Keywords: Algal bloom; Allochthonous organic carbon; Ion micro distribution; Microcystis; Phosphorus availability.