Towards understanding the role of extracellular polymeric substances in cyanobacterial Microcystis aggregation and mucilaginous bloom formation

•The quantitative role of EPS matrix in Microcystis aggregation and bloom formation was studied.•The aggregation potential of Microcystis samples decreased by 27.6-57.4% after EPS extraction.•Increased energy barrier and second energy minimum accounted for the deteriorated aggregation.•The predominant energy contribution transformed from TB-EPS to LB-EPS during the bloom formation.•A conceptual model about EPS function in Microcystis aggregation and bloom formation was proposed.

The development of mucilaginous cyanobacterial Microcystis blooms is a serious environmental and ecological problem, and information on the bloom-formation mechanism has been lacking until now. The aggregation of microbial cells was attributed to the matrix of extracellular polymeric substances (EPS). In this study, the quantitative role of EPS matrix in Microcystis aggregation and mucilaginous bloom formation was investigated. The results showed that when EPS matrix was extracted, the aggregation abilities decreased by 27.6% and 57.4% for the lab-cultured Microcystis suspension and the field-sampled Microcystis aggregates, respectively. The extended DLVO theory revealed that EPS extraction increased the energy barrier and the values of the second energy minimum, which accounted for the deteriorated aggregation. Further analysis showed an increasing attraction energy of EPS matrix during the Microcystis bloom development, whereas the predominant contribution originated from tightly bound EPS (TB-EPS) and loosely bound EPS (LB-EPS) for the lab-cultured and field-sampled Microcystis samples. The heterogeneous energy contribution of EPS subfractions was found to be associated with the variations in organic contents. Specifically, Microcystis aggregates exhibited a higher organic content of TB-EPS than of LB-EPS compared with the lab-cultured Microcystis suspension, whereas organic content in only the LB-EPS fraction for the bloom samples was significantly higher (p < 0.01) than that of the Microcystis aggregates. Based on these results, a conceptual model of EPS function was proposed in which TB-EPS plays an important role in the formation of Microcystis aggregates, after which LB-EPS contributed to the subsequent development from Microcystis aggregates to mucilaginous bloom formation.

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