**1. Introduction**

Clean drinking water plays a critical role in human physical health and welfare [1]. Lakes are the most important clean drinking water sources in China because they can provide a relatively stable water supply with few nature fluctuations (i.e., floods, droughts, and freezing) [2]. Lake Taihu (30◦05 –32◦08 N, 119◦08 –121◦55 S) is the third largest freshwater lake in China. The lake watershed covers approximately 36,500 km<sup>2</sup> and is an important drinking water source for more than 10 million people and several modern cities, such as Shanghai, Wuxi, and Suzhou. Moreover, Lake Taihu also serves numerous industrial, agricultural, and municipal activities [3]. However, harmful cyanobacteria blooms caused by the phytoplankton *Microcystis* have occurred successively since 1980 in Lake Taihu, which have directly threatened the safety of drinking water and triggered serious health and social problems, particularly the "Water supply crisis" in Wuxi in 2007 [4–7]. Qin et al. [8] promoted a large-scale integrated monitoring and forecasting system for cyanobacterial bloom management in Lake Taihu, and they found that the distribution area of cyanobacterial blooms reached 997.5 km2 in 2011, which was the maximum value for the four consecutive years of monitoring (2009–2012). Generally, cyanobacterial bloom growth can be influenced by temperature, daylight, water turbulence, pH, and macronutrient. In addition, wind-induced hydrodynamic effects, such as sediment

**Citation:** Chen, J.; Zhou, Y.; Zhang, Y. New Insights into Microbial Degradation of Cyanobacterial Organic Matter Using a Fractionation Procedure. *Int. J. Environ. Res. Public Health* **2022**, *19*, 6981. https:// doi.org/10.3390/ijerph19126981

Academic Editors: Alban Kuriqi and Luis Garrote

Received: 7 May 2022 Accepted: 1 June 2022 Published: 7 June 2022

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resuspension and the corresponding nutrient release from the sediment–water interface, played an important role in intensifying cyanobacterial bloom expansion [9,10].

After blooms, the massive cyanobacterial biomass aggregates into scum and is then degraded by indigenous heterotrophs [11]. Large fractions of cyanobacterial organic matter are released from the biomass as dissolved organic matter (DOM) mainly via three major decline steps, which were proposed to describe the bloom decline process: scum disaggregation, colony settlement, and cell lysis in colonies [12]. Various bacteria of myxobacterium and the genera *Alcaligenes* and *Pseudomonas* and the *Cytophaga*/*Flavobacterium* group from aquatic environments were found to be lysed *Microcystis*, which is closely related to the degradation of biomass produced by cyanobacteria [13,14]. This algal-released DOM can be referred to as bulk algal-derived DOM. When large complex algal-derived DOM enters the aquatic system, it may cause oxygen depletion and cyanobacterial toxin secretion by biological activities, resulting in the appearance of a "black water mass," which may pose serious risks to aquatic plants, fish, and oxygen-sensitive invertebrates and cause mass mortality events [15–17]. The high frequency formation of a massive bloom composed of cyanobacteria of the genus *Microcystis*, which can produce potent hepatotoxins, neurotoxins, and dermatoxins and promote tumor formation (i.e., microcystins), and they finally cause damage to the liver [18,19].

Several studies have suggested that bulk algal-derived DOM is closely related to the biogeochemical cycle and energy flow of lake ecosystems, which indirectly impact human health and the dynamics and driving factors of cyanobacterial blooms [20–22]. For example, Bittar et al. [23] confirmed that extracellular and intracellular DOM were produced in axenic cultures by *Microcystis aeruginosa*, which can effectively increase the biolabile DOM (BDOM) to bacterial growth and activity in lake waters for timescales of minutes to days. Moreover, Lee et al. [24] found that algal-derived BDOM can be converted into recalcitrant organic matter (such as humic substances), which remains in the water column for a long period. On the one hand, this freshly produced BDOM would strongly influence its binding properties to heavy metals and thus their fate, mobility, and toxicity in aquatic environments; especially, the algal-derived polymeric component increases the coagulation and sedimentation rates of colloidal material and associated metals, and thus brings hidden potential dangers to benthic healthy [25,26]. On the other hand, after long-term biodegradation, progressive accumulation of algal-derived recalcitrant DOM, as disinfection by-product precursor compounds, is transformed into trihalomethanes and haloacetic acids (i.e., carcinogenic and mutagenic disinfection byproducts), which inevitably leads to increased costs of drinking water supply systems [27–29]. In addition, during the decay of cyanobacteria blooms in lake ecosystems, cyanobacteria toxins are introduced into water and could directly threaten human health [30,31].

Dissolved organic matter is a fundamental regulator of aquatic ecosystems, and algalderived DOM often dominates the DOM composition in water during algal bloom decay in Lake Taihu [32]. Several authors have studied the production of DOM with unique compositions and stoichiometries that fuel successive trophic transfers of fixed carbon through initial assimilation by heterotrophs. However, their rates of processing phytoplankton DOM are controlled to a large extent by the biological availability of cyanobacterial exudate and lysate; thus, two different cyanobacteria fractions will have implications for lake microorganisms to facilitate the efficient turnover of the highly heterogeneous cycle of available DOM [33,34]. Microbial-mediated metabolism reactions have been demonstrated to transform DOM from labile to a relatively recalcitrant state. This process is associated with nutrient recycling, greenhouse outgassing, and microbial secondary production, affecting microbial succession, as reflected in the taxonomic composition and functional diversity, as well as the growth rates of specific groups [35–39].

For lake ecosystems, especially eutrophic lakes, the nutrients needed to maintain the system largely depend on the internal circulation and regeneration of the system rather than external input [40]. Among them, the degradation of cyanobacterial organic matter and the release process of nutrients, which are important carriers of nutrients in water, may be important sources of active nutrients in water [41]. Algal-derived DOM has generally been used to represent the heterogeneous matrix for the entire decomposition of cyanobacterial blooms; however, most studies have focused primarily on the environmental behavior of bulk algal-derived DOM or the response of the interaction between bulk algal-derived DOM and water contaminants. However, the relationship between released DOM refers to the different fractions of cyanobacterial organic matter, and there have been few studies on reproduced nutrient and microbial secondary production (i.e., ecological effect) following the cyanobacterial cell lysis mechanism.

Therefore, the objective of this study was to gain new insight into the role of molecular weight-fractionated cyanobacterial organic matter on DOM mineralization, sequestration, and related nutrients. We set up a medium-volume, long-term incubation experiment and combined it with a fractionation procedure to investigate how DOM from lysed cyanobacteria cells impacts the variation of the microbial population, and how processing of algal-derived DOM impacts nutrient mineralization by comparative analysis. The results will provide data support for the ecological effects of cyanobacteria degradation.

## **2. Materials and Methods**
