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Article

Effects of Algal Utilization of Dissolved Organic Phosphorus by Microcystis Aeruginosa on Its Adaptation Capability to Ambient Ultraviolet Radiation

by
Lingxiao Ren
1,*,
Jing Huang
2,*,
Huagang Zhu
3,
Wei Jiang
4,
Haoyu Wu
1,
Yuyang Pan
1,
Yinghui Mao
1,
Minghan Luo
1 and
Taeseop Jeong
5
1
School of Environmental Engineering, Nanjing Institute of Technology, Nanjing 211167, China
2
Beijing Enterprises Changbao Nanjing Water Group Co., Ltd., Nanjing 210000, China
3
Jiangsu Provincial Water Conservancy Survey and Design Institute Co., Ltd., Yangzhou 225000, China
4
Jiangsu Hehai⊕ Environmental Design Institute Co., Ltd., Nanjing 210000, China
5
Department of Environmental Engineering, Jeonbuk National University, Jeonju 561-756, Korea
*
Authors to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2022, 10(9), 1257; https://doi.org/10.3390/jmse10091257
Submission received: 17 July 2022 / Revised: 23 August 2022 / Accepted: 31 August 2022 / Published: 6 September 2022
(This article belongs to the Special Issue Marine Harmful Algae)
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Abstract

:
Phosphorus (P) plays an important role in eutrophication and algal adaptation to environmental stresses; therefore, a better understanding of the impact of P is essential to control cyanobacterial bloom. In this study, Microcystis aeruginosa is treated with 5 h of ambient irradiation in the culture medium with different availabilities of dissolved organic P (DOP) and dissolved organic matter (DOM) to explore algal physiological responses. Compared to photosynthetically active radiation (PAR), ambient UV-A and UV-B radiation exerted oxidative stresses and has inhibitive effects on the growth and photosynthesis of M. aeruginosa. However, M. aeruginosa had a strong adaptation capability, and the negative effects of UV radiation can be alleviated with DOM addition in the DOP-rich medium. The adaptation of M. aeruginosa to UV radiation in the DOP-rich waters can be mainly achieved through hydrolysis of DOP and metabolism of dissolved inorganic P (DIP), and the DOP utilization behaviors of M. aeruginosa might greatly affect algal UV adaptation capability. In the DOP-rich medium without DOM, the great inactivation of algal alkaline phosphatase (APase) after UV radiation could result in worse affinity for DOP, slower DOP uptake and lower cellular P quota. Consequently, the P demand of M. aeruginosa could not be satisfied for UV adaptation processes, including decreasing UV-induced damages and promoting self-repair. However, DOM could act as an antioxidant and significantly decrease APase inactivation of UV-radiated M. aeruginosa. In the DOP-rich medium with DOM, DOP utilization by M. aeruginosa in the UV-A and UV-B treatments is promoted and algal demand for P is satisfied for its adaptation, such as enhanced production of photosynthetic pigments, increased superoxide dismutase (SOD) activity, recovery of photosynthetic efficiency, etc. Overall, our findings indicate the close relationship between algal DOP utilization and the adaptation to ambient UV radiation of typical cyanobacteria in DIP-limited and DOP-enriched natural waters.

1. Introduction

Eutrophication is a significant threat to aquatic ecosystems and harmful algal blooms (HABs) are often a troubling indicator of accelerating eutrophication [1], which could adversely affect the water quality and sustainability of impacted systems [2,3]. For a long time, cyanobacteria ranked prominently among the causes of problems with HABs from environmental degradation and human health perspectives [4,5]. Consequently, studies have focused on the growth patterns and physiology of Microcystis in recent years, which is one of the dominant cyanobacterial genera in natural waters and can produce many secondary metabolites such as microcystins and allelopathy exudates [6,7,8]. Especially, microcystins have been detected in coastal environments across the world, and scholars have strongly suggested increased monitoring and research efforts to prevent ecological problems associated with toxic Microcystis in both freshwater and coastal environments [9,10]. Results showed that Microcystis has developed a range of adaptive strategies to defend against complex environmental stresses, which are vital for its proliferation [11,12,13].
In all kinds of environmental factors, light has a marked impact on the photosynthesis and growth of cyanobacteria, which is highly dependent on the intensity, exposure time and wavelength of light [14,15,16]. For example, photosynthetically active radiation (PAR; 400–700 nm) in the sunlight is essential for the metabolism of photosynthetic organisms. However, increased solar ultraviolet (UV) radiation is reaching the earth’s surface due to serious stratospheric ozone depletion and other factors [12,17]. Especially, the complex effects of UV radiation on phytoplankton have received considerable attention, and most studies have used Microcystis as a model species [13,18]. For example, elevated CO2 and other environmental factors could exhibit interactive effects on the sensitivity of marine primary producers to ultraviolet radiation [18], which was helpful in explaining the effects of global climate change on aquatic food chains in the ocean. The extracellular polysaccharides (EPS) of Microcystis could facilitate the aggregation of algal cells, which was helpful in reducing the negative or harmful effects of UV radiation [19,20]. Moreover, the synthesis of microcystin by Microcystis could contribute to the higher fitness of algal cells under enhanced light irradiation through a covalent interaction with the cysteine residue of proteins [21]. These results indicate that adaptation of Microcystis to UV radiation could be a complicated process, but many studies have used enhanced UV radiation rather than ambient irradiance in natural ecosystems [22,23]. Moreover, less attention was paid to the effects of the availability of macronutrients and other common substances in water on the UV adaptation capability of typical cyanobacterial species.
Phosphorus (P) is an essential macro-nutrient for algae, and the important roles of P for algal growth have been extensively studied. It was indicated that P availability could influence the physiological processes and adaptation of cyanobacteria to environmental stresses [6,24,25]. For example, higher dissolved inorganic P (DIP, mainly as phosphate) in water could enhance the algal production of photosynthetic pigments and the antioxidase activity of UV-radiated M. aeruginosa, leading to a higher adaptation capability [26]. However, DIP shortage has become a common phenomenon in many systems and algae often produced alkaline phosphatase (APase) to hydrolyze dissolved organic P (DOP) for DIP, which was considered an indirect process [27,28] and it might result in different manners for algal adaptation to enhanced UV radiation. Especially, aquatic ecosystems in the middle and low latitudes are more threatened by light stress [29,30], and Microcystis often occurs as the surface blooms that encounter enhanced UV radiation [31,32]. However, the frequency and intensity of Microcystis blooms are still maintained at high levels in the eutrophic lakes, and it is crucial to intensively study the adaptation of Microcystis to UV radiation. Moreover, APase was sensitive to UV radiation and the inactivation of APase might affect P utilization by Microcystis [33,34], but there are few relevant studies. Meanwhile, high contents of dissolved organic matter (DOM) often exist in eutrophic freshwater and marine ecosystems [35,36]. It was reported that DOM could absorb photons and encounter many reactions. However, these results are often contradictory [37,38], and the effects of DOM on algal utilization of DOP should gain considerable attention. Consequently, the existing studies might not adequately explain the relationship between algal adaptation to UV radiation and the evolution of the water environment from the perspective of engineering control.
In this study, we selected M. aeruginosa and investigated its physiological responses after short-term irradiation in the culture medium with different availability of DOP and DOM. The main aims were the following: (i) analyze the effects of UV radiation on the growth and photosynthesis of M. aeruginosa; (ii) explore the relationships of algal UV adaptation capability with its DOP utilization behavior.

2. Materials and Methods

2.1. Preparation of Algae Cultures and DOM Solution

A common unicellular bloom-forming cyanobacteria (M. aeruginosa FACHB 905) was selected and obtained from the Freshwater Algae Culture Collection of the Institute of Hydrobiology, Chinese Academy of Sciences (FACHB). Preliminary culture of this strain was operated and the exponential growth of algae was maintained by transferring 5 mL of growing cultures to fresh standard BG11 medium in the Erlenmeyer flasks every 8–10 days [39]. The preliminary culture was performed under sterile conditions and flasks were placed at 25 °C under 40 μmol photons m−2 s−1 PAR with the cool white fluorescent lamps (light/dark regime of 12 h:12 h) in the illuminated incubator (GZX-250BS-II, Cimo, Shanghai, China). After three or four times of inoculation, M. aeruginosa was cultured for enlargement and cell density was monitored until it exceeded 2.0 × 107 cells mL−1. Then, algal cells were harvested by centrifugation (5000× g for 10 min, 4 °C), washed with ultrapure water and suspended in P-free BG11 medium for experiment in this study. The detailed procedures can be seen in Ren et al. [40].
Since humic substances often occur from plant or animal remains through biological or chemical transformations and are known as the main pool of DOM [41], DOM solution was directly obtained using humic acids (HA) from Sigma-Aldrich in our study. HA was dissolved in the ultrapure water at pH = 10.0 and the ultrasonic treatment was conducted intermittently until pH remained stable. Then, the solutions were adjusted to pH = 7.0, filtered (0.2-μm, Whatman, Little Chalfont, Buckinghamshire, UK) and preserved in the dark at low temperatures (4 °C). The total organic carbon (TOC) content of DOM stock solution was about 150.0 mg L−1, which was determined by a TOC analyzer (Shimadzu, Kyoto, Japan).

2.2. Experimental Setup

2.2.1. Effects of Irradiation on M. aeruginosa

After preliminary culture, culture enlargement and preservation, the prepared M. aeruginosa was collected by centrifugation (5000× g for 10 min, 4 °C) and transferred into different kinds of culture media for formal experiments. The following four regimes were used for different groups: without DOM in DOP-rich medium (NM-P group), with DOM in DOP-rich medium (M-P group), without DOM in DOP-free medium (NM-NP group), with DOM in DOP-free medium (M-NP group). Details can be seen in the Supplementary Materials (SM) and a schematic diagram of experiment is shown in Figure S6.

2.2.2. Effects of Irradiation on APase Inactivation

After preliminary culture, culture enlargement and preservation, the exponentially growing cells were harvested by centrifugation (5000× g for 10 min, 4 °C) and suspended in the Tris-HCl buffer solution (20 mmol L−1, pH 8.2). Then, enzyme solution containing M. aeruginosa APase was also prepared and it was used for irradiation experiments. Details can be seen in Supplementary Materials.

2.3. Analytical Methods of Parameters

2.3.1. Cell Density and Photosynthetic Efficiency

Subsamples were taken immediately after irradiation treatment and every two days for determining cell density. Cells were enumerated by using a flow cytometer (CytoFLEX S, Beckman Coulter, Fullerton, CA, USA). Meanwhile, a Phyto-PAM fluorometer (Hein Walz, Effeltrich, Germany) was used to regularly determine the effective quantum yield (Fv/Fm) of M. aeruginosa [42,43].

2.3.2. ROS in Cells and Superoxide Dismutase (SOD) Activity

At the beginning and after 5 h of light exposure, subsamples were collected to determine ROS in algal cells and activity of SOD. The details can be seen in Supplementary Materials.

2.3.3. Contents of Photosynthetic Pigments

At the beginning and after 5 h of light exposure, subsample was collected and filtrated through 0.2-mm mixed cellulose ester filters (Whatman, Little Chalfont, Buckinghamshire, UK) to determine the contents of photosynthetic pigments (pg cell−1) in single cells, including chlorophyll a (Chl-a), carotenoid (CAR) and phycocyanin (PC). The details can be seen in Supplementary Materials.

2.3.4. Kinetic Parameters of DOP Uptake

At the beginning and after light exposure, the kinetic parameters of DOP uptake by M. aeruginosa were determined to investigate the combined effects of the irradiation treatments and DOM addition. The methods were modified from Fu et al. [44] and details can be seen in Supplementary Materials.

2.3.5. P Fractions and Cellular P Quota

Based on inductively coupled plasma (ICP) method, DOP and DIP concentrations in the culture medium were measured. Meanwhile, the total amount of P associated with M. aeruginosa cells was determined and cellular P quota was estimated (pg cell−1). Detailed methods can be seen in Ren et al. [26].

2.3.6. Morphology of Algae Cells

To explore the microstructure of M. aeruginosa after radiation, scanning electron microscopy (SEM) analysis was conducted on Day 1 when algae cells were collected by centrifugation (5000× g for 10 min, 4 °C) and fixed with 2.5% glutaraldehyde solution for 24-h. After rinsing with phosphate buffer solution (PBS), cells were dehydrated successively by a series of ethanol solutions in a vacuum drier (50%, 70%, 90% and 100%). Subsequently, the treated cells were mounted on copper stubs, coated with spray gold and examined through an SEM (S-4800, Hitachi, Tokyo, Japan) at 5 kV.

2.3.7. Estimation of APA and Its Inactivation Rates

After regular collection of algal cultures or the enzyme solutions, APA was estimated using p-nitrophenylphosphate (pNPP) as the substrate [45]. The inactivation rates of APase (Kina) were calculated as follows: Kina = (ln APAt − ln APA0)/T, where APAt and APA0 are the measured APA and initial APA, respectively, and T was the irradiation time [46].

2.4. Statistical Analysis

All experiments were conducted in triplicate and means ± standard deviations of three replicates were calculated. The parametric three-way repeated-measures analysis of variance (RM-ANOVA) was used to determine the effects of irradiation treatments, DOM and sampling time on the cell density, photosynthetic parameters, cellular P quota, APA of algal samples and APase inactivation. Meanwhile, two-way RM-ANOVA was used to determine the effects of irradiation and DOM on the photosynthetic pigments, ROS, algal SOD activity and DOP uptake rates. Data were tested for normality and the variance assumptions of parametric ANOVA, and no data transformation was needed. If the interaction factor was significant at p < 0.05, a one-way ANOVA followed by Tukey’s test was adopted to determine where differences lie. All statistical analyses were performed using SPSS 22.0 (Chicago, IL, USA).

3. Results

3.1. Effects on the Growth of M. aeruginosa

In our previous experiment [26], higher P availability in the water could significantly alleviate the negative effects of UV radiation on algal growth (Figure 1a,b), leading to a better adaption capability of M. aeruginosa. Similar variation patterns of cell density were observed in this study when the cell density of M. aeruginosa did not change significantly (p > 0.05) after 5 h of PAR, UV-A or UV-B radiation and the differences were evident (p < 0.05) during the recovery period.
In the NM-P group, M. aeruginosa grew persistently during the whole incubation but the inhibition effects of UV radiation became significant after Day 2, which was largest in the UV-B treatment (p < 0.05). Compared to the results using DIP, high DOP contents in the water could not eliminate the negative effects of UV radiation on algal growth (Figure 1c). However, with DOM addition in the M-P group, the maximum cell density in the PAR treatment was similar to that in the NM-P group, and M. aeruginosa growth in all three treatments was comparable (p > 0.05) during the incubation (Figure 1d). In the NM-NP and M-NP groups, M. aeruginosa grew slowly in the PAR treatment and UV radiation showed remarkable inhibition effects on algal growth when the impact was greater in the UV-B treatment (p < 0.05; Figure 1e,f). Moreover, DOM addition did not significantly change the effects of irradiation on algal growth (p > 0.05) in the DOP-free medium (NM-NP and M-NP groups).

3.2. Effects on Algal Photosynthetic Efficiency

Compared to PAR, 5 h of UV radiation might directly impair the normal function of the algal photosynthetic system, and Fv/Fm of M. aeruginosa both declined significantly after UV radiation under different experimental conditions (p < 0.05; Figure 2). However, the degree of decline and the recovery efficiency of algal Fv/Fm after withdrawing UV radiation showed a significant difference (p < 0.05).
In the NM-P group, Fv/Fm remained relatively constant after PAR treatment, and Fv/Fm decreased by 58.2% and 78.2% after UV-A and UV-B radiation, respectively. Then, Fv/Fm increased to 74.5% and 63.6% of the initial value on Day 1 in the UV-A and UV-B treatments, respectively, and the differences among treatments were not observed until Day 7. With DOM addition in the M-P group, Fv/Fm decline decreased greatly after UV radiation, and Fv/Fm could recover and exceed 95% of the initial value on Day 1. Then, Fv/Fm in three treatments were similar during the subsequent incubation.
In the DOM-free medium, the declines in Fv/Fm were comparable in the NM-NP and M-NP groups after UV radiation, when Fv/Fm decreased by about 70% and 90% in the UV-A and UV-B treatments, respectively. Moreover, the recovery of Fv/Fm and its variation patterns after withdrawing UV radiation also did not differ significantly (p > 0.05) in the NM-NP and M-NP groups. In comparison, Fv/Fm showed a decline in the PAR treatment during the recovery period, which could be affected by nutrient deficiency.

3.3. Antioxidant Responses and Photosynthetic Pigments

3.3.1. ROS in the Cells and SOD Activity

Compared to the initial values, ROS content in the cells of M. aeruginosa and its SOD activity changed slightly after PAR treatment in all four groups (Figure 3). In comparison, ROS in algal cells were enhanced greatly after 5 h of UV radiation, and they were significantly higher (p < 0.05) in the DOP-free medium (NM-NP and M-NP groups). Moreover, two distinct effects of DOM on ROS in algal cells were observed in the DOP-rich medium and the DOP-free medium. More specifically, ROS in algal cells were lower with DOM addition in the DOP-rich medium (p > 0.05; M-P group) and they were higher with DOM addition in the DOP-free medium (p > 0.05; M-NP group).
Consistent with ROS in cells, algal SOD activity remained constant after PAR treatment and M. aeruginosa could increase SOD activity after UV radiation, which was higher in the UV-B treatment (p < 0.05). In the DOP-rich medium, algal SOD activity greatly decreased with the addition of DOM (M-P group). However, in the DOP-free medium, algal SOD activity increased obviously with DOM addition (M-NP group).

3.3.2. Photosynthetic Pigments of M. aeruginosa

Chl-a contents in single cells of M. aeruginosa did not change significantly after irradiation in four groups (p > 0.05; Figure 4a), but the increase in CAR and PC contents was observed after UV radiation in the NM-P and M-P groups, which was more pronounced in the UV-B treatment (Figure 4b,c). Meanwhile, significantly higher levels of CAR and PC were observed in the M-P group (p < 0.05), and CAR and PC in single cells only increased to a lesser degree in the NM-P group. In comparison, the evident decrease of CAR and PC was observed after UV-A or UV-B radiation in the NM-NP and M-NP groups, and DOM did not show significant effects (p > 0.05).

3.4. Surface Morphology of Algal Cells

SEM images on Day 1 showed that the spherical shape of algal cells did not change greatly after PAR treatment in four groups when cell surfaces were glossy and intact (Figure 5). In the NM-P group, the intact surfaces of cells were also observed in the UV-A and UV-B treatments, and several evident wrinkles existed with clear boundaries. Meanwhile, the exterior morphology of M. aeruginosa in the UV-A and UV-B treatments was fairly glossy in the M-P group, when cells with sharp edges were easy to distinguish. In the NM-NP and M-NP groups, the evident changes of algal cells after UV radiation were observed when the surfaces were both shrunk and became rough.

3.5. Algal Utilization of DOP after Irradiation

3.5.1. Kinetic Parameters for DOP Uptake

The kinetics parameters for DOP uptake by M. aeruginosa changed slightly after PAR exposure, and they were strongly affected by the availability of DOM and DOP after UV radiation (Table 1). In the NM-P group, a significant drop in Vmax (p < 0.05, 19.8–34.2%) was observed, and Km increased significantly after UV radiation (p < 0.05), indicating the slower DOP uptake rate and the worse affinity for DOP. In comparison, Vmax increased (p < 0.05, 11.4–22.4%) after UV radiation in the M-P group and Km was less affected, indicating a faster DOP uptake rate and a better affinity for DOP.
In the NM-NP and M-NP groups, Vmax was further decreased (40.4–60.2%) after UV radiation and the increase in Km was higher compared to that in the NM-P group. In addition, Vmax and Km in the UV-A and UV-B treatments did not differ significantly (p > 0.05) in the NM-NP and M-NP groups, indicating a small effect of DOM in the DOP-free medium.

3.5.2. Cellular P Quota and P Fractions in the Medium

The fast accumulation and slow utilization of DOP by M. aeruginosa were observed in the DOP-rich medium, and results were distinct in the NM-P and M-P groups. Compared with PAR treatment, cellular P quota was lower after UV radiation in the NM-P group (p < 0.05) and the decline of DOP content in the medium was slower, with more pronounced effects in the UV-B treatment (Figure 6a). Meanwhile, the UV-radiated M. aeruginosa produced less DIP in the NM-P group compared with PAR treatment. However, the promotion effect of UV radiation on cellular P quota was observed in the M-P group, which was stronger in the UV-B treatment (Figure 6b). Compared with PAR treatment, DOP decline in the medium was also faster after UV radiation in the M-P group and DIP showed high values in all three treatments.
In the DOP-free medium (NM-NP and M-NP groups), the cellular P quota of M. aeruginosa decreased gradually in the PAR treatment, and UV radiation could promote the decline of cellular P quota (p < 0.05; Figure 6c,d), even though M. aeruginosa could not grow after UV-A or UV-B radiation. Moreover, the variation patterns of cellular P quota did not differ significantly (p > 0.05) in the NM-NP and M-NP groups.

3.6. Effects on APase Inactivation of M. aeruginosa

3.6.1. APA after Irradiation Treatments

Since the absorbance peak of M. aeruginosa-derived APase was centered around 280–315 nm and the light absorbance was lower in PAR (Figure S3), the APA of algal cultures did not change obviously after 5 h of PAR and it decreased greatly after UV-A or UV-B radiation in the NM-P group (28.4% and 40.0%; Figure 7). During the 10-day recovery period in the NM-P group, APA increased gradually, and it was always higher in the PAR treatment before Day 4. In comparison, APA decreased slightly after UV radiation in the M-P group (8.8% and 15.8%), and APA increased quickly after withdrawing UV radiation, with similar variation patterns in three treatments during the whole incubation.
In the M-NP and NM-NP groups, APA of algal cultures both increased before Day 4 and decreased afterward in the PAR treatment. In the NM-NP group, algal APA dropped by 32.8–58.4% after UV radiation and leveled off after Day 4. In the M-NP group, APA exhibited a greater decrease (42.4–85.8%) after UV radiation and the inactivation of algal APA was also higher in the UV-B treatment.

3.6.2. APA after Different Irradiation Treatments

As shown in Figure 8, the irradiation treatments and DOM had significant interactive effects (p < 0.05) on the inactivation of M. aeruginosa-derived APase, with an apparent first-order decrease in APA. In the dark, APase had good stability and its inactivation was enhanced with DOM addition (p < 0.05). Under PAR, the high persistence of APase was also observed and the effect of DOM addition on APase inactivation was slowed down. Consistent with previous results, the significant inactivation of APase emerged after UV radiation. Meanwhile, the addition of DOM could significantly suppress (p < 0.05) the inactivation of APase in the UV-A and UV-B treatments.

4. Discussion

4.1. Algal Adaptation to UV Radiation in Different Groups

Our previous study reported that short-term exposure to ambient UV radiation had inhibitory effects on the growth and photosynthesis of M. aeruginosa, and the effects could be eliminated with high DIP availability in the water [26]. Confirmed by cell density, SEM analysis and Chl-a content in single cells, UV radiation exerted similar effects on M. aeruginosa in DOP-rich waters, which referred to oxidative stresses rather than direct lethal effects [26,47]. However, the negative effects on M. aeruginosa could be eliminated with DOM addition and algal cells exhibited a stronger adaptation to UV radiation.
Previous studies have reported that UV radiation could cause the overexcitation of various substances and produce excess ROS in the algal cultures, leading to impairment of algal photosynthetic systems and slower algal growth [48,49]. Consistently, ROS contents in algal cultures were all higher after UV radiation in four groups and the surface morphology of algal cells could greatly change. However, the oxidative stresses and resulting damage could be mitigated with algal adaptive strategies, including up-regulation of SOD activity, CAR and PC synthesis, and recovery of Fv/Fm. For example, CAR and PC in algal cells could efficiently adsorb UV light and quench ROS to alleviate the photo-induced damage, and higher CAR could increase the algal utilization efficiency of light [50]. As an important biological substance, DIP directly affected algal capability to produce ATP as a substrate of phosphorylation and it also directly participated in algal adaptive processes to environmental stresses, such as energy production, resynthesis of proteins, etc. [51,52]. However, algal utilization of DOP was usually an indirect process when DOP was firstly associated with its surface phosphatase and then hydrolyzed to DIP for metabolism [28,40,53]. Combing results of cell density, Fv/Fm variation and SEM images, the stronger adaptation capability of M. aeruginosa to UV radiation was observed in the M-P group, together with the less affected APA of algal cells, enhanced DOP utilization and higher DIP production. This indicated that adaptation of M. aeruginosa to UV radiation in our study could also be mainly achieved through the hydrolysis of DOP and metabolism of DIP [54,55]. By comparison, the significant inactivation of APase after UV radiation in the NM-P group could hinder algal utilization of DOP by M. aeruginosa, resulting in the low DIP production and weaker adaptation capability of M. aeruginosa. It was highly consistent with Korbee et al. [56] that an increase in extracellular APA under UV radiation stress could constitute an additional mechanism that favored algal acclimation by augmenting inorganic P availability in the water. There were reports elsewhere about algal preferences for utilizing different forms of nutrients when they were under environmental stresses [57,58]. Especially, the UV adaptation processes of algae could result in an elevated P demand and UV-radiated M. aeruginosa might acquire more P from the surrounding environment [26]. Consequently, the poor adaptation capability of M. aeruginosa to UV radiation was observed in the DOP-free medium (M-NP and NM-NP groups), when M. aeruginosa could only utilize stored P quota for both alleviating photo-induced damage and sustaining its growth.

4.2. Variation and Effects of Algal Utilization of DOP

Studies have demonstrated that environmental factors can greatly affect algal adaptation after UV radiation [59,60]. For example, Li et al. [61] reported that iron-deficient cyanobacterial cells were more susceptible to UV-B radiation and the effects of UV radiation could be underestimated in natural waters. Ren et al. [20] found that higher EPS production by algal cells could absorb UV radiation and promote the aggregated morphology of algae to reduce photo-induced damage. However, they focused less on the variation and effects of algal utilization of DOP after UV radiation, despite the fact that DIP shortage has become a common phenomenon and DOP released from sediments and external DOP inputs are becoming the major sources of P loading [27,62].
In DOP-rich waters (NM-P and M-P groups), our results were consistent with previous studies that found ambient UV-A and UV-B radiation had a great impact on the nutrient utilization behaviors and cell-nutrient contents of algae, which might in turn significantly influence their adaptation processes [17,51]. Medina-Sánchez et al. [63] also reported that the deleterious effects of UV radiation on algae in oligotrophic systems were largely restricted by the nutritional status of cells. In this study, inactivation of APase of M. aeruginosa after UV radiation in the NM-P group could result in algal worse affinity for DOP, slower DOP uptake rate, and lower cellular P quota. This was in accordance with Tank et al. [64] and Sereda et al. [65], which the disrupted P cycling and reduced P acquisition ability of planktons after UV radiation could be partly caused by APA declines. As mentioned above, UV adaptation of M. aeruginosa under sublethal UV radiation could result in an elevated P demand and algae under UV exposure might depend more on the external DIP, partly due to its inability to mobilize stored P [51]. Consequently, the P demand of M. aeruginosa after UV radiation could not be satisfied and the adverse effects were more significant in the NM-P group.
By comparison, DOM availability could change the photochemical reactions of APase and DOM could protect APase of M. aeruginosa from substantial inactivation under ambient UV radiation in the M-P group. In this case, algal demand for P was satisfied with the faster DOP uptake rate, higher cellular P quota and higher DIP production. Consequently, algal SOD activity increased in accordance with higher ROS production under UV exposure, and the superior up-regulation of CAR and PC by M. aeruginosa was conducive to decreasing the UV-induced damage and increasing algal self-repair efficiency. Considering that DOM was a ubiquitous substance in the aquatic environment and M. aeruginosa displayed a better accumulation ability for DOP [36,40], the experimental results in this study might provide a competitive advantage for M. aeruginosa in the natural waters. García-Gómez et al. [66] also reported that the unicellular chlorophyte Dunaliella tertiolecta could quickly activate DNA repair under UV radiation when the repair capacity and tolerance to high UVR doses could provide an advantage over other species in the photic zone and the whole water column.

4.3. Effects of DOM on APase Inactivation

Although many studies have examined the kinetic and fate of APase under varying conditions [27,45], limited information was provided on the effects and regulation of irradiation and DOM. Actually, the roles of DOM in water have been widely explored in recent years, including light attenuation, photochemical reaction, the release of nutrients, etc. [67,68]. However, although UV adsorption by DOM has been reported [29], this might not be the main function of DOM in our study considering the effects of DOM on APase inactivation in the NM-NP and M-NP groups. Meanwhile, as reported by many scholars, UV-absorbing compounds (UVCs) are widespread in various cyanobacterial species and could protect them against harsh environments [69,70]. For example, Hu et al. [71] pointed out that mycosporine-like amino acids (MAAs) producing Microcystis were not to the point that they exclusively predominated over non-MAAs-producers, but they might be ecologically advantageous under high UV conditions. However, since APase of M. aeruginosa was mainly located on the outer surfaces of algal cells or as freely dissolved enzymes in algal cultures [53,72], UV radiation might easily reach APase before UV radiation was adsorbed by HA or UV-absorbing compounds (UVCs) in the Petri dishes [73,74]. Some other scholars also reported that Microcystis uses a combination of photoprotective strategies to cope with high solar UV radiation at the water surface and MAAs conferred only a smaller part of light screening [69]. Scholars reported that APase was stable in the water and it could remain active for several days, and DOM could associate with APase produced by algal cells [75,76]. Our study supported this result, and HA might block the active sites of APase, leading to an APA decrease in the dark. However, DOM alleviated APase inactivation in the PAR treatment, when PAR might break down the binding between DOM and APase [33]. As a result, APA of algal cultures did not decrease after 5 h of PAR in both four groups, and DOP utilization of M. aeruginosa might not be significantly affected.
In comparison, UV radiation could enhance ROS production and result in APase inactivation in UV-A and UV-B treatments [37]. Moreover, the absorbance of UV-band light by APase was high (Figure S3) and the direct oxidation of APase might occur after UV radiation [46]. However, suitable electron donors could convert radical cations of amino acids back to the ground states [77,78], and DOM likely played as an antioxidant to repair the oxidized APase, resulting in the slower APase inactivation and a slighter APA decrease in algal cultures after UV-A and UV-B radiation. The antioxidant potential of HA was also detected in some other laboratory experiments [79,80]. Another less-specific mechanism that underlies APA variation in the M-P group was the complexation of DOM with APase while retaining high activity, thus displaying a stabilization effect of DOM on APase [74]. Consequently, water environmental conditions such as sediment resuspension and exogenous inputs should be considered when some engineering measures are used to control Microcystis blooms since enhancement of P in the water could promote algal growth and DOM might increase the adaptation capability of M. aeruginosa to UV radiation. Furthermore, our study suggested that reductions of DIP and DOP could be both important considering the interactive effects of P availability and algal adaptation to UV radiation. The higher APA decrease in the algal cultures in the M-NP group could be that the composition of extracellular organic matter (EOM) produced by cyanobacteria was complicated [81], which could act as a photosensitizer to generate more ROS in the water.
Considering the wide distribution of M. aeruginosa in eutrophic lakes, our results could partly provide a framework to elucidate the mechanisms that enable cyanobacteria to utilize DOP and adapt to UV radiation in natural ecosystems. Especially, UVCs such as MAAs might influence the results and MAAs should be considered to explain the comprehensive mechanism of algal adaptation to ambient UV radiation. The complexities and unexamined factors deserve further study in the future.

5. Conclusions

(1)
Ambient UV-A and UV-B radiation exerted oxidative stress on M. aeruginosa and exhibited inhibitive effects on the growth and photosynthesis of algae. However, the negative effects of UV radiation could be eliminated with DOM addition in the DOP-rich medium and M. aeruginosa showed a stronger adaptation capability, including decreasing UV-induced damages and promoting self-repair;
(2)
The adaptation of M. aeruginosa to ambient UV radiation in the DOP-rich waters could be mainly achieved through DOP hydrolysis and the metabolism of DIP. In the NM-P group, the great inactivation of algal APase after UV radiation resulted in worse affinity for DOP, slower DOP uptake and lower cellular P quota. Consequently, the P demand of M. aeruginosa after UV radiation could not be satisfied for adaptation processes, such as up-regulation of SOD activity, CAR and PC synthesis recovery of photosynthetic efficiency;
(3)
DOM could act as an antioxidant and greatly decrease APase inactivation under UV radiation, and DOP utilization by M. aeruginosa was promoted, including faster DOP uptake rate, higher cellular P quota and higher DIP production. Thus, algal P demand was satisfied for adaptation to UV radiation in the M-P group when M. aeruginosa alleviated UV-induced damages and quickly recovered its photosynthetic efficiency.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse10091257/s1, Figure S1. The spectral power distribution and weighted UV radiation of UV-A lamps (PL-L 36W/09/4P, Philips) used in the irradiation experiment. Figure S2. The spectral power distribution and weighted UV radiation of UV-B lamps (TL20W/01RS, Philips) used in the irradiation experiment. Figure S3. The energy-based flux of sun spectrum at solar noon (13:00 pm) in summer of Nanjing, Jiangsu (red line) and the absorbance of M. aeruginosa-derived alkaline phosphatase (APase, 0.84 μmol L−1 h−1, green line). Figure S4. Average values of the hourly UV-B dosage in Nanjing, China in spring (April) and summer (July). Dashed horizontal line indicates the hourly irradiation of 0.5 and 1.0 W m−2 UV-B in spring and summer, respectively. Figure S5. Stability of glucose-6-phosphate (initial DOP concentration of 2.5 mg L−1) under different irradiation (70 W m−2 PAR, 30 W m−2 UV-A and 1.0 W m−2 UV-B). Figure S6. Schematic diagram of the irradiation experiments on M. aeruginosa. References [26,44,45,48,50,62,82,83,84] are cited in the supplementary materials.

Author Contributions

Conceptualization, J.H. and L.R.; methodology, H.Z.; data curation, W.J. and M.L.; writing—original draft preparation, L.R.; writing—review and editing, J.H. and T.J.; investigation, H.W., Y.P. and Y.M. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the Natural Science Foundation of Jiangsu Province (BK20210933) and Practical innovation Training Program for College students in Jiangsu Province (202211276073Y).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author, upon reasonable request.

Acknowledgments

We are grateful to the editor and anonymous reviewers for their efforts to improve this manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Effects of different irradiation on the growth of M. aeruginosa in (a) high-DIP medium, (b) moderate-DIP medium, (c) NM-P group, (d) M-P group, (e) NM-NP group and (f) M-NP group.
Figure 1. Effects of different irradiation on the growth of M. aeruginosa in (a) high-DIP medium, (b) moderate-DIP medium, (c) NM-P group, (d) M-P group, (e) NM-NP group and (f) M-NP group.
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Figure 2. Photosynthetic efficiency of M. aeruginosa after 5 h of irradiation and during the 10-day recovery period in (a) NM-P group, (b) M-P group, (c) NM-NP group and (d) M-NP group. (Arrow indicates the initial value of Fv/Fm; * indicates a significant difference between UV-A or UV-B treatment and PAR control at p < 0.05).
Figure 2. Photosynthetic efficiency of M. aeruginosa after 5 h of irradiation and during the 10-day recovery period in (a) NM-P group, (b) M-P group, (c) NM-NP group and (d) M-NP group. (Arrow indicates the initial value of Fv/Fm; * indicates a significant difference between UV-A or UV-B treatment and PAR control at p < 0.05).
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Figure 3. ROS in the cells of M. aeruginosa (vertical bar) and algal SOD activity (scatter) after 5 h of PAR, UV-A or UV-B radiation.
Figure 3. ROS in the cells of M. aeruginosa (vertical bar) and algal SOD activity (scatter) after 5 h of PAR, UV-A or UV-B radiation.
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Figure 4. Contents of (a) chlorophyll a, (b) carotenoid and (c) phycocyanin in single cells after 5 h of different irradiation (Arrows indicate the initial values of photosynthetic pigment).
Figure 4. Contents of (a) chlorophyll a, (b) carotenoid and (c) phycocyanin in single cells after 5 h of different irradiation (Arrows indicate the initial values of photosynthetic pigment).
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Figure 5. SEM images of M. aeruginosa cells on Day 1 in (a) NM-P group, (b) M-P group, (c) NM-NP group and (d) M-NP group after 5 h of different irradiation.
Figure 5. SEM images of M. aeruginosa cells on Day 1 in (a) NM-P group, (b) M-P group, (c) NM-NP group and (d) M-NP group after 5 h of different irradiation.
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Figure 6. Cellular P quota of M. aeruginosa (vertical bar) and contents of P fractions in the medium (line and scatter, solid line referred to DOP and dashed line referred to DIP) in (a) NM-P group, (b) M-P group, (c) NM-NP group and (d) M-NP group after different irradiation treatment.
Figure 6. Cellular P quota of M. aeruginosa (vertical bar) and contents of P fractions in the medium (line and scatter, solid line referred to DOP and dashed line referred to DIP) in (a) NM-P group, (b) M-P group, (c) NM-NP group and (d) M-NP group after different irradiation treatment.
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Figure 7. APA of algal cultures in (a) NM-P group, (b) M-P group, (c) NM-NP group and (d) M-NP group after different irradiation treatment.
Figure 7. APA of algal cultures in (a) NM-P group, (b) M-P group, (c) NM-NP group and (d) M-NP group after different irradiation treatment.
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Figure 8. Effects of irradiation and DOM on the inactivation of M. aeruginosa-derived APase: (a) dark, (b) PAR, (c) UV-A radiation and (d) UV-B radiation.
Figure 8. Effects of irradiation and DOM on the inactivation of M. aeruginosa-derived APase: (a) dark, (b) PAR, (c) UV-A radiation and (d) UV-B radiation.
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Table
Table 1. Kinetic parameters for DOP uptake by M. aeruginosa after 5 h of irradiation (* indicates a significant difference between treatments and the initial value at p < 0.05).
Table 1. Kinetic parameters for DOP uptake by M. aeruginosa after 5 h of irradiation (* indicates a significant difference between treatments and the initial value at p < 0.05).
Experimental GroupsIrradiation TreatmentVmaxKm
(μg P mg−1 DW·h−1)(μg P L−1)
Initial value10.25 (±0.08)480.23 (±5.40)
NM-PPAR10.30 (±0.12)474.48 (±2.66)
UV-A8.22 (±0.20) *626.87 (±5.63) *
UV-B6.75 (±0.46) *775.18 (±13.03) *
M-PPAR10.24 (±0.14)465.82 (±4.20)
UV-A11.42 (±0.25) *470.30 (±5.29)
UV-B12.55 (±0.21) *473.20 (±4.69)
NM-NPPAR10.24 (±0.09)485.52 (±3.24)
UV-A6.11 (±0.14) *688.26 (±8.21) *
UV-B4.22 (±0.22) *835.45 (±10.35) *
M-NPPAR10.30 (±0.18)474.26 (±5.68)
UV-A6.35 (±0.26) *695.24 (±14.21) *
UV-B4.38 (±0.19) *826.3 (±13.35) *
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Ren, L.; Huang, J.; Zhu, H.; Jiang, W.; Wu, H.; Pan, Y.; Mao, Y.; Luo, M.; Jeong, T. Effects of Algal Utilization of Dissolved Organic Phosphorus by Microcystis Aeruginosa on Its Adaptation Capability to Ambient Ultraviolet Radiation. J. Mar. Sci. Eng. 2022, 10, 1257. https://doi.org/10.3390/jmse10091257

AMA Style

Ren L, Huang J, Zhu H, Jiang W, Wu H, Pan Y, Mao Y, Luo M, Jeong T. Effects of Algal Utilization of Dissolved Organic Phosphorus by Microcystis Aeruginosa on Its Adaptation Capability to Ambient Ultraviolet Radiation. Journal of Marine Science and Engineering. 2022; 10(9):1257. https://doi.org/10.3390/jmse10091257

Chicago/Turabian Style

Ren, Lingxiao, Jing Huang, Huagang Zhu, Wei Jiang, Haoyu Wu, Yuyang Pan, Yinghui Mao, Minghan Luo, and Taeseop Jeong. 2022. "Effects of Algal Utilization of Dissolved Organic Phosphorus by Microcystis Aeruginosa on Its Adaptation Capability to Ambient Ultraviolet Radiation" Journal of Marine Science and Engineering 10, no. 9: 1257. https://doi.org/10.3390/jmse10091257

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