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Turn the potential greenhouse gases into biomass in harmful algal blooms waters: A microcosm study
Science of the Total Environment 655 (2019) 520–528
Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Turn the potential greenhouse gases into biomass in harmful algal blooms waters: A microcosm study Hainan Ai, Yixi Qiu, Qiang He, Yixin He, Chun Yang, Li Kang, Huarui Luo, Wei Li, Yufeng Mao, Meijuan Hu, Hong Li ⁎ Key Laboratory of Eco-Environment of Three Gorges Region, Ministry of Education, Chongqing University, Chongqing 400044, China
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Flocculation, capping and macrophytes incubation jointly caused N98% algae removal. • Aerobic microorganism predominant the sediment hence depressed CH4 production. • Algal-derived carbon were captured by plant biomass instead of released as CH4.
a r t i c l e
i n f o
Article history: Received 10 August 2018 Received in revised form 22 October 2018 Accepted 17 November 2018 Available online 19 November 2018 Editor: Daniel Wunderlin Keywords: Harmful algae blooms Algae removal Methane emission Carbon capture Carbon cycle
a b s t r a c t Carbon sources are a critical requirement for the proliferation of algae and the occurrence of harmful algal blooms (HABs), but are often turned into methane (CH4) after the collapse of severe HABs. Here, we attempt to remove HABs, reduce algal-derived CH4 emissions, and repair the broken carbon biogeochemical cycle in aquatic systems using an integrated ecological approach including flocculation, capping, and submerged macrophyte induction, preliminary at a microcosm scale. This strategy sustainably reached 98% algal removal after 65 days of incubation and resulted in an aerobic microenvironment (ORP = +12 mv) at the sediment-water interface. The approach contributed to an approximate 60% decline in CH4 released from the aquatic environment into the atmosphere jointly through assimilation of mineralized organic carbon by submerged macrophytes, production of carbon dioxide (CO2) under aerobic conditions, and aerobic CH4 oxidation. Some of the CO2 produced in the aquatic phase contributed to inorganic carbon and formed the submerged macrophytes biomass. A combination of flocculation, capping, and submerged macrophyte incubation were significant contributors to altering the carbon budget and sealing nearly 99% of the carbon in the simulated ecosystem (the majority in sediment, followed by submerged macrophytes), providing a sustainable way to reuse algal-derived carbon and reduce CH4 emissions. © 2018 Elsevier B.V. All rights reserved.
1. Introduction
⁎ Corresponding author at: NO. 174 Shazheng Street, Shapingba District, Chongqing 400044, China. E-mail address: [email protected] (H. Li).
https://doi.org/10.1016/j.scitotenv.2018.11.262 0048-9697/© 2018 Elsevier B.V. All rights reserved.
Freshwater lakes occupy only a small portion of the earth's surface but contribute up to 16% of the methane (CH4) in the atmosphere (Bastviken et al. 2004). A higher CH4 contribution area may be observed when harmful algal blooms (HABs) attack aquatic ecosystems. HABs
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result from eutrophication and the dominance of certain phytoplankton have raised global concerns. During the recent decades, HABs have frequently occurred worldwide in both fresh and marine ecosystems (Fig. 1a). Eutrophication is the result of nutrient over-enrichment caused by human activities, such as population growth, urbanization, agricultural and industrial expansion, and the synergistic effects of global climate change (Liu and Lal 2014; Mrdjen et al. 2018; Xiao et al. 2017). When the nutrition level, predominately nitrogen and phosphorus (Wang et al. 2017), suits phytoplankton growth, biological fixation and export of carbon to the aquatic phase and absorption by phytoplankton (as CO2 or HCO3−) - the biological carbon pump (Rafter et al. 2017) - could largely enhance the proliferation of certain phytoplankton and even cover the water surface (Toh et al. 2012) (Fig. 1b). During the occurrence of HABs, nutrients and carbon sources are recognized as essential but hazardous contributors (Glibert et al. 2014). However, when dense HABs occur, the following collapse of algal cells usually cause hypoxic or anoxic conditions. Moreover, when HABs settle from the overlying water to the sediment, they may be utilized by bacteria and result in the exhaustion of dissolved oxygen (DO), triggering the production of CH4 hence contributing to global warming (Xing et al. 2013). Numerous efforts have been made to solve the dilemma of HABs. The use of clay for removing HABs has been extensively studied. Clay particles are useful in flocculating algae cells and then migrating algal flocs to sediment (Louzao et al. 2015). To achieve high algae removal efficiency, chemically modified clay is produced by utilizing hydroxide and different amounts of sulfuric acid (Kim et al. 2017). Algicidal microbes can not only efficiently attack and lyse algal cells but also reduce their exudates (Cai et al. 2016). Copper-based algaecide can effectively
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depress the cyanobacteria population in Lake Rockwell (Crafton et al. 2018). A magnetic coagulant synthesized by compounding acidmodified fly ash with magnetite (Fe3O4) was also found capable of substantial removal of algae from the water column (Liu et al. 2013). Indeed the abovementioned approaches are effective in removing HABs, but present challenges since algae decomposition contributes to the exhaustion of DO and the production of greenhouse gases (GHGs), especially after the collapse of severe HABs. During the proliferation of phytoplankton and occurrence of HABs, carbon in the atmosphere, such as CO2, can enter aquatic systems through free diffusion, and then be adsorbed and fixed by phytoplankton. However, after the collapse of algal cells, their metabolites are turned into CO2 or CH4, depending on the DO levels. The key to explain why CO2 contributes to the formation of phytoplankton and HABs but is then released into the air as CH4 lies in the broken carbon cycles in aquatic ecosystems. CO2 is essential for aquatic vegetation, which indicates that CO2 sequestration by submerged macrophytes, if using an proper ecological approaches, is a potential way to repair the carbon cycles (Chen et al. 2012) and depress CH4 production in aquatic systems. To control HABs and algal-derived CH4 emissions simultaneously, here, microcosm studies were conducted to migrate phytoplanktonfixed CO2 into submerged macrophytes. We studied the effects of integrated approaches, including flocculation, capping, and submerge macrophyte induction, on the removal of HABs and release of CH4. We also investigated the responses of carbon cycle-associated water parameters, and analyzed the structure of microorganism communities in response. This report concerns the utilization of an ecological approach to achieve multiple goals, including HABs controlling, GHGs reduction and carbon cycle repairing, for the first time.
Fig. 1. Global occurrence of HABs and the collapse of severe HABs. (a) the occurrence of HABs according to the available articles. (b) Occurrence of dense HABs in Lake Taihu, China, and (c) After the collapse of the severe HABs. The photos were supplied by Hong Li.
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2. Material and methods 2.1. HABs, sediment, soil, activated carbon and flocculants The HABs was collected from Dianchi, a shallow lake which is frequently attacked by the cyanobacterial dominant HABs. The sediment was also collected from Lake Dianchi using a gravity core sampler. Soil was collected from the bank of lake, and was washed with deionized water to exclude the small particles which cannot be easily sedimented to the bottom water, then the soil was dried for 20 h at 90 °C. The activated carbon were purchased from Mingmo Water Treatment Equipment Co. Ltd., Chongqing, China. The flocculant, Poly Aluminium Chloride (PAC), was obtained from Guangfu Fine Chemical (Tianjin, China), and its Al2O3 content was 28.59%. 2.2. Incubation experiment A microcosm scale study was established to investigate the migration of carbon from phytoplankton to submerged plants or the gas phase using a self-designed column, with a height of 58 cm and a diameter of 14 cm. An illustration of the column is shown in Fig. 2. A volume of 3600 mL cyano-HABs water was added into the columns of which the initial algae concentration was 1.22 × 108 cells/L. Fifteen columns containing the same amount sediment and algal water were prepared, and were divided into 5 treatments. 1) Columns containing water, sediment and phytoplankton, which were used as controls. 2) Flocculation of phytoplankton using PAC with a dosage of 5.0 mg/L, then the migrated algal cells were capped using 2.0 cm thick soil. 3) Following the treatment 2, the seeds of the submerged macrophytes Vallisneria natans were added. 4) Following flocculation, activated carbon served as a capping material instead of soil, and 5) the same amount of Vallisneria natans was introduced in the column based on treatment 4. The test was performed at a constant 25 °C in an illumination incubator (GZX250BSH-III) with a light intensity of 40 μmol photons/(m2/s) under 12 h:12 h light and dark cycles.
in the gas bag (HB.3-CQD, China) using a pump (WT-80, China). The CH4 concentration was then measured using a gas chromatograph (PE Clarus 500, PerkinElmer, Inc., USA) equipped with a flame ionization detector, and the CO2 concentration was assessed with an intelligent gas detector (WT-80). The CH4 and CO2 fluxes were calculated by Eq. (1) (Chen et al. 2008) f ¼
V ΔC A ΔT
ð1Þ
where f = CH4 or CO2 emission flux (mg∙m−2∙h−1), V = volume of chamber above the soil (m3), A = cross-section of chamber (m2), ΔC = concentration difference between time zero and time t (mg∙m3), and Δt = time duration between two sampling periods (h). After 65-day incubation, the sediment, water, submerged plants and capping materials were gently separated from the column and stored at −20 °C until analysis. Then, the carbon contents of the sediment in each treatment were measured with an elemental analyzer (CHS-580A, Germany). The carbon content in the raw water was measured with a total organic carbon analyzer (vario TOC, Germany). The carbon budget was calculated linking the carbon content to the weight, volume and biomass in different parts of the system. 2.4. Analysis of microorganism community The sediment was stored at −20 °C followed by high-throughput sequencing analysis with detailed information supplied in SI. 2.5. Statistical analysis Analysis of variance (ANOVA) was employed to study the difference between treatments, with a significant difference recognized when p b 0.05. 3. Results
2.3. Sample preparation
3.1. Algae migration
The gas emissions (CH4 and CO2) at the water-air surface were collected every 5 days using a static chamber, the pH in the water column and the ORP value at the sediment-water interface were measured at 5day intervals. During the gas collection, the static chamber was deployed above the water surface for 3 h, and then, the gas was collected
In comparison to that of the controls, when the algal cells were subjected to flocculation, the algal density showed an approximate 98% reduction before day 15, irrespective of capping and submerged macrophyte incubation (Fig. 3). However, in the flocculationcapping system, the algal cells seemed to have escaped from the
Fig. 2. An illustration of the experimental system.
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Fig. 3. Dynamics of algal cell density during the incubation experiment (a). Data represent the mean values of triplicates. b, d, f, h, j illustrated the view of algal removal effects looking down from the column in control, flocculation-soil capping, flocculation-soil capping-submerged macrophytes incubation, flocculation-AC capping, and flocculation-AC capping-submerged macrophytes incubation treatment, respectively. c, e, j, i, k showed the effects from their horizontal view. The yellow and white dashed revealed the occurrence of Daphnia magna and Bellamya aeruginosa in submerged macrophytes incubated systems, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
flocs in the following days and maximally exhibited a nearly 17-fold increase, and an insignificant difference (P = 0.172, N0.05) was shown between soil and activated carbon capping. In contrast, the incubation of submerged macrophytes contributed to a dramatic depression of algae resuspension. Hence, the algal density dynamics revealed slight changes during the 65 days incubation, and N97% algae removal was maintained. In the controls treatment, the algal density showed a dramatic increase after 25 days of incubation, and the algal density far exceeded that in the capping and submerged macrophyte-added groups during the experimental periods.
3.2. Gas flux at the water-air interface The CH4 and CO2 fluxes showed a discernable pattern between treatments (Fig. 4). In the controls, the algal cells covered the water surface, which not only impaired the oxygen exchange between the water column and atmosphere but also enhanced algae decomposition. As a result, anaerobic digestion of algal-derived carbon led to a dramatic increase in CH4, which ranged between 33.5 and 159.5 μg/(m2·d) during the 65-day incubation. Flocculation-capping treatments accelerated algal decomposition and enhanced CH4 production, which maximally reached 252.5 and 224.8 μg/(m2·d) in the soil- and AC-capped systems,
Fig. 4. CH4 and CO2 flux at the water-atmosphere interface between treatments over the span of 65 days incubation.
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respectively. With the extension of the study period, the production of CH4 was impaired in capping or submerged macrophyte incubated treatments, which contrasted with the CH4 profile in the control (Supporting Information, SI, Fig. S1). The minimum CH4 flux was observed in the flocculation-capping-submerged macrophyte system, which substantially reversed the CH4 profile, and the average CH4 flux accounted for approximately 40% of that in the controls. A different pattern of CO2 flux was shown in comparison to that of CH4. Flocculationcapping migrated the majority of algal cells into sediment, while algae resuspension elevated oxygen levels in the water column, contributing to the aerobic digestion of algal-derived carbon and maximum CO2 production among the treatments (Fig. 4). The maximum CO2 flux was supposed to occur in the flocculation-capping-submerged macrophyte system since its ORP value was significantly higher than that of the other treatments. However, in the submerged macrophyte system, the average CO2 flux accounted for 38.3–71.2% of that in the flocculationcapping system, implying the submerged macrophytes may be responsible for the reduction of both CH4 and CO2 production. It should be noted that the CO2 production in the control was significantly lower (P = 0.041, b0.05) than that in the other groups, suggesting the algal biomass regulated the carbon fate. In contrast to the production of CH4, the peak of CO2 flux appeared during the later stage of the study period, particularly in the submerged macrophyte- incubated system. (Fig. S2). 3.3. Shift of microorganism community in the sediment The populations at the phyla level were identified between treatments and are presented in Fig. 5a. It was shown that Firmicutes (52.23%), Proteobacteria (24.29%), Chloroflexi (6.94%), Acidobacteria (3.71%) and Cyanobacteria (2.25%) were the dominant phyla in controls. The relative abundances of Firmicutes, Chloroflexi, and Cyanobacteria tended to decrease in the flocculation-AC capping as well as in the submerged macrophyte-incubated systems after 65 days of incubation. In contrast, the total percentage of predominant phyla, including Proteobacteria, Bacteroidetes and Acidobacteria, increased from 5.55% to 63.46%. Further analysis of the microbial community profiles was conducted at the genus level (Fig. 5b). Among 308 different detected genera bacteria, the abundance of Arenimonas, Actibacter, Thermomonas and Acidobacteria was highly enriched in the presence of submerged macrophytes. To be specific, the abundance of Arenimonas was approximate 26 times higher in submerged macrophyte incubated treatments than controls, and Actibacter, Thermomonas and Acidobacteria were about 24, 6 and 3 folds higher than control, respectively. On the other hand, the abundance of Clostridium, Romboutsia and Sporacetigenium was remarkably reduced with addition of submerged macrophyte, which constituted 2.8–8.2%, 20.5–22.8%, and 22.0–50.2% of that in control. In addition, the relative abundance of the genera Thermoanaerobaculum, Roseomonas, Limnobacter and Novosphingobium was also largely stimulated compared to that of the control. The present results indicated that flocculation-capping followed by submerged macrophyte incubation were critical contributors to the shift in the community structure of microorganisms. 3.4. Carbon budget The carbon budget in the treatments was assessed, including carbon content in sediment, aquatic phase, phytoplankton, submerged macrophytes biomass as well as the GHGs (CO2 and CH4). Before treatment, the predominant media of carbon stock in the study was sediment (44.78 g), followed by the aquatic phase (0.21 g) and phytoplankton (0.03 g) (Fig. 6). In controls, after 65 days incubation, a nearly 40-fold increase of carbon content appeared in the algal cells, 0.75 g of carbon turned into gaseous carbon (including CO2 and CH4), and a 9.4% reduction in the carbon content in the sediment was observed. However, flocculation, subsequent capping as well as the associated submerged
macrophyte incubation impacted the carbon fraction greatly, which slightly reduced aqueous carbon, while its fraction in the sediment increased by 1.27–2.89%. Capping materials were linked with gaseous carbon content: the utilization of soil as a capping material increased the gaseous carbon by 10.67% compared to that of the control, whereas the employment of AC hardly impacted the gaseous carbon fraction. After 65 days incubation, the biomass carbon (indicated by the carbon content in submerged macrophytes) accounted for 0.56% and 0.91% of the total carbon in the systems with soil and AC as capping materials, respectively. In Fig. 6, it can be clearly seen that the incubation of submerged macrophytes resulted in a reduction in algal-originated gaseous, which were transferred to vegetable biomass. 4. Discussion 4.1. Flocculation-capping-plant induction systems are effective for HABs removal Developing cost-effective and environmentally benign ways to remove HABs from aquatic systems is essential for restoring the deteriorated water quality. Special attention had been paid to the use of flocculation-based approaches, which are useful to settle algae cells to sediment. Traditional inorganic flocculants, such as ferric salts or aluminum salts (Sun et al. 2012; Takaara et al. 2007), are effective in removing algae, but these flocculants have some disadvantages and lead to various ecological concerns, such as the potential risk to the ecosystem imposed by residual Al. Additionally, the decay of dense algal cells may contribute to the release of nutrients and an expansive area of dark, discolored water called “black bloom”, which causes greater threat to water quality (Zhang et al. 2016). Previously, we proposed a biological strategy for simultaneous HABs removal and cyanotoxin degradation (Li et al. 2016). While these efforts provided promising insights for quick and efficient HABs control, their long-term effects on HABs control were not satisfactory because the flocs were frequently subjected to bioor wind-induced disturbances, which facilitated algae resuspension. In the present study, algae density didn't reduced significantly during the incubation in control, in contrast, proliferation of algal cells contributed to nearly 1.8-flod increase of the algae density (Fig. 3). Flocculationcapping treatment capable of N98% algal removal relative to that of the control, but the resuspension of algal cells led to the impairment of removal efficiency. This concern can be solved when the submerged macrophytes were incubated following capping. As illustrated in Fig. 3, N98% algae removal efficiency was achieved throughout the 65 days experiment, and this effect depended less on the capping material, indicating that the submerged macrophytes were the dominant contributor to long-term HABs control. 4.2. Bio-pump-based carbon capture and GHGs reduction The link between the nutrient supply and the appearance of HABs has been proposed frequently. It is accepted that the availability of dissolved inorganic nitrogen and phosphorus is most likely to influence phytoplankton growth. However, instead of being exclusively dependent on nitrogen and phosphorus concentration, the proliferation of algae can highly rely on atmospheric CO2 levels (Bussi et al. 2016). Atmospheric or dissolved CO2 (or HCO3−) can be fixed by cyanobacterial cells, which is helpful in alleviating the “greenhouse effect”. However, the collapse of severe HABs is generally associated with the return of atmospheric carbon, in a more worse way (CH4, which exhibited 45 times stronger GHGs effects than CO2 (Kosten et al. 2016)). The cyanobacterial biomass generated from the fixed CO2 can be utilized for other purposes (Chen et al. 2012), while in HABs water, the reuse of algal-derived carbon lies in the conversion of CH4 to CO2, which requires a substantial improvement in the microenvironment at the sediment-water interface. The flocculation-capping-submerged macrophyte induction treatments caused abrupt increase of ORP value
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Fig. 5. Microbial community analyses of distribution of phyla (a) and heat-map of the classified genera (b) in treatments.
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Fig. 6. The carbon budget in 5 treatments over the span of 65 days incubation. The original column indicates the carbon budget before treatment.
(from approximately −200 mv to 12 mv), indicating that the production of CO2 is favored. In controls, the 2.20 g reduction of the carbon content in the sediment contributed to nearly 40-fold increase of carbon content as phytoplankton biomass and 0.75 g GHGs (Fig. 6). This can be regulated using the proposed ecologically sound and sustainable method. After 65 days incubation, the carbon content in phytoplankton had nearly vanished in both the flocculation-capping and submerged macrophyte incubated treatment, suggesting the initially added phytoplankton were totally decomposed and the algal-derived carbon were converted. In comparison to controls, flocculation-capping treatments still contributed 0.74–0.83 g GHGs emission, while the sequestration of CO2 can be magnified through the incubation of submerged macrophytes, which were responsible for a 0.43–0.45 g decline in the CH4 released from the aquatic system to the atmosphere (Fig. 6). The possible explanation for this result may be that: 1) submerged macrophyte adsorb mineralized algal-derived carbon and contribute to the increase in the submerged macrophyte biomass; 2) the submerged macrophytes remarkably improved the oxygen level at sediment-water interface, as a result, the algal-derived carbon is mineralized to CO2, which can be supported by the pH values (Fig. S4); and 3) with the increase of ORP values at sediment-water interface (Fig. S3), the aerobic methane oxidation processes act as methane filter in aquatic systems (Donis et al. 2017; Michaud et al. 2017; Milucka et al. 2015), which is also related to the photosynthesis of the submerged macrophytes. Therefore, as the carbon budget analysis revealed, 1.28–1.45 g carbon was transferred to the submerged macrophytes and fixed in the ecosystem as biomass. Our results confirmed that through integrated approaches of flocculation-cappingsubmerged macrophyte induction, distribution of algal-derived carbon can be positively manipulated. During this process, the release of CO2 and CH4 can be substantially impaired while the submerged macrophyte biomass was stimulated. This is helpful for restoring a healthier ecological system dominated by submerged vegetation, which can be turned into edible proteins through reconstruction of the food web (Pan et al. 2012). 4.3. Shift in the microorganism structure is responsible for carbon reuse It has been suggested that organic matter could be released into sediment and mineralized into CO2 or CH4 during the decomposition of HABs (Mann et al. 2013), and capping the dense flocs can substantially accelerate the process. The most dominant genus, Clostridium (cellulolytic
anaerobic bacteria (Peng et al. 2014)), was highly enriched in the controls (Fig. 5a), which was helpful for the decay of algal cells. Carbon stored in the sediment showed a 0.54–1.23 g increase in flocculation and subsequent capping groups after 65 days incubation (Fig. 6), indicating the treatment sealed algal-derived carbon in the sediment and provided extra substrate for the mineralization of organic matter. In the controls, the ORP value constantly decreased throughout the study and reached −205 mv on day 65 (Fig. S3). In contrast, flocculation and subsequent capping as well as the submerged macrophyte addition substantially increased the ORP values. The ORP value in the flocculation-capping system generally remained at approximately −120 mv, but were turned to be positive with the incubation of submerged macrophytes (day 45) and further increased to nearly +15 mv by the end of the study, irrespective of capping with soil or AC. Despite substrates were essential for the production of CO2 or CH4, the ORP value at the sediment-water interface regulated the fate of carbon mineralization. Flocculation-capping largely accelerated the decomposition of the algal cells and caused a constant decline in the ORP values at the sediment-water interface (Fig. S3); this anaerobic microenvironment facilitated CH4 production (Fig. 4) by many species of methanogenic bacteria. Methane fermentation during anaerobic digestion comprises the following four steps: hydrolysis, acidogenesis, acetogenesis and methanation (Chandra et al. 2012). In this study, the maximum relative abundance of the genus sporacetigenium (Fig. 5b), which played an imperative role in producing acetate and butyrate (the intermediate product during CH4 formation) during the fermentation process (Zhao et al. 2012), was enhanced when flocculation-capping was conducted, but was reduced by 82.82 and 92.46% in the 2 groups that incubated with submerged macrophytes, respectively. In addition, the genus Romboutsia (responsible for hydrogen (Kuribayashi et al. 2017) and acetic acid (Gerritsen et al. 2014) production) was largely depressed in the submerged macrophyte- incubated system (Fig. 5b). This result suggested that the incubation of submerged macrophytes impaired the production of CH4 through modification of the microenvironment at the sediment-water interface, as well as the interdiction of the acetogenesis process during methane fermentation. The incubation of submerged macrophytes caused aerobic conditions at the sediment-water surface (Fig. S3). Given this circumstance, the relative abundance of the Arenimonas, a genus active in aerobic metabolism (Yuan et al. 2014), showed 26 to 28-fold increase relative to that of the controls (Fig. 5b). Therefore, the majority of the organic matter was supposed to be mineralized to CO2. However, CH4 was the dominant product during the mineralization of the organic matter in the submerged macrophytes incubated treatments, and the released CH4 content accounts for 87.10% and 90.64% of the sum of CH4 and CO2 for soil capping- submerged macrophytes and AC capping - submerged macrophytes treatments, respectively. The values are higher than those in previous literature (Kelley et al. 1990) but are consistent with a recent study that revealed the amount of algal-derived CH4 reached 92% of the sum of CH4 and CO2 (Yan et al. 2017). The probable reason is that the CO2 produced by the mineralization of organic matter was constricted in the water column, which caused an increase in the total inorganic carbon in the water and the reduction of the pH; this agreed well with the dynamic of pH (maintained at nearly 7.50 in the submerged macrophyte- added system, while reaching 7.81 in the flocculation-capping treatment) during this study (Fig. S4). In contrast, capping the dense HABs in sediment and subsequent algae decomposition depleted the oxygen, hence, the ORP value was maintained at approximately −120 mv and −150 mv. This microenvironment favored the proliferation of methanogen, as illustrated by the CH4 flux. Overall, in addition to alternation of the aquatic microenvironment (pH, ORP), the response of microbial compositions contributed to the carbon budget variation in the studied systems. Given the above data, the fate of phytoplankton-derived carbon in the studied systems is presented in Fig. 7. Carbon source enters the aquatic environment as carbon dioxide, which is assimilated by algae cells. However, the over growth of the algae and occurrence of HABs,
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Fig. 7. Conceptual schematic of the effects of flocculation-capping-submerged macrophytes incubation systems on regulation the fate of algal-derived carbon. The yellow arrows here indicate the increase or decrease of parameters. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
along with its subsequent collapse exhausted DO and caused anoxic or anaerobic environment. As a result, the majority of the algal-derived carbon would be turned to CH4, which can contribute to the global warming and in turn benefit HABs occurrence (route ① in Fig. 7). When flocculation and capping is jointly employed, although HABs are removed from water system, the decomposition of the sealed algal cells in the sediment could deteriorate the DO condition and accelerate the process of anaerobic digestion, which favored the production of CH4 (route ② in Fig. 7). The above vicious loop can be entirely turned back if submerged macrophyte incubation is followed. Despite algal decomposition depletes DO in the sediment, the photosynthesis of submerged macrophyte can compensate its depletion to some extent, hence the ORP value can be prompted substantially. With respected to the fate of algal-derived carbon, although algae decomposition cannot be prevented, the released carbohydrate can be the assimilated by the submerged macrophyte to produce biomass, or tend to be transferred to CO2 under the aerobic condition, contributing to the increase of inorganic carbon and reduction of pH (route ③ in Fig. 7), therefore a benign and sustainable circle can be achieved. 4.4. Environmental impact HABs are increasing worldwide and represent a serious threat to freshwater ecosystems (Fig. 1). Nitrogen, phosphorus and dissolved CO2 (CO2(aq)) have been traditionally implicated as having a crucial role in the development of HABs (Paerl et al. 2011; Visser et al. 2016). Some of the contributors to HABs, i.e., phosphorus, are nonrenewable resources and, ironically, are also considered hazardous materials for the occurrence of HABs. Free CO2 can be converted into highly available inorganic carbon, including HCO3– and CO32– (Yan et al. 2017), and as a result, leads to a rise in carbon availability in an aquatic environment, which is converted to algal biomass through assimilation. However, when the collapse of severe HABs occurs, the decay of the algal cells results in the release of algal-derived sources into the water column, causing an expansive area of dark, discolored water with extremely low DO
and prompting the production of CH4 (Zhang et al. 2016). During this carbon biogeochemical process, the atmospheric and aqueous CO2 represent a source of potential precursors for CH4 production, suggesting a break in the carbon cycle from land to lake. Therefore, repairing this broken cycle of carbon is not only essential for the reduction of GHGs emissions from aquatic systems but is also imperative for the reuse of algalderived organic matter. Carbon capture and storage are broadly recognized as having the potential to play a key role in meeting climate change targets (Bui et al. 2018), while carbon capture in HABsattacked water is rarely recommended. In this study, we attempted to repair broken aquatic ecosystems and a vicious carbon loop by utilizing solar energy to make the aquatic system sustainable. We proposed a multidisciplinary approach including flocculation, capping and submerged macrophyte incubation for HABs removal and CH4 emission regulation, and we confirmed that the methodology is capable of: 1) efficient removal of HABs from the water column, 2) remarkable impairment of GHGs (CO2 and CH4) emissions, and 3) conversion of algalderived carbon into plant biomass, which has the benefit that the biomass generated from the fixed CO2 can be further turned into marketable proteins through a reconstructed food web, forming a bigger sustainable circle. The results here provide an ecological principle for manipulating the carbon distribution between algae, water, gas and sediment, contributing to the recycling of carbon resources and alleviating of GHGs emissions, and bring prospects for turning HABs from nightmare situations into an opportunity from the perspective of carbon recycling. 5. Conclusion The combination of flocculation, capping and submerged macrophyte incubation method is promising for HABs removal. Flocculation and capping can seal the algae in the sediment and accelerated the decomposition of algal cells. The subsequent incubation of submerged macrophyte served as a bio-bump which not only deliver oxygen to the sediment-water interface, but also turned algal-derived carbon
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source into plant biomass, hence prevented considerable CH4 production and emission. This environmental benign biochemical process was achieved through the modification of the microenvironment at the sediment-water interface, depression of methanogenic bacteria, and aerobic CH4 oxidation. Acknowledgements This work was jointly supported by the Natural Science Foundation of China (NSFC 51478061, 51609024, 41877472, and 51779020), China Postdoctoral Science Foundation (2016M592641), and Chongqing Research Program of Basic Research and Frontier Technology (cstc2016jcyjA0498). Conflict of interest The authors declare no competing financial interest. Appendix A. Supplementary data Detailed information on analysis of microorganism community, dynamic of CH4 and CO2 flux, ORP, and changes of aquatic pH are supplied. Supplementary data associated with this article can be found in the online version, at doi: https://doi.org/10.1016/j.scitotenv.2018.11.262. References Bastviken, D., Cole, J., Pace, M., Tranvik, L., 2004. Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Glob. Biogeochem. Cycles 18, 1–12. Bui, M., Adjiman, C.S., Bardow, A., Anthony, E.J., Boston, A., Brown, S., Fennell, P.S., Fuss, S., Galindo, A., Hackett, L.A., Hallett, J.P., Herzog, H.J., Jackson, G., Kemper, J., Krevor, S., Maitland, G.C., Matuszewski, M., Metcalfe, I.S., Petit, C., Puxty, G., Reimer, J., Reiner, D.M., Rubin, E.S., Scott, S.A., Shah, N., Smit, B., Trusler, J.P.M., Webley, P., Wilcox, J., Mac Dowell, N., 2018. Carbon capture and storage (CCS): the way forward. Energy Environ. Sci. 11 (5), 1062–1176. Bussi, G., Whitehead, P.G., Bowes, M.J., Read, D.S., Prudhomme, C., Dadson, S.J., 2016. Impacts of climate change, land-use change and phosphorus reduction on phytoplankton in the River Thames (UK). Sci. Total Environ. 572, 1507–1519. Cai, G., Yang, X., Lai, Q., Yu, X., Zhang, H., Li, Y., Chen, Z., Lei, X., Zheng, W., Xu, H., Zheng, T., 2016. Lysing bloom-causing alga Phaeocystis globosa with microbial algicide: an efficient process that decreases the toxicity of algal exudates. Sci. Rep. 6, 20081. Chandra, R., Takeuchi, H., Hasegawa, T., 2012. Methane production from lignocellulosic agricultural crop wastes: a review in context to second generation of biofuel production. Renew. Sust. Energ. Rev. 16 (3), 1462–1476. Chen, I.C., Hegde, U., Chang, C.H., Yang, S.S., 2008. Methane and carbon dioxide emissions from closed landfill in Taiwan. Chemosphere 70 (8), 1484–1491. Chen, P.H., Liu, H.L., Chen, Y.J., Cheng, Y.H., Lin, W.L., Yeh, C.H., Chang, C.H., 2012. Enhancing CO2 bio-mitigation by genetic engineering of cyanobacteria. Energy Environ. Sci. 5, 8318–8327. Crafton, E.A., Glowczewski, J., Ott, D.W., Cutright, T.J., 2018. In situ field trial to evaluate the efficacy of Cutrine Ultra to manage a cyanobacteria population in a drinking water source. Environ. Sci.: Water Res. Technol. 4 (6), 863–871. Donis, D., Flury, S., Stöckli, A., Spangenberg, J.E., Vachon, D., McGinnis, D.F., 2017. Full-scale evaluation of methane production under oxic conditions in a mesotrophic lake. Nat. Commun. 8 (1), 1661. Gerritsen, J., Fuentes, S., Grievink, W., van Niftrik, L., Tindall, B.J., Timmerman, H.M., Rijkers, G.T., Smidt, H., 2014. Characterization of Romboutsia ilealis gen. nov., sp. nov., isolated from the gastro-intestinal tract of a rat, and proposal for the reclassification of five closely related members of the genus Clostridium into the genera Romboutsia gen. nov., Intestinibacter gen. nov., Terrisporobacter gen. nov. and Asaccharospora gen. nov. Int. J. Syst. Evol. Microbiol. 64 (5), 1600–1616. Glibert, P.M., Icarus Allen, J., Artioli, Y., Beusen, A., Bouwman, L., Harle, J., Holmes, R., Holt, J., 2014. Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: projections based on model analysis. Glob. Chang. Biol. 20 (12), 3845–3858. Kelley, C.A., Martens, C.S., Chanton, J.P., 1990. Variations in sedimentary carbon remineralization rates in the White Oak River Estuary, North Carolina. Limnol. Oceanogr. 35 (2), 372–383.
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Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Turn the potential greenhouse gases into biomass in harmful algal blooms waters: A microcosm study Hainan Ai, Yixi Qiu, Qiang He, Yixin He, Chun Yang, Li Kang, Huarui Luo, Wei Li, Yufeng Mao, Meijuan Hu, Hong Li ⁎ Key Laboratory of Eco-Environment of Three Gorges Region, Ministry of Education, Chongqing University, Chongqing 400044, China
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• Flocculation, capping and macrophytes incubation jointly caused N98% algae removal. • Aerobic microorganism predominant the sediment hence depressed CH4 production. • Algal-derived carbon were captured by plant biomass instead of released as CH4.
a r t i c l e
i n f o
Article history: Received 10 August 2018 Received in revised form 22 October 2018 Accepted 17 November 2018 Available online 19 November 2018 Editor: Daniel Wunderlin Keywords: Harmful algae blooms Algae removal Methane emission Carbon capture Carbon cycle
a b s t r a c t Carbon sources are a critical requirement for the proliferation of algae and the occurrence of harmful algal blooms (HABs), but are often turned into methane (CH4) after the collapse of severe HABs. Here, we attempt to remove HABs, reduce algal-derived CH4 emissions, and repair the broken carbon biogeochemical cycle in aquatic systems using an integrated ecological approach including flocculation, capping, and submerged macrophyte induction, preliminary at a microcosm scale. This strategy sustainably reached 98% algal removal after 65 days of incubation and resulted in an aerobic microenvironment (ORP = +12 mv) at the sediment-water interface. The approach contributed to an approximate 60% decline in CH4 released from the aquatic environment into the atmosphere jointly through assimilation of mineralized organic carbon by submerged macrophytes, production of carbon dioxide (CO2) under aerobic conditions, and aerobic CH4 oxidation. Some of the CO2 produced in the aquatic phase contributed to inorganic carbon and formed the submerged macrophytes biomass. A combination of flocculation, capping, and submerged macrophyte incubation were significant contributors to altering the carbon budget and sealing nearly 99% of the carbon in the simulated ecosystem (the majority in sediment, followed by submerged macrophytes), providing a sustainable way to reuse algal-derived carbon and reduce CH4 emissions. © 2018 Elsevier B.V. All rights reserved.
1. Introduction
⁎ Corresponding author at: NO. 174 Shazheng Street, Shapingba District, Chongqing 400044, China. E-mail address: [email protected] (H. Li).
https://doi.org/10.1016/j.scitotenv.2018.11.262 0048-9697/© 2018 Elsevier B.V. All rights reserved.
Freshwater lakes occupy only a small portion of the earth's surface but contribute up to 16% of the methane (CH4) in the atmosphere (Bastviken et al. 2004). A higher CH4 contribution area may be observed when harmful algal blooms (HABs) attack aquatic ecosystems. HABs
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result from eutrophication and the dominance of certain phytoplankton have raised global concerns. During the recent decades, HABs have frequently occurred worldwide in both fresh and marine ecosystems (Fig. 1a). Eutrophication is the result of nutrient over-enrichment caused by human activities, such as population growth, urbanization, agricultural and industrial expansion, and the synergistic effects of global climate change (Liu and Lal 2014; Mrdjen et al. 2018; Xiao et al. 2017). When the nutrition level, predominately nitrogen and phosphorus (Wang et al. 2017), suits phytoplankton growth, biological fixation and export of carbon to the aquatic phase and absorption by phytoplankton (as CO2 or HCO3−) - the biological carbon pump (Rafter et al. 2017) - could largely enhance the proliferation of certain phytoplankton and even cover the water surface (Toh et al. 2012) (Fig. 1b). During the occurrence of HABs, nutrients and carbon sources are recognized as essential but hazardous contributors (Glibert et al. 2014). However, when dense HABs occur, the following collapse of algal cells usually cause hypoxic or anoxic conditions. Moreover, when HABs settle from the overlying water to the sediment, they may be utilized by bacteria and result in the exhaustion of dissolved oxygen (DO), triggering the production of CH4 hence contributing to global warming (Xing et al. 2013). Numerous efforts have been made to solve the dilemma of HABs. The use of clay for removing HABs has been extensively studied. Clay particles are useful in flocculating algae cells and then migrating algal flocs to sediment (Louzao et al. 2015). To achieve high algae removal efficiency, chemically modified clay is produced by utilizing hydroxide and different amounts of sulfuric acid (Kim et al. 2017). Algicidal microbes can not only efficiently attack and lyse algal cells but also reduce their exudates (Cai et al. 2016). Copper-based algaecide can effectively
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depress the cyanobacteria population in Lake Rockwell (Crafton et al. 2018). A magnetic coagulant synthesized by compounding acidmodified fly ash with magnetite (Fe3O4) was also found capable of substantial removal of algae from the water column (Liu et al. 2013). Indeed the abovementioned approaches are effective in removing HABs, but present challenges since algae decomposition contributes to the exhaustion of DO and the production of greenhouse gases (GHGs), especially after the collapse of severe HABs. During the proliferation of phytoplankton and occurrence of HABs, carbon in the atmosphere, such as CO2, can enter aquatic systems through free diffusion, and then be adsorbed and fixed by phytoplankton. However, after the collapse of algal cells, their metabolites are turned into CO2 or CH4, depending on the DO levels. The key to explain why CO2 contributes to the formation of phytoplankton and HABs but is then released into the air as CH4 lies in the broken carbon cycles in aquatic ecosystems. CO2 is essential for aquatic vegetation, which indicates that CO2 sequestration by submerged macrophytes, if using an proper ecological approaches, is a potential way to repair the carbon cycles (Chen et al. 2012) and depress CH4 production in aquatic systems. To control HABs and algal-derived CH4 emissions simultaneously, here, microcosm studies were conducted to migrate phytoplanktonfixed CO2 into submerged macrophytes. We studied the effects of integrated approaches, including flocculation, capping, and submerge macrophyte induction, on the removal of HABs and release of CH4. We also investigated the responses of carbon cycle-associated water parameters, and analyzed the structure of microorganism communities in response. This report concerns the utilization of an ecological approach to achieve multiple goals, including HABs controlling, GHGs reduction and carbon cycle repairing, for the first time.
Fig. 1. Global occurrence of HABs and the collapse of severe HABs. (a) the occurrence of HABs according to the available articles. (b) Occurrence of dense HABs in Lake Taihu, China, and (c) After the collapse of the severe HABs. The photos were supplied by Hong Li.
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2. Material and methods 2.1. HABs, sediment, soil, activated carbon and flocculants The HABs was collected from Dianchi, a shallow lake which is frequently attacked by the cyanobacterial dominant HABs. The sediment was also collected from Lake Dianchi using a gravity core sampler. Soil was collected from the bank of lake, and was washed with deionized water to exclude the small particles which cannot be easily sedimented to the bottom water, then the soil was dried for 20 h at 90 °C. The activated carbon were purchased from Mingmo Water Treatment Equipment Co. Ltd., Chongqing, China. The flocculant, Poly Aluminium Chloride (PAC), was obtained from Guangfu Fine Chemical (Tianjin, China), and its Al2O3 content was 28.59%. 2.2. Incubation experiment A microcosm scale study was established to investigate the migration of carbon from phytoplankton to submerged plants or the gas phase using a self-designed column, with a height of 58 cm and a diameter of 14 cm. An illustration of the column is shown in Fig. 2. A volume of 3600 mL cyano-HABs water was added into the columns of which the initial algae concentration was 1.22 × 108 cells/L. Fifteen columns containing the same amount sediment and algal water were prepared, and were divided into 5 treatments. 1) Columns containing water, sediment and phytoplankton, which were used as controls. 2) Flocculation of phytoplankton using PAC with a dosage of 5.0 mg/L, then the migrated algal cells were capped using 2.0 cm thick soil. 3) Following the treatment 2, the seeds of the submerged macrophytes Vallisneria natans were added. 4) Following flocculation, activated carbon served as a capping material instead of soil, and 5) the same amount of Vallisneria natans was introduced in the column based on treatment 4. The test was performed at a constant 25 °C in an illumination incubator (GZX250BSH-III) with a light intensity of 40 μmol photons/(m2/s) under 12 h:12 h light and dark cycles.
in the gas bag (HB.3-CQD, China) using a pump (WT-80, China). The CH4 concentration was then measured using a gas chromatograph (PE Clarus 500, PerkinElmer, Inc., USA) equipped with a flame ionization detector, and the CO2 concentration was assessed with an intelligent gas detector (WT-80). The CH4 and CO2 fluxes were calculated by Eq. (1) (Chen et al. 2008) f ¼
V ΔC A ΔT
ð1Þ
where f = CH4 or CO2 emission flux (mg∙m−2∙h−1), V = volume of chamber above the soil (m3), A = cross-section of chamber (m2), ΔC = concentration difference between time zero and time t (mg∙m3), and Δt = time duration between two sampling periods (h). After 65-day incubation, the sediment, water, submerged plants and capping materials were gently separated from the column and stored at −20 °C until analysis. Then, the carbon contents of the sediment in each treatment were measured with an elemental analyzer (CHS-580A, Germany). The carbon content in the raw water was measured with a total organic carbon analyzer (vario TOC, Germany). The carbon budget was calculated linking the carbon content to the weight, volume and biomass in different parts of the system. 2.4. Analysis of microorganism community The sediment was stored at −20 °C followed by high-throughput sequencing analysis with detailed information supplied in SI. 2.5. Statistical analysis Analysis of variance (ANOVA) was employed to study the difference between treatments, with a significant difference recognized when p b 0.05. 3. Results
2.3. Sample preparation
3.1. Algae migration
The gas emissions (CH4 and CO2) at the water-air surface were collected every 5 days using a static chamber, the pH in the water column and the ORP value at the sediment-water interface were measured at 5day intervals. During the gas collection, the static chamber was deployed above the water surface for 3 h, and then, the gas was collected
In comparison to that of the controls, when the algal cells were subjected to flocculation, the algal density showed an approximate 98% reduction before day 15, irrespective of capping and submerged macrophyte incubation (Fig. 3). However, in the flocculationcapping system, the algal cells seemed to have escaped from the
Fig. 2. An illustration of the experimental system.
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Fig. 3. Dynamics of algal cell density during the incubation experiment (a). Data represent the mean values of triplicates. b, d, f, h, j illustrated the view of algal removal effects looking down from the column in control, flocculation-soil capping, flocculation-soil capping-submerged macrophytes incubation, flocculation-AC capping, and flocculation-AC capping-submerged macrophytes incubation treatment, respectively. c, e, j, i, k showed the effects from their horizontal view. The yellow and white dashed revealed the occurrence of Daphnia magna and Bellamya aeruginosa in submerged macrophytes incubated systems, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
flocs in the following days and maximally exhibited a nearly 17-fold increase, and an insignificant difference (P = 0.172, N0.05) was shown between soil and activated carbon capping. In contrast, the incubation of submerged macrophytes contributed to a dramatic depression of algae resuspension. Hence, the algal density dynamics revealed slight changes during the 65 days incubation, and N97% algae removal was maintained. In the controls treatment, the algal density showed a dramatic increase after 25 days of incubation, and the algal density far exceeded that in the capping and submerged macrophyte-added groups during the experimental periods.
3.2. Gas flux at the water-air interface The CH4 and CO2 fluxes showed a discernable pattern between treatments (Fig. 4). In the controls, the algal cells covered the water surface, which not only impaired the oxygen exchange between the water column and atmosphere but also enhanced algae decomposition. As a result, anaerobic digestion of algal-derived carbon led to a dramatic increase in CH4, which ranged between 33.5 and 159.5 μg/(m2·d) during the 65-day incubation. Flocculation-capping treatments accelerated algal decomposition and enhanced CH4 production, which maximally reached 252.5 and 224.8 μg/(m2·d) in the soil- and AC-capped systems,
Fig. 4. CH4 and CO2 flux at the water-atmosphere interface between treatments over the span of 65 days incubation.
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respectively. With the extension of the study period, the production of CH4 was impaired in capping or submerged macrophyte incubated treatments, which contrasted with the CH4 profile in the control (Supporting Information, SI, Fig. S1). The minimum CH4 flux was observed in the flocculation-capping-submerged macrophyte system, which substantially reversed the CH4 profile, and the average CH4 flux accounted for approximately 40% of that in the controls. A different pattern of CO2 flux was shown in comparison to that of CH4. Flocculationcapping migrated the majority of algal cells into sediment, while algae resuspension elevated oxygen levels in the water column, contributing to the aerobic digestion of algal-derived carbon and maximum CO2 production among the treatments (Fig. 4). The maximum CO2 flux was supposed to occur in the flocculation-capping-submerged macrophyte system since its ORP value was significantly higher than that of the other treatments. However, in the submerged macrophyte system, the average CO2 flux accounted for 38.3–71.2% of that in the flocculationcapping system, implying the submerged macrophytes may be responsible for the reduction of both CH4 and CO2 production. It should be noted that the CO2 production in the control was significantly lower (P = 0.041, b0.05) than that in the other groups, suggesting the algal biomass regulated the carbon fate. In contrast to the production of CH4, the peak of CO2 flux appeared during the later stage of the study period, particularly in the submerged macrophyte- incubated system. (Fig. S2). 3.3. Shift of microorganism community in the sediment The populations at the phyla level were identified between treatments and are presented in Fig. 5a. It was shown that Firmicutes (52.23%), Proteobacteria (24.29%), Chloroflexi (6.94%), Acidobacteria (3.71%) and Cyanobacteria (2.25%) were the dominant phyla in controls. The relative abundances of Firmicutes, Chloroflexi, and Cyanobacteria tended to decrease in the flocculation-AC capping as well as in the submerged macrophyte-incubated systems after 65 days of incubation. In contrast, the total percentage of predominant phyla, including Proteobacteria, Bacteroidetes and Acidobacteria, increased from 5.55% to 63.46%. Further analysis of the microbial community profiles was conducted at the genus level (Fig. 5b). Among 308 different detected genera bacteria, the abundance of Arenimonas, Actibacter, Thermomonas and Acidobacteria was highly enriched in the presence of submerged macrophytes. To be specific, the abundance of Arenimonas was approximate 26 times higher in submerged macrophyte incubated treatments than controls, and Actibacter, Thermomonas and Acidobacteria were about 24, 6 and 3 folds higher than control, respectively. On the other hand, the abundance of Clostridium, Romboutsia and Sporacetigenium was remarkably reduced with addition of submerged macrophyte, which constituted 2.8–8.2%, 20.5–22.8%, and 22.0–50.2% of that in control. In addition, the relative abundance of the genera Thermoanaerobaculum, Roseomonas, Limnobacter and Novosphingobium was also largely stimulated compared to that of the control. The present results indicated that flocculation-capping followed by submerged macrophyte incubation were critical contributors to the shift in the community structure of microorganisms. 3.4. Carbon budget The carbon budget in the treatments was assessed, including carbon content in sediment, aquatic phase, phytoplankton, submerged macrophytes biomass as well as the GHGs (CO2 and CH4). Before treatment, the predominant media of carbon stock in the study was sediment (44.78 g), followed by the aquatic phase (0.21 g) and phytoplankton (0.03 g) (Fig. 6). In controls, after 65 days incubation, a nearly 40-fold increase of carbon content appeared in the algal cells, 0.75 g of carbon turned into gaseous carbon (including CO2 and CH4), and a 9.4% reduction in the carbon content in the sediment was observed. However, flocculation, subsequent capping as well as the associated submerged
macrophyte incubation impacted the carbon fraction greatly, which slightly reduced aqueous carbon, while its fraction in the sediment increased by 1.27–2.89%. Capping materials were linked with gaseous carbon content: the utilization of soil as a capping material increased the gaseous carbon by 10.67% compared to that of the control, whereas the employment of AC hardly impacted the gaseous carbon fraction. After 65 days incubation, the biomass carbon (indicated by the carbon content in submerged macrophytes) accounted for 0.56% and 0.91% of the total carbon in the systems with soil and AC as capping materials, respectively. In Fig. 6, it can be clearly seen that the incubation of submerged macrophytes resulted in a reduction in algal-originated gaseous, which were transferred to vegetable biomass. 4. Discussion 4.1. Flocculation-capping-plant induction systems are effective for HABs removal Developing cost-effective and environmentally benign ways to remove HABs from aquatic systems is essential for restoring the deteriorated water quality. Special attention had been paid to the use of flocculation-based approaches, which are useful to settle algae cells to sediment. Traditional inorganic flocculants, such as ferric salts or aluminum salts (Sun et al. 2012; Takaara et al. 2007), are effective in removing algae, but these flocculants have some disadvantages and lead to various ecological concerns, such as the potential risk to the ecosystem imposed by residual Al. Additionally, the decay of dense algal cells may contribute to the release of nutrients and an expansive area of dark, discolored water called “black bloom”, which causes greater threat to water quality (Zhang et al. 2016). Previously, we proposed a biological strategy for simultaneous HABs removal and cyanotoxin degradation (Li et al. 2016). While these efforts provided promising insights for quick and efficient HABs control, their long-term effects on HABs control were not satisfactory because the flocs were frequently subjected to bioor wind-induced disturbances, which facilitated algae resuspension. In the present study, algae density didn't reduced significantly during the incubation in control, in contrast, proliferation of algal cells contributed to nearly 1.8-flod increase of the algae density (Fig. 3). Flocculationcapping treatment capable of N98% algal removal relative to that of the control, but the resuspension of algal cells led to the impairment of removal efficiency. This concern can be solved when the submerged macrophytes were incubated following capping. As illustrated in Fig. 3, N98% algae removal efficiency was achieved throughout the 65 days experiment, and this effect depended less on the capping material, indicating that the submerged macrophytes were the dominant contributor to long-term HABs control. 4.2. Bio-pump-based carbon capture and GHGs reduction The link between the nutrient supply and the appearance of HABs has been proposed frequently. It is accepted that the availability of dissolved inorganic nitrogen and phosphorus is most likely to influence phytoplankton growth. However, instead of being exclusively dependent on nitrogen and phosphorus concentration, the proliferation of algae can highly rely on atmospheric CO2 levels (Bussi et al. 2016). Atmospheric or dissolved CO2 (or HCO3−) can be fixed by cyanobacterial cells, which is helpful in alleviating the “greenhouse effect”. However, the collapse of severe HABs is generally associated with the return of atmospheric carbon, in a more worse way (CH4, which exhibited 45 times stronger GHGs effects than CO2 (Kosten et al. 2016)). The cyanobacterial biomass generated from the fixed CO2 can be utilized for other purposes (Chen et al. 2012), while in HABs water, the reuse of algal-derived carbon lies in the conversion of CH4 to CO2, which requires a substantial improvement in the microenvironment at the sediment-water interface. The flocculation-capping-submerged macrophyte induction treatments caused abrupt increase of ORP value
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Fig. 5. Microbial community analyses of distribution of phyla (a) and heat-map of the classified genera (b) in treatments.
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Fig. 6. The carbon budget in 5 treatments over the span of 65 days incubation. The original column indicates the carbon budget before treatment.
(from approximately −200 mv to 12 mv), indicating that the production of CO2 is favored. In controls, the 2.20 g reduction of the carbon content in the sediment contributed to nearly 40-fold increase of carbon content as phytoplankton biomass and 0.75 g GHGs (Fig. 6). This can be regulated using the proposed ecologically sound and sustainable method. After 65 days incubation, the carbon content in phytoplankton had nearly vanished in both the flocculation-capping and submerged macrophyte incubated treatment, suggesting the initially added phytoplankton were totally decomposed and the algal-derived carbon were converted. In comparison to controls, flocculation-capping treatments still contributed 0.74–0.83 g GHGs emission, while the sequestration of CO2 can be magnified through the incubation of submerged macrophytes, which were responsible for a 0.43–0.45 g decline in the CH4 released from the aquatic system to the atmosphere (Fig. 6). The possible explanation for this result may be that: 1) submerged macrophyte adsorb mineralized algal-derived carbon and contribute to the increase in the submerged macrophyte biomass; 2) the submerged macrophytes remarkably improved the oxygen level at sediment-water interface, as a result, the algal-derived carbon is mineralized to CO2, which can be supported by the pH values (Fig. S4); and 3) with the increase of ORP values at sediment-water interface (Fig. S3), the aerobic methane oxidation processes act as methane filter in aquatic systems (Donis et al. 2017; Michaud et al. 2017; Milucka et al. 2015), which is also related to the photosynthesis of the submerged macrophytes. Therefore, as the carbon budget analysis revealed, 1.28–1.45 g carbon was transferred to the submerged macrophytes and fixed in the ecosystem as biomass. Our results confirmed that through integrated approaches of flocculation-cappingsubmerged macrophyte induction, distribution of algal-derived carbon can be positively manipulated. During this process, the release of CO2 and CH4 can be substantially impaired while the submerged macrophyte biomass was stimulated. This is helpful for restoring a healthier ecological system dominated by submerged vegetation, which can be turned into edible proteins through reconstruction of the food web (Pan et al. 2012). 4.3. Shift in the microorganism structure is responsible for carbon reuse It has been suggested that organic matter could be released into sediment and mineralized into CO2 or CH4 during the decomposition of HABs (Mann et al. 2013), and capping the dense flocs can substantially accelerate the process. The most dominant genus, Clostridium (cellulolytic
anaerobic bacteria (Peng et al. 2014)), was highly enriched in the controls (Fig. 5a), which was helpful for the decay of algal cells. Carbon stored in the sediment showed a 0.54–1.23 g increase in flocculation and subsequent capping groups after 65 days incubation (Fig. 6), indicating the treatment sealed algal-derived carbon in the sediment and provided extra substrate for the mineralization of organic matter. In the controls, the ORP value constantly decreased throughout the study and reached −205 mv on day 65 (Fig. S3). In contrast, flocculation and subsequent capping as well as the submerged macrophyte addition substantially increased the ORP values. The ORP value in the flocculation-capping system generally remained at approximately −120 mv, but were turned to be positive with the incubation of submerged macrophytes (day 45) and further increased to nearly +15 mv by the end of the study, irrespective of capping with soil or AC. Despite substrates were essential for the production of CO2 or CH4, the ORP value at the sediment-water interface regulated the fate of carbon mineralization. Flocculation-capping largely accelerated the decomposition of the algal cells and caused a constant decline in the ORP values at the sediment-water interface (Fig. S3); this anaerobic microenvironment facilitated CH4 production (Fig. 4) by many species of methanogenic bacteria. Methane fermentation during anaerobic digestion comprises the following four steps: hydrolysis, acidogenesis, acetogenesis and methanation (Chandra et al. 2012). In this study, the maximum relative abundance of the genus sporacetigenium (Fig. 5b), which played an imperative role in producing acetate and butyrate (the intermediate product during CH4 formation) during the fermentation process (Zhao et al. 2012), was enhanced when flocculation-capping was conducted, but was reduced by 82.82 and 92.46% in the 2 groups that incubated with submerged macrophytes, respectively. In addition, the genus Romboutsia (responsible for hydrogen (Kuribayashi et al. 2017) and acetic acid (Gerritsen et al. 2014) production) was largely depressed in the submerged macrophyte- incubated system (Fig. 5b). This result suggested that the incubation of submerged macrophytes impaired the production of CH4 through modification of the microenvironment at the sediment-water interface, as well as the interdiction of the acetogenesis process during methane fermentation. The incubation of submerged macrophytes caused aerobic conditions at the sediment-water surface (Fig. S3). Given this circumstance, the relative abundance of the Arenimonas, a genus active in aerobic metabolism (Yuan et al. 2014), showed 26 to 28-fold increase relative to that of the controls (Fig. 5b). Therefore, the majority of the organic matter was supposed to be mineralized to CO2. However, CH4 was the dominant product during the mineralization of the organic matter in the submerged macrophytes incubated treatments, and the released CH4 content accounts for 87.10% and 90.64% of the sum of CH4 and CO2 for soil capping- submerged macrophytes and AC capping - submerged macrophytes treatments, respectively. The values are higher than those in previous literature (Kelley et al. 1990) but are consistent with a recent study that revealed the amount of algal-derived CH4 reached 92% of the sum of CH4 and CO2 (Yan et al. 2017). The probable reason is that the CO2 produced by the mineralization of organic matter was constricted in the water column, which caused an increase in the total inorganic carbon in the water and the reduction of the pH; this agreed well with the dynamic of pH (maintained at nearly 7.50 in the submerged macrophyte- added system, while reaching 7.81 in the flocculation-capping treatment) during this study (Fig. S4). In contrast, capping the dense HABs in sediment and subsequent algae decomposition depleted the oxygen, hence, the ORP value was maintained at approximately −120 mv and −150 mv. This microenvironment favored the proliferation of methanogen, as illustrated by the CH4 flux. Overall, in addition to alternation of the aquatic microenvironment (pH, ORP), the response of microbial compositions contributed to the carbon budget variation in the studied systems. Given the above data, the fate of phytoplankton-derived carbon in the studied systems is presented in Fig. 7. Carbon source enters the aquatic environment as carbon dioxide, which is assimilated by algae cells. However, the over growth of the algae and occurrence of HABs,
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Fig. 7. Conceptual schematic of the effects of flocculation-capping-submerged macrophytes incubation systems on regulation the fate of algal-derived carbon. The yellow arrows here indicate the increase or decrease of parameters. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
along with its subsequent collapse exhausted DO and caused anoxic or anaerobic environment. As a result, the majority of the algal-derived carbon would be turned to CH4, which can contribute to the global warming and in turn benefit HABs occurrence (route ① in Fig. 7). When flocculation and capping is jointly employed, although HABs are removed from water system, the decomposition of the sealed algal cells in the sediment could deteriorate the DO condition and accelerate the process of anaerobic digestion, which favored the production of CH4 (route ② in Fig. 7). The above vicious loop can be entirely turned back if submerged macrophyte incubation is followed. Despite algal decomposition depletes DO in the sediment, the photosynthesis of submerged macrophyte can compensate its depletion to some extent, hence the ORP value can be prompted substantially. With respected to the fate of algal-derived carbon, although algae decomposition cannot be prevented, the released carbohydrate can be the assimilated by the submerged macrophyte to produce biomass, or tend to be transferred to CO2 under the aerobic condition, contributing to the increase of inorganic carbon and reduction of pH (route ③ in Fig. 7), therefore a benign and sustainable circle can be achieved. 4.4. Environmental impact HABs are increasing worldwide and represent a serious threat to freshwater ecosystems (Fig. 1). Nitrogen, phosphorus and dissolved CO2 (CO2(aq)) have been traditionally implicated as having a crucial role in the development of HABs (Paerl et al. 2011; Visser et al. 2016). Some of the contributors to HABs, i.e., phosphorus, are nonrenewable resources and, ironically, are also considered hazardous materials for the occurrence of HABs. Free CO2 can be converted into highly available inorganic carbon, including HCO3– and CO32– (Yan et al. 2017), and as a result, leads to a rise in carbon availability in an aquatic environment, which is converted to algal biomass through assimilation. However, when the collapse of severe HABs occurs, the decay of the algal cells results in the release of algal-derived sources into the water column, causing an expansive area of dark, discolored water with extremely low DO
and prompting the production of CH4 (Zhang et al. 2016). During this carbon biogeochemical process, the atmospheric and aqueous CO2 represent a source of potential precursors for CH4 production, suggesting a break in the carbon cycle from land to lake. Therefore, repairing this broken cycle of carbon is not only essential for the reduction of GHGs emissions from aquatic systems but is also imperative for the reuse of algalderived organic matter. Carbon capture and storage are broadly recognized as having the potential to play a key role in meeting climate change targets (Bui et al. 2018), while carbon capture in HABsattacked water is rarely recommended. In this study, we attempted to repair broken aquatic ecosystems and a vicious carbon loop by utilizing solar energy to make the aquatic system sustainable. We proposed a multidisciplinary approach including flocculation, capping and submerged macrophyte incubation for HABs removal and CH4 emission regulation, and we confirmed that the methodology is capable of: 1) efficient removal of HABs from the water column, 2) remarkable impairment of GHGs (CO2 and CH4) emissions, and 3) conversion of algalderived carbon into plant biomass, which has the benefit that the biomass generated from the fixed CO2 can be further turned into marketable proteins through a reconstructed food web, forming a bigger sustainable circle. The results here provide an ecological principle for manipulating the carbon distribution between algae, water, gas and sediment, contributing to the recycling of carbon resources and alleviating of GHGs emissions, and bring prospects for turning HABs from nightmare situations into an opportunity from the perspective of carbon recycling. 5. Conclusion The combination of flocculation, capping and submerged macrophyte incubation method is promising for HABs removal. Flocculation and capping can seal the algae in the sediment and accelerated the decomposition of algal cells. The subsequent incubation of submerged macrophyte served as a bio-bump which not only deliver oxygen to the sediment-water interface, but also turned algal-derived carbon
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source into plant biomass, hence prevented considerable CH4 production and emission. This environmental benign biochemical process was achieved through the modification of the microenvironment at the sediment-water interface, depression of methanogenic bacteria, and aerobic CH4 oxidation. Acknowledgements This work was jointly supported by the Natural Science Foundation of China (NSFC 51478061, 51609024, 41877472, and 51779020), China Postdoctoral Science Foundation (2016M592641), and Chongqing Research Program of Basic Research and Frontier Technology (cstc2016jcyjA0498). Conflict of interest The authors declare no competing financial interest. Appendix A. Supplementary data Detailed information on analysis of microorganism community, dynamic of CH4 and CO2 flux, ORP, and changes of aquatic pH are supplied. Supplementary data associated with this article can be found in the online version, at doi: https://doi.org/10.1016/j.scitotenv.2018.11.262. References Bastviken, D., Cole, J., Pace, M., Tranvik, L., 2004. Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Glob. Biogeochem. Cycles 18, 1–12. Bui, M., Adjiman, C.S., Bardow, A., Anthony, E.J., Boston, A., Brown, S., Fennell, P.S., Fuss, S., Galindo, A., Hackett, L.A., Hallett, J.P., Herzog, H.J., Jackson, G., Kemper, J., Krevor, S., Maitland, G.C., Matuszewski, M., Metcalfe, I.S., Petit, C., Puxty, G., Reimer, J., Reiner, D.M., Rubin, E.S., Scott, S.A., Shah, N., Smit, B., Trusler, J.P.M., Webley, P., Wilcox, J., Mac Dowell, N., 2018. Carbon capture and storage (CCS): the way forward. Energy Environ. Sci. 11 (5), 1062–1176. Bussi, G., Whitehead, P.G., Bowes, M.J., Read, D.S., Prudhomme, C., Dadson, S.J., 2016. Impacts of climate change, land-use change and phosphorus reduction on phytoplankton in the River Thames (UK). Sci. Total Environ. 572, 1507–1519. Cai, G., Yang, X., Lai, Q., Yu, X., Zhang, H., Li, Y., Chen, Z., Lei, X., Zheng, W., Xu, H., Zheng, T., 2016. Lysing bloom-causing alga Phaeocystis globosa with microbial algicide: an efficient process that decreases the toxicity of algal exudates. Sci. Rep. 6, 20081. Chandra, R., Takeuchi, H., Hasegawa, T., 2012. Methane production from lignocellulosic agricultural crop wastes: a review in context to second generation of biofuel production. Renew. Sust. Energ. Rev. 16 (3), 1462–1476. Chen, I.C., Hegde, U., Chang, C.H., Yang, S.S., 2008. Methane and carbon dioxide emissions from closed landfill in Taiwan. Chemosphere 70 (8), 1484–1491. Chen, P.H., Liu, H.L., Chen, Y.J., Cheng, Y.H., Lin, W.L., Yeh, C.H., Chang, C.H., 2012. Enhancing CO2 bio-mitigation by genetic engineering of cyanobacteria. Energy Environ. Sci. 5, 8318–8327. Crafton, E.A., Glowczewski, J., Ott, D.W., Cutright, T.J., 2018. In situ field trial to evaluate the efficacy of Cutrine Ultra to manage a cyanobacteria population in a drinking water source. Environ. Sci.: Water Res. Technol. 4 (6), 863–871. Donis, D., Flury, S., Stöckli, A., Spangenberg, J.E., Vachon, D., McGinnis, D.F., 2017. Full-scale evaluation of methane production under oxic conditions in a mesotrophic lake. Nat. Commun. 8 (1), 1661. Gerritsen, J., Fuentes, S., Grievink, W., van Niftrik, L., Tindall, B.J., Timmerman, H.M., Rijkers, G.T., Smidt, H., 2014. Characterization of Romboutsia ilealis gen. nov., sp. nov., isolated from the gastro-intestinal tract of a rat, and proposal for the reclassification of five closely related members of the genus Clostridium into the genera Romboutsia gen. nov., Intestinibacter gen. nov., Terrisporobacter gen. nov. and Asaccharospora gen. nov. Int. J. Syst. Evol. Microbiol. 64 (5), 1600–1616. Glibert, P.M., Icarus Allen, J., Artioli, Y., Beusen, A., Bouwman, L., Harle, J., Holmes, R., Holt, J., 2014. Vulnerability of coastal ecosystems to changes in harmful algal bloom distribution in response to climate change: projections based on model analysis. Glob. Chang. Biol. 20 (12), 3845–3858. Kelley, C.A., Martens, C.S., Chanton, J.P., 1990. Variations in sedimentary carbon remineralization rates in the White Oak River Estuary, North Carolina. Limnol. Oceanogr. 35 (2), 372–383.
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