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Prevention of Cyanobacterial Blooms using Nanosilica: A Biomineralization-inspired Strategy Wei Xiong, Yiming Tang, Changyu Shao, Yueqi Zhao, Biao Jin, Tingting Huang, Ya'nan Miao, Lei Shu, Weimin Ma, Xurong Xu, and Ruikang Tang Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b02985 • Publication Date (Web): 26 Sep 2017 Downloaded from http://pubs.acs.org on September 26, 2017
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Environmental Science & Technology
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Prevention of Cyanobacterial Blooms using Nano-
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silica: A Biomineralization-inspired Strategy
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Wei Xiong,† Yiming Tang,‡ Changyu Shao,† Yueqi Zhao, †,§ Biao Jin, † Tingting Huang, ‡ Ya’nan
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Miao, ‡ Lei Shu, †,§ Weimin Ma*,‡, Xurong Xu*,§ and Ruikang Tang*,†
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†
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Hangzhou 310027, China ‡
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Center for Biomaterials and Biopathways, Department of Chemistry, Zhejiang University,
College of Life and Environmental Science, Shanghai Normal University, Shanghai 200234, China
§
Qiushi Academy for Advanced Studies, Zhejiang University, Hangzhou 310027, China
Keywords: cyanobacteria • bloom • silicification • nanoparticles • prevention
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ABSTRACT: Cyanobacterial blooms represent a significant threat to global water resources
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because blooming cyanobacteria deplete oxygen and release cyanotoxins, which cause the mass
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death of aquatic organisms. In nature, a large biomass volume of cyanobacteria is a precondition
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for a bloom, and the cyanobacteria buoyancy is a key parameter for inducing the dense
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accumulation of cells on the water surface. Therefore, blooms will likely be curtailed if
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buoyancy is inhibited. Inspired by diatoms with naturally generated silica shells, we found that
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silica nanoparticles can be spontaneously incorporated onto cyanobacteria in the presence of
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poly(diallyldimethyl-ammonium chloride), a cationic polyelectrolyte that can simulate
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biosilicification proteins. The resulting cyanobacteria-SiO2 complexes can remain sedimentary in
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water. This strategy significantly inhibited the photoautotrophic growth of the cyanobacteria and
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decreased their biomass accumulation, which could effectively suppress harmful bloom events.
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Consequently, several of the adverse consequences of cyanobacteria blooms in water bodies,
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including oxygen consumption and microcystin release, were significantly alleviated. Based on
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the above results, we propose that the silica nanoparticle treatment has the potential for use as an
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efficient strategy for preventing cyanobacteria blooms.
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INTRODUCTION
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As primary photosynthetic microorganisms, cyanobacteria are found almost everywhere and
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have a profound impact on the earth’s atmosphere and biosphere.1-3 However, cyanobacteria can
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also reproduce exponentially and uncontrollably, and they die rapidly under certain conditions
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such as virus infection,4,5 which is commonly referred to as a harmful cyanobacterial bloom.6,7
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The frequency of blooms has increased in water bodies around the world.6,7 These blooms
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produce cyanotoxins that can poison and cause the death of animals and humans,8-11 and more
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importantly, the resulting anaerobic water induces the large-scale death of aerobic organisms,
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threatens the safety of drinking water, and destroys aquatic ecosystems.12,13 For instance, a large-
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scale cyanobacterial bloom in Taihu Lake (Jiangsu Province, China) led to a highly publicized
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drinking water crisis in 2007 that affected more than five million people.7,13,14 To reduce and
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hopefully avoid the potential risks associated with cyanobacteria blooms, several approaches
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have been developed, such as the addition of toxic algaecides and flocculants.15,16 However,
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these methods have significant disadvantages, such as secondary pollution, low biological
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Environmental Science & Technology
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selectivity and adverse environmental impacts.17 Therefore, developing novel pathways for
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avoiding cyanobacterial blooms represents a great challenge.
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A cyanobacterial bloom is caused by variations in the vertical position of large volumes of
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cyanobacterial biomass, which develops gradually and accumulates over a long time.18 In nature,
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many cyanobacteria have intracellular gas vesicles that make the cells buoyant.19-21 The floating
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characteristic is an important factor in the occurrence of cyanobacterial blooms because buoyant
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cyanobacteria float upward to accumulate in dense surface blooms.19-21 Subsequently, their
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accelerated death induced by rising temperatures and light intensities, which result in the large-
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scale consumption of dissolved oxygen and the release of cyanotoxins when huge cyanobacterial
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cells are hard to disperse within certain time and space.8-13 Therefore, the control of buoyant cells
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is the key to preventing cyanobacterial blooms in advance. Compared with cyanobacteria,
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diatoms can use their siliceous walls as a ballast to control water column position.22,23 Cell walls
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made of silica (hydrated silicon dioxide) are called frustules.24 Inspired by diatoms, we
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conceived that cyanobacteria could be encapsulated within silica to confer upon them diatom-
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like features. It was also found that cyanobacteria with biosilica shells and green algae
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aggregates induced by silicification have the tendency to sink to the bottom due to the increased
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density.25,26 Compared with diatoms, the silica-adsorbed cyanobacteria cells can remain in a
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sedimentary state, thereby inhibiting rapid cell growth and subsequent death and possibly
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reducing the risks of blooms. However, one challenge is that cyanobacteria cannot inherently
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generate silica walls. Previous biomineralization research has shown that silica formation by
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diatoms is induced by polycationic peptides that contain polyamine.27,28 Recently, silicification
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proteins and long-chain polyamines (LCPA) have been reported to mimic biosilification proteins
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to induce silica precipitation in vitro.29-31 As a cationic polyelectrolyte containing positively
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charged quaternary amines, poly(diallyldimethylammonium chloride) (PDADMAC) has been
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successfully used to improve cell silicification abilities.25,26,32,33 Herein, we developed a feasible
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one-step treatment method of directly incorporating silica nanoparticles onto cyanobacteria using
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PDADMAC, and this approach can suppress cyanobacterial blooms via tactics that are analogous
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to those in diatoms.
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MATERIALS AND METHODS
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Cyanobacterial cell culture. In the experiment, Microcystis flos-aquae was isolated from
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Meiliang Bay, Taihu Lake, China (120º30′N, 31º27′E), a water body that has experienced an
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increased frequency and intensity of major cyanobacterial blooms in warm seasons in recent
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years. Microcystis flos-aquae cells were cultured at 30°C in a 500-mL reagent bottle (Schott
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Duran) containing 400 mL of BG-11 cultivation medium,34 buffered with Tris-HCl (5 mM, pH
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8.0) bubbled with 2% (v/v) CO2 in air (30 mL/min), and subjected to continuous illumination by
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fluorescent lamps (40 µE·m-2·s-1) for 24 h (OD730=0.2-0.3). The chlorophyll a concentration was
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determined spectrophotometrically in methanol.35,36
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Silica-induced cell sedimentation. In the experiment, commercially available silica
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nanoparticles (Ludox TM-40 colloidal silica, diameter (26±4) nm, 40 wt% suspension in water,
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purchased from Sigma–Aldrich, Saint Louis, Missouri, USA) were diluted to 5 g/L in NaCl
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solution (0.02 M). Aqueous NaCl solution (0.02 M) was also used to prepare a 1 g/L
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poly(diallyldimethylammonium chloride) (PDADMAC, Mw
