A trigger mechanism of herbicides to phytoplankton blooms: From the standpoint of hormesis involving cytochrome b559, reactive oxygen species and nitric oxide
Graphical abstract
Introduction
The hazard of phytoplankton blooms and controlling of them have been crucial issues of freshwater and coastal environment. Several key factors including nitrogen and phosphorus resources (Blomqvist et al., 1994; Smith, 1983; Xie et al., 2003), pH (An and Jones, 2000) and temperature (George et al., 2015; Green and Aller, 1998; Yamamoto and Nakahara, 2005) have been proposed to account for the occurrence of phytoplankton blooms. However, these factors were thought to be external conditions that catalyzed the bloom development rather than primary or initial ones, causing corresponding control measures to fall short of expectation. Several studies have now documented the stimulatory effects of low-level (levels below no observed effect concentrations or environmental residual concentrations) environmental contaminants such as polycyclic aromatic hydrocarbons, pentachlorophenol and pesticides on cyanobacteria and algae, which were thought to contributed to phytoplankton blooms (Cedergreen et al., 2007; Morais et al., 2014; Qiu et al., 2013; Zhu et al., 2012). This phenomenon is called hormesis, a distinctly beneficial effect of low-dose toxic substances to organisms.
Hormesis is a dose-response relationship characterized by low-dose stimulation and high-dose inhibition (Calabrese and Baldwin, 2003). It has been observed in properly designed studies and is broadly generalizable as being independent of chemical/physical agent, biological model, and endpoint measured (Calabrese and Baldwin, 2002; Calabrese and Blain, 2011; Carere and Claudio, 2014). However, to date, mechanisms of hormesis have been elusive due to the complexity that integrates the ranges and intensities of stimulation with testing compounds and with organisms. The present hypothetical mechanisms include oxidative stress (OS), overcompensation stimulation, receptor-mediated mechanisms, and signaling-mediated mechanisms (Arumugam et al., 2006; Calabrese, 2013, 2015; Carere and Claudio, 2014). The most noteworthy one is the cellular adaptation to OS, as it has been used to address the stimulatory mechanism of compounds or severe environmental conditions on a variety of types of organisms including human and animal cells, plants, bacteria and cyanobacteria (Belz et al., 2011; Chobot and Hadacek, 2009; Hoffmann et al., 2013; Ludovico and Burhans, 2014; Luna et al., 2014; Mittler, 2017; Ristow and Schmeisser, 2011; Semchyshyn, 2014). In particular, the differentiation of cells from human, mouse, and Drosophila was enhanced by increasing reactive oxygen species (ROS), whereas lowering cellular ROS slowed the rate of differentiation (Hamanaka et al., 2013; Juntilla et al., 2010; Owusu-Ansah and Banerjee, 2009). Although the cellular adaptation to equilibrium shifting of OS is crucial to physiology, a widely applicable mechanism of OS involving ROS and reactive nitrogen species (RNS) for hormesis has not been clarified.
Herbicides, a type of pollutants generally detected in soil and aquatic environment, are drawing research interests due to their potential hazard to organisms. It is especially interesting that sulfonylurea, imidazole and organophosphorus herbicides have been demonstrated to favor algal and cyanobacterial proliferation in the laboratory (Cedergreen, 2008; Cedergreen et al., 2007), which was considered to be a main factor in inducing algae blooms (Sun et al., 2013). Some studies attributed stimulative effects of herbicides, including organophosphorus and substituted ureas herbicides on algae to phosphorus utilization and reactive oxygen species (ROS) (Qiu et al., 2013; Subramanian & Sampoornam, 1994; Valiente et al., 2012; Zhou et al., 2004). Field observations demonstrated that Microcystis wesenbergii bloomed a few days after application of organophosphorus herbicides around the lake for several times (Li et al., 2010), indicating possible connections between algae blooming and the use of herbicides. In the present study, we investigated the hormesis effects of two widely-used herbicides, triazine and substituted ureas on green algae and cyanobacteria, in an effort to clarify the regulatory role of ROS and RNS in hormesis effect of herbicides on phytoplankton blooms.
Triazine herbicides and substituted ureas herbicides can inhibit photosynthesis of plants and phytoplankton by blocking electron transfers within photosystem II (PSII). As detailed in Fig. 1, electrons produced from oxidation of water molecules are transferred from primary electron donor, P680 to a primary electron acceptor, pheophytin (Pheo), after which a plastoquinone (QA) accepts electrons and then transfers them to a second plastoquinone (QB), proceeding with normal photosynthesis (Broser et al., 2011; Hankamer et al., 2001). Triazine and substituted ureas herbicides can depress the electron transfer from QA to QB, thus causing photosynthesis inhibition and acceptor side photoinhibition (ASP) (Broser et al., 2011; Pospisil et al., 2006). ASP is characterized as the degradation of the D1 polypeptide by highly reactive singlet O2 formed (Allakhverdiev & Carpentier, 1997; Durrant et al., 1990; Miyao et al., 1995).
Cytochrome b559 (Cyt b559), an integral part of the PSII reaction center that possesses a spectrum of midpoint redox potentials (high-potential form of Cyt b559 (HP Cyt b559) and low-potential form of Cyt b559 (LP Cyt b559) et al.), can alleviate photoinhibition through electron donation and acceptation within PSII (Pospíšil, 2011; Pospisil et al., 2006; Pospíšil and Tiwari, 2010; Stewart and Brudvig, 1998). Numerous studies have addressed that Cyt b559 can exchange electrons with inherent P680+, Pheo− and QA− (Davis and Tai, 1986; Roncel et al., 2001), accompanied by oxygen reduction (Pospíšil, 2011; Pospíšil and Tiwari, 2010) and superoxide generation, causing oxidation or reduction of heme iron within Cyt b559 (Barber and De, 1993; Buser et al., 1992; Mor et al., 1997; Ortega et al., 1989; Sinha et al., 2010). In this sense, Cyt b559 serves to protect PSII from photoinhibition and creates extra ROS simultaneously. As mentioned before, equilibrium shifting of OS involving ROS generates direct impacts on physiological processes of cells; it is therefore necessary to investigate the vital roles of Cyt b559 in hormesis produced by herbicides and corresponding OS equilibrium shifting for further understanding of hormesis. Moreover, Cyt b559 could also be modulated by nitric oxide (NO) (Shi et al., 2011), a widely existed signal molecule that was reported to affect the structure and functions of Cty b559 (Mello et al., 2012).
Taken together, the objective of the present work is to clarify the stimulatory mechanism underlying phytoplankton blooms by the following steps: 1) to verify the hormesis effects of herbicides on phytoplankton, 2) to determine the content of Cyt b559 in different thermodynamic states and the level of intracellular ROS and NO under the effect of herbicides, 3) to clarify the regulatory process of Cyt b559 with regards to ROS and NO and reveal an underlying mechanism of hormesis in this system, 4) to propose a new possible cause for phytoplankton blooms.
Section snippets
Experimental materials
The test compounds were triazine herbicides and substituted ureas herbicides, seven species in total which were purchased from Sigma-Aldrich Co. LLC. (Shanghai, China). The detailed information is listed in Table 1.
Cyanophyta Microcystis aeruginosa (M. aeruginosa) and Chlorophyta Selenastrum capricornutum (S. capricornutum) were obtained from Institute of Hydrobiology, Chinese Academy of Sciences (Wuhan, China) and underwent experiments. The microalgae were cultured at 22 °C BG-11 culture
The effect of triazine and substituted ureas herbicides on M. aeruginosa and S. capricornutum at 96 h
In the present study, the effect of seven herbicides on cyanobacteria (M. aeruginosa) and on green algae (S. capricornutum) at 96 h were evaluated. The dose-response relationship of monuron on M. aeruginosa and on S. capricornutum are shown in Fig. 2A-1 and Fig. 2A-2, respectively (other results detailed in Supplementary Fig. 2 and Supplementary Fig. 3), in which the fitted curves were plotted by previous methods (Deng et al., 2012). Generally, herbicides generates low-dose stimulation and
Discussion
The experimental results demonstrate that triazine herbicides and substituted ureas herbicides show striking hormesis effects on M. aeruginosa and S. capricornutum, which are in agreement with previous observations (Cedergreen, 2008; Cedergreen et al., 2007; Valiente et al., 2012). For convenience, the phases in which herbicides produce increasing stimulation on algae and cyanobacteria are named Stage I, and that in which the stimulation decreases followed by gradual enhancement of inhibition
Conclusions
Seven triazine and substituted ureas herbicides exhibited hormesis effects on Microcystis aeruginosa and Selenastrum capricornutum, among which the stimulatory concentration ranges of herbicides generally coincided with those detected in natural waters. It is inferred that herbicides residual in water environment are like to be a contributory factor to phytoplankton blooms. There is a need for consideration about low-dose environment contaminants in terms of their environmental risks. Moreover,
Data availability
Data that support the findings of the current study are available from the corresponding author on reasonable request.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank Shengyou Huang and Ruochong Gong for the assistance in the experiments. This work is funded by the Foundation of the State Key Laboratory of Pollution Control and Resource Reuse, China (PCRRK16007), the National Natural Science Foundation of China (21577105, 21777123), the National Water Pollution Control and Treatment Science and Technology Major Project of China (2018ZX07109-1), the Science & Technology Commission of Shanghai Municipality (14DZ2261100, 17DZ1200103), the State Key
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