Long-term transformation of nanoscale zero-valent iron explains its biological effects in anaerobic digestion: From ferroptosis-like death to magnetite-enhanced direct electron transfer networks
Graphical abstract
Introduction
Due to its intrinsic high reactivity, large surface areas and environmental friendliness, nanoscale zero-valent iron (nZVI) has been intensively used for in situ environmental remediation over the past decades (Xu et al., 2020a, 2020b; Phenrat et al., 2009). On the other hand, as a kind of nanoparticle, nZVI has attracted much attention in terms of nanotoxicology, and indeed, the adverse effects of nZVI on aquatic organisms, microorganisms and mammalian cells have been widely documented (Chen et al., 2012; Kotchaplai et al., 2017). Disruption of cell membrane structures, DNA damage and apoptosis related to the production of reactive oxygen species (ROS) are potential toxicity mechanisms of nZVI in a broad range of microbes (Lee et al., 2008; Yang et al., 2013). However, the majority of current studies have focused on the short-term effects of nZVI on pure cultures. In long-term application, nZVI certainly oxidizes over time (i.e., “ages”), which would likely change its bioavailability and toxicity (Phenrat et al., 2009; Chen et al., 2012). Several in vitro studies have shown that the bactericidal effect of pristine nZVI is greater than that of aged nZVI or nanoscale iron oxides (Lee et al., 2008; Auffan et al., 2008). Moreover, some bacteria preferentially thrive by utilizing (semi)conductive iron minerals for respiration in natural environments (Kato et al., 2010, 2012). Thus, the biological effects of nZVI, either toxic or beneficial to microbial communities, are supposedly associated with its aging process. Unfortunately, to date, the causal mechanisms linking the long-term transformation of nZVI with its biological effects are not yet defined.
Anaerobic digestion (AD) is considered to be the most widely used and cost-effective technology for high-strength wastewater treatment and renewable energy recovery (Li et al., 2019). Recently, nZVI was reported to be a promising candidate for elevating methane production in AD, improving the hydrolysis-acidification steps and/or promoting the hydrogenotrophic methanogenesis (HM) process (Feng et al., 2014; He et al., 2017). Nevertheless, the inhibition of methanogenesis was also observed due to the destroyed cell integrity and the rapid H2 accumulation caused by nZVI dissolution (Yang et al., 2013). Such contradictory effects of nZVI in AD may derive from the complex interactions between nZVI and microbial aggregates, which would not only alter nZVI reactivity but also affect the physiological status of cells (Auffan et al., 2008; Jin et al., 2015). For example, the interactions of nZVI with extracellular polymeric substances (EPSs) could reduce its inhibition of the AD process by avoiding the fast accumulation of H2 and restricting damage to cell integrity (He et al., 2020). Moreover, a rebound in cell number was observed after prolonged exposure to nZVI, which is attributed to the decreased membrane-fluidizing effect of fatty acids that hindering the interactions between cells and nZVI (Kotchaplai et al., 2017). However, previous studies mainly focused on the responsive mechanism of microbial cells at the single or sequential nZVI exposure endpoints and neglected the dynamic transformation processes of nZVI during long-term incubation. Unlike most aging studies of nZVI undertaken in pure water or simplified simulation conditions (Pullin et al., 2017; Sarathy et al., 2008), limited research in terms of the transformation of nZVI has been conducted in AD where more complex microbial communities are involved, which are closely correlated with the performance of methanogenesis.
Four stages, namely, hydrolysis, acidogenesis, acetogenesis and methanogenesis, are predominantly involved in canonical AD, in which syntrophic acetogenesis often governs the overall rate of anaerobic digestion process due to the slow and indirect way of interspecies electron transfer (IET) via H2/acetate (Huang et al., 2016; Rotaru et al., 2014). In contrast, as a faster and more specific electron transfer pathway, direct IET (DIET), in which species exchange electrons through electrical connections, including conductive pili, cytochromes (Cyt) and iron minerals, was demonstrated to be an alternative to IET in anaerobic methane-producing communities (Lovley, 2017; Shi et al., 2016). In comparison to IET, DIET can provide more energy benefits for syntrophic partners and accelerate reaction rate, finally enhancing methane production (Lovley, 2017). The transformation of nZVI might boost methane production, since some aging products, especially the magnetite, were conductive and probably participated in DIET (Kato et al., 2010; Suanon et al., 2016; Li et al., 2015). In addition, supplementation with nZVI or nanoscale iron oxides could biochemically improve the electron transfer by mediating electron transfer chain activity and the biosynthesis of fluvic acid in EPSs (He et al., 2020; You et al., 2021). Consequently, the transformation of nZVI may thrive in electron transfer networks, which affected the cooperative behaviors between consortium members and further facilitated methanogenesis (Kato et al., 2012; You et al., 2021). However, there is still a lack of detailed studies demonstrating DIET in syntrophic communities during the aging of nZVI in AD.
In this study, we aimed to investigate the dynamic relationships between transformation processes and biological effects of nZVI in AD, with an emphasize on the potential DIET-stimulation mechanism for methanogenesis during nZVI aging. To achieve this goal, the performance of ADs was consecutively estimated during long-term exposure to nZVI. Simultaneously, the aging products of nZVI as well as their interactions with anaerobes at different operation stages were characterized through multiple spectrum analysis and electron microscopy images. The dynamics of functional gene regulation, microbial metabolism and electron transfer potential were further quantified to explore the adaptative strategy of anaerobes in response to nZVI aging.
Section snippets
Anaerobic reactor operation and nZVI exposure experiments
Anaerobic sequencing batch reactors (AnSBRs) with a working volume of 4 L (Fig. S1A) were constructed to culture anaerobic sludge taken from the AD of Jiangxinzhou Municipal Wastewater Treatment Plant (Nanjing, China). The accumulation and cultivation processes were performed with the injection of synthetic wastewater (SW) and 17.19 g volatile solids (VS)/L into AnSBRs. A SW with glucose, NH4Cl and KH2PO4 as carbon, nitrogen and phosphorus sources was employed, and the specific components of SW
Chronic effects of nZVI on the performance of AD
COD removal and CH4 production are two decisive indicators that reflect the biological effects of nZVI on AD. Fig. 1A showed that the COD removal efficiency in R1 fluctuated between 65.61% and 80.56%, with an average value of 74.63% during the whole exposure period. After the addition of nZVI and 12 days of operation, the average COD removal efficiency decreased to 50.98%, indicating overall deterioration in the effluent performance in R2. After that, a gradual recovery to 80.63% at day 27 was
Conclusions
This study demonstrated that the effects of nZVI on methanogenesis were time dependent, which was attributed to the transformation of nZVI as well as the specific regulation of microbes in response to nZVI aging. When operating AD with nZVI, the nZVI-induced ferroptosis-like death to anaerobes could inhibit the methane production at initial exposure period, whereas a recovery and promotion of methane production were achieved with the aging of nZVI, as a result of the reinforced membrane
Declaration of Competing Interest
There are no conflicts of interest to declare.
Acknowledgment
We are grateful for the grants for the project from National Natural Science Funds for Youth of China (Grant Nos. 42107386, 52009031), Key Program of National Natural Science Foundation of China (Grant No. 92047201), National Postdoctoral Program for Innovative Talents (Grant No. BX20190106) and PAPD.
References (55)
- et al.
Metagenomic analysis reveals nonylphenol-shaped acidification and methanogenesis during sludge anaerobic digestion
Water Res.
(2021) - et al.
Enhanced anaerobic digestion of waste activated sludge digestion by the addition of zero valent iron
Water Res.
(2014) - et al.
Interactions between nanoscale zero valent iron and extracellular polymeric substances of anaerobic sludge
Water Res.
(2020) - et al.
Impact of zero-valent iron nanoparticles on the activity of anaerobic granular sludge: from macroscopic to microcosmic investigation
Water Res.
(2017) - et al.
Hydrogen production from the dissolution of nano zero valent iron and its effect on anaerobic digestion
Water Res.
(2016) - et al.
Effect of bacterial communities on the formation of cast iron corrosion tubercles in reclaimed water
Water Res.
(2015) ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12
Res. Microbiol.
(2001)- et al.
Enhancement of methane production in anaerobic digestion process: a review
Appl. Energy
(2019) - et al.
Zero valent iron simultaneously enhances methane production and sulfate reduction in anaerobic granular sludge reactors
Water Res.
(2015) - et al.
Insight into the mechanism of ferroptosis inhibition by ferrostatin-1
Redox Biol.
(2020)
Impact of nano zero valent iron on tetracycline degradation and microbial community succession during anaerobic digestion
Chem. Eng. J.
The effect of aqueous corrosion on the structure and reactivity of zero-valent iron nanoparticles
Chem. Eng. J.
Nano-decocted ferrous polysulfide coordinates ferroptosis-like death in bacteria for anti-Infection therapy
Nano Today
Effect of nanoscale zero-valent iron and magnetite (Fe3O4) on the fate of metals during anaerobic digestion of sludge
Water Res.
Iron speciation and iron species transformation in activated sludge membrane bioreactors
Water Res.
Vivianite as an important iron phosphate precipitate in sewage treatment plants
Water Res.
Iron and phosphorus speciation in Fe-conditioned membrane bioreactor activated sludge
Water Res.
Impact of nano zero valent iron (NZVI) on methanogenic activity and population dynamics in anaerobic digestion
Water Res.
Clarifying electron transfer and metagenomic analysis of microbial community in the methane production process with the addition of ferroferric oxide
Chem. Eng. J.
Effects of zero valent iron on nitrate removal in anaerobic bioreactor with various carbon-to-nitrate ratios: bio-electrochemical properties, energy regulation strategies and biological response mechanisms
Chem. Eng. J.
Insights into the short-term effects of CeO2 nanoparticles on sludge dewatering and related mechanism
Water Res.
Insights into the microbial response of anaerobic granular sludge during long-term exposure to polyethylene terephthalate microplastics
Water Res.
Chlorpyrifos and 3,5,6-trichloro-2-pyridinol degradation in zero valent iron coupled anaerobic system: performances and mechanisms
Chem. Eng. J.
Relation between the redox state of iron-based nanoparticles and their cytotoxicity toward Escherichia coli
Environ. Sci. Technol.
Reactivity of nanoscale zero-valent iron in unbuffered systems: effect of pH and Fe(II) dissolution
Environ. Sci. Technol.
Stabilization or oxidation of nanoscale zerovalent iron at environmentally relevant exposure changes bioavailability and toxicity in medaka fish
Environ. Sci. Technol.
Regulation of lipid peroxidation and ferroptosis in diverse species
Gene. Dev.
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