New insight into ammonium removal in riverbanks under the exposure of microplastics

Highlights

• MPs remarkedly changed riverbank water stable aggregate and water holding capacity.

• MPs accumulation reduced ammonium removal by 8.2 %−12.8 % in riverbanks.

• MPs accumulation decreased N₂O emissions by 16.3 %−34.3 % in riverbanks.

• MPs decreased nitrifier and the relatedly functional gene abundance in riverbanks.

• MPs indirectly weakened riverbank nitrification by changing physical properties.

Abstract

Riverbanks play the key role in ammonium removal from runoff entering river. Currently, microplastics (MPs) are frequently detected in riverbanks receiving urban and agricultural runoff. Nevertheless, the effect of MPs accumulation on ammonium removal in riverbanks is still unknown. We utilized sediment flow-through reactors to investigate the impact and mechanism of MPs accumulation on ammonium removal in riverbanks. These results revealed that MPs accumulation decreased ammonium removal in sediment by 8.2 %−12.8 % resulting from the reduction in nitrifier abundance (Nitrososphaera and Nitrososphaeraceae) and genes encoding ammonium and hydroxylamine oxidation (amoA, amoB, amoC, and hao) by MPs accumulation. Furthermore, MPs accumulation decreased the substrate and gene abundance of hydroxylamine oxidation process to reduce N₂O emission (16.3 %−34.3 %). Notably, mathematic model verified that sediment physical properties changed by MPs accumulation were direct factors affecting ammonium removal in riverbank. It was suggested that both the biotoxicity of MPs and sediment physical properties should be considered in the ammonium removal process. To summarize, this study for the first time comprehensively clarifies the impact of MPs on the ammonium removal capacity of riverbanks, and provides information for taking measures to protect the ecological function of the riverbank and river ecosystem from MPs and ammonium pollution.

Introduction

Riverbanks are the transition region between the terrestrial and aquatic ecosystem (Chen et al., 2020, Covatti and Grischek, 2021). Because of their special location, riverbanks create a barrier between anthropogenic activities and natural rivers, which can prevent the deterioration and eutrophication of river ecosystems (Cole et al., 2020, Feld et al., 2018). For example, with the intensive application of nitrogen fertilizer and the unreasonable discharge of wastewater, ammonium accumulates in the river ecosystem due to untimely microbial transformation and cause eutrophication in river (Jiang et al., 2022, Gooddy et al., 2016). Riverbanks are the hot spots and hot moments for the biogeochemical cycle of nitrogen (Dwivedi et al., 2018), and can reduce ammonium concentrations in runoff to 0.06 − 0.80 mg L⁻¹ (Covatti and Grischek, 2021). Nitrification is the most common ammonium transformation pathway in riverbanks and is considered as the sink of ammonium in riverbanks (Covatti and Grischek, 2021, Hu et al., 2016). Thus, more attention should be focused on riverbank nitrification to better understand the nitrogen cycle of the biosphere.

Riverbanks can also withhold microplastics (MPs) in urban runoff (Werbowski et al., 2021) and agriculture runoff (Liu et al., 2019, Liu et al., 2021). The abundance of MPs has been reported to be 3877 ± 2356 particle kg⁻¹ in riverbanks of the Yangtze River (Zhou et al., 2021). Previous studies indicate that massive MPs accumulation can affect nitrification in terrestrial and aquatic ecosystems. Han et al. (2022) reveal that MPs accumulation inhibits the transformation of ammonium, and the inhibition can be exacerbated with MPs concentration in paddy fields. Seeley et al. (2020) and Zhu et al. (2022) indicate that MPs addition will inhibit nitrification in sea sediment and agricultural soil. A study further found that MPs accumulation greatly decreases the abundance of nitrifiers and the relatedly functional genes in agricultural soils, and the reduces the emission of nitrous oxide (N₂O) formed by hydroxylamine oxidation process (Gao et al., 2021), which the N₂O is formed by hydroxylamine oxidation (Butterbach-Bahl et al., 2013) and contribute to the global greenhouse effect (Chen et al., 2020). Currently, the recognized mechanism of MPs inhibiting nitrification is as following: 1) plasticizer or additive released by MPs pose the toxicity to nitrifier activity (Zhu et al., 2022); 2) small size particles can disrupt the membrane potential, penetrate the cell membrane, and destroy both membrane integrity and reactive oxygen species balance (Lee et al., 2022, Yang et al., 2020). Nevertheless, although a large amount of MPs accumulate in riverbanks, very little is known about the response of nitrifier and the relatedly functional genes to MPs.

In addition to microbial activity, previous study also revealed that soil physical properties were affected by MPs accumulation (Mbachu et al., 2021). A study reported by Machado et al. (2018) indicated that MPs accumulation decreases soil bulk density and water stable aggregates. Zhang et al. (2019) and Liang et al. (2021) found that MPs accumulation accelerates macroaggregates breaking into microaggregates. Normally, soil physical properties are considered the most important set of factors affecting nitrification (Shrestha et al., 2015), and soil nitrification is significantly affected by soil aggregate size (Hernandez-Ramirez et al., 2021, Wu et al., 2021), bulk density (Chen et al., 2015, Yan et al., 2008), and water holding capacity (Cheng et al., 2014, Xin et al., 2017). For example, Meng et al. (2020) found that increased riverbank moisture content above 27.03 % can inhibit nitrification. Jiang et al. (2011) indicated that macroaggregate can promote sediment nitrification differing to other size of aggregates. Compared with agricultural soil or river sediment, the soil structure and soil properties of riverbanks varied with the alteration of the river hydrology, leading to the different nitrification potentials in riverbanks (Xie et al., 2022, Sigler et al., 2022). However, it is unknown how nitrification responds to the change of riverbank sediment physical properties under the exposure of MPs. Furthermore, it is still unclear whether the MPs or sediment physical properties is the direct factor of riverbank nitrification.

Therefore, the laboratory microcosms were conducted using sediment flow-through reactors (FTRs) to explore the effects of MPs on sediment physical properties, ammonium removal efficiency, N₂O emission flux, microbial community composition, and functional genes associated with nitrifier. This study utilized pyrosequencing, metagenomic analysis and structural equation models to address the following questions: (i) What are the impacts of MPs on sediment physical properties? (ii) How does nitrification respond to MPs accumulation? (iii) How do MPs influence microbial community composition and ammonium oxidation gene abundance? (iv) What is the mechanism of MPs accumulation on riverbanks nitrification?