Bioavailability of organic phosphorus in the water level fluctuation zone soil and the effects of ultraviolet irradiation on it in the Three Gorges Reservoir, China

Jun-Min Gao 1, Zhu-Man Chen 1, Chao Wang 1, Fang Fang 2, Jun-Jie Huang 1, Jin-Song Guo 1

Highlights
•Enzymatically hydrolysable organic phosphorus in the water level fluctuation zone soil was dominated by labile monoester P.
•Ultraviolet irradiation could improve the bioavailability of organic phosphorus in the water level fluctuation zone soil.
•The increase of phytate-like P in NaOH extracts was significantly after ultraviolet irradiation (P < 0.01).
•The effect of ultraviolet irradiation on organic phosphorus bioavailability cannot be neglected.

Abstract
Ultraviolet (UV) irradiation is an abiotic pathway for the transformation of complex phosphorus (P) components into inorganic P in ecosystems. To explore the effect of UV irradiation on organic P (OP) bioavailability in the water level fluctuation zone (WLFZ) soil, we collected representative soil samples from WLFZ of the Pengxi River, a tributary of the TGR, China. We determined the contents of different forms of OP in the WLFZ soil through sequential extraction. The bioavailability of different forms of OP and the effect of UV light were characterised using a combination of enzymatic hydrolysis and UV irradiation. The OP contents of the different extracts (Po) were ranked as NaOH-Po > NaHCO3-Po > H2O-Po, whereas those of enzymatically hydrolysable organic P (EHP) were ranked as NaOH-EHP > NaHCO3-EHP > H2O-EHP. UV irradiation was found to improve OP bioavailability, as demonstrated by increased levels of UV-sensitive P (UV-P) and EHP in the extracts after irradiation. The total contents of bioavailable Po in extracts were 5.6–35.3% higher after UV irradiation than before irradiation. Thus, the effect of UV irradiation on the OP bioavailability and release activity cannot be neglected in TGR WLFZ soil.

Introduction
As the most important nutrient limiting factor in agricultural production, phosphorus (P) plays an important role in eutrophication of aquatic ecosystems. Inorganic forms of P (IP) are the major bioavailable P in the environment (Zhu et al., 2013). However, the content of organic P (OP), another important part of P, accounts for 15–80% of the total P (TP) in soil (Chen, 2018). Except for a small proportion of OP that is directly absorbed and used by crops, most OP can be used by crops only after its transformation into IP through biomineralisation and chemical decomposition. Different forms of OP, such as inositol phosphates, phospholipids, condensed P, and sugar phosphates, are also potential sources of P, and their amounts in sediment are comparable to those of IP (Zhu et al., 2013). Inositol phosphates are abundant forms of OP in most soils, existing as inositols in different phosphorylation states and isomeric forms (Turner et al., 2002a). Like IP, inositol phosphates in soil can be bound to iron-aluminum oxide, clay minerals, and humic substances due to adsorption effects (Gerke, 2015).

Because of the variety and complex structure of OP in soil, the soil OP content cannot be determined directly. Sequential extraction, which is on the basis of the hypothesis that chemical extractants can dissolve different P compounds selectively, is therefore generally applied to estimate the relative contents of different forms of P. Recently, sequential extraction procedures have been widely adopted to study the OP pools in sediments and soil, which can analyse IP and OP forms in environmental samples rapidly (Keller et al., 2012; Zhu et al., 2013; Ni et al., 2019; Wang et al., 2020). However, because most OP must be converted to IP through biomineralisation and chemical decomposition before it can be used by organisms, OP bioavailability estimates based on chemical solubility are misleading.

The enzymatic hydrolysis of OP has been traditionally considered to be the main pathway for transformation to IP (Monbet et al., 2007), which further links OP with uptake by plant and microorganisms. Turner et al. (2002b) used alkaline phosphatase (APase), phosphodiesterase (PDEase), and phytase to analyse the composition of water soluble molybdate-unreactive P forms from grassland soils, and classified them into three forms of bioavailable OP. Monbet et al. (2007) improved the enzymatic hydrolysis method developed by Turner et al. (2002b) by combining a variety of phosphatase enzymes and conducting experiments within the pH range of natural waters to characterise the bioavailability of dissolved OP under natural conditions. Thus, enzymatic hydrolysis has been widely used to characterise OP compounds and estimate their potential bioavailability in environmental samples (Büenemann, 2008; Zhu et al., 2013; Ni et al., 2019), and sequential extraction coupled with enzymatic hydrolysis has become a useful tool for identifying and quantifying individual OP species and monitoring the transformation and bioavailability of OP species in the environment (He et al., 2004; Zhu et al., 2013).

Ultraviolet (UV) light has an important impact on the migration and transformation of elements in aquatic and terrestrial ecosystems (Imoberdorf and Mohseni, 2011; Carena et al., 2020). UV irradiation is an abiotic pathway for the transformation of complex P components into IP in ecosystems (Francko and Heath, 1979) and can cause the photodegradation of OP in water, soil, and sediment (Sandy et al., 2013; Katagi, 2018; Li et al., 2019; Guo et al., 2020). In aquatic environments, UV irradiation affects the direct photodegradation of OP. Some OP compounds can release dissolved phosphate following decomposition after absorbing solar energy; this process is directly related to the structure and morphology of OP (Lesueur et al., 2005). It has been found that photochemical decomposition of OP into IP cannot be negligible after sedimentary OP enters the overlying water (Zhang et al., 2019). Dissolved P can also be released from resuspended sediments exposed to sunlight, and the dominant OP species participating in most photochemical reactions is the phosphate monoester (Guo et al., 2020).

Photodegradation of OP during sediment resuspension may be a potential pathway for phosphate supply to shallow lakes (Li et al., 2019). However, few studies have focused on the photochemical transformation of OP into IP in soil, and the information about the effect of UV light on OP bioavailability in soil is very limited. Previous studies have shown that UV irradiation can cause phosphate release and reduce the enzymatic hydrolysable OP (EHP) content in soil humic acid fractions (He et al., 2009; He et al., 2011). However, little is known about the transformation of EHP due to UV irradiation or its mechanism.

The Three Gorges Reservoir (TGR), built in the main stream of the upper Yangtze River, is the largest hydroelectric project ever conducted. Following the completion of the TGR in 2009, the hydrological conditions of the main stream and tributaries of the Yangtze River in the reservoir region have changed significantly. According to the design, the water level of the TGR is maintained at 145 m (low level) in the flood season (May–September) and 175 m (high level) in the drought season (October–February), which is opposite to that of natural rivers (Wang et al., 2020). The seasonal water level fluctuations of the TGR formed a water level fluctuation zone (WLFZ) with a total area of 350 km2 and vertical height of 30 m between high water level and low water level (Ye et al., 2011). WLFZ has the characteristics of both aquatic and terrestrial environments, in which the transport and transformation of matter and energy are very active (Bao et al., 2015).

The impact of environmental changes in the WLFZ of the TGR on the environmental behavior of soil nutrients has received much research attention in recent years. The forms, spatial distribution, and release mechanism of P in the WLFZ soil are research hotspots (Qu et al., 2019; Zhou et al., 2019; Wang et al., 2020). Due to the periodic inundation of WLFZ soil, soil P, such as Fe-bound P and organic P, can be reduced to soluble P and released into the overlying water, leading to eutrophication of surface water in the TGR (Zhou et al., 2019; Wang et al., 2020). Qu et al. (2019) characterised the properties of OP fractions in the WLFZ soil of the TGR, and found that periodic submersion/emersion cycles of the WLFZ soil facilitated the transfer of phytate-like P from Fe/Al-OP to the water column of the TGR. In addition, the anti-seasonal fluctuation of the TGR water level causes the soil in the WLFZ to be inundated in winter but exposed in summer, when it receives strong sunlight radiation that can cause OP photodegradation and influence its bioavailability in the WLFZ soil. However, to date, information on OP bioavailability in the soil of WLFZ related to UV irradiation remains scarce.
Therefore, in this study, we aimed to characterise OP mobility and bioavailability in the WLFZ soil of the TGR through a combination of sequential extraction and enzymatic hydrolysis. We also combined UV irradiation with enzymatic hydrolysis to study the effects of UV irradiation on OP bioavailability in the WLFZ soil. The results of this study provide important information about the effects of UV irradiation on OP bioavailability in the WLFZ soil of the TGR.

Section snippets
Study area
As an important tributary of the Yangtze River, Pengxi River located in the middle of the TGR and has a WLFZ with a length of 67.33 km and a total area of 56.60 km2 (Zhang et al., 2012). This WLFZ area was exposed and used as cultivated land from April to September, and inundated from October to March in the subsequent year (Huang et al., 2019). The long-term agricultural management inevitably results in the enrichment of P in the soil, which may release to the water environment with surface.

The characteristics of WLFZ soil
The characteristics of WLFZ soil are shown in Table S3. The sampling site soils were purple except for those at sites S4 and S5. The TP and TIP contents ranged from 434.13–785.66 and 297.69–641.44 mg/g, respectively; their trends were similar, with maximum and minimum values appearing in S7 and S6, respectively. S7 is near a residential area, and WLFZ soil is easily affected by human factors, which may explain the high TP and TIP contents at S7.

Conclusions
The forms and bioavailability of OP in the WLFZ soil of the Pengxi River Basin of the TGR were studied. The OP contents in the WLFZ soil were ranked as NaOH-Po > NaHCO3-Po > H2O-Po, and those of EHP were ranked as NaOH-EHP > NaHCO3-EHP > H2O-EHP. The EHP in the WLFZ soil was dominated by labile monoester P, followed by diester P and phytate-like P. The bioavailability of OP in the WLFZ soil was high, which would lead to environmental risk of P in the TGR.

Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships 3PO that could have appeared to influence the work reported in this paper.

Acknowledgments
This study was financially supported by National Natural Science Foundation of China (41430750, 21976021, 41771520) and National Key Research and Development Program of China (2019YFD1100504).