Evidence for coupled iron and nitrate reduction in the surface waters of Jiaozhou Bay

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Abstract

Iron and nitrate (NO3) are dominant physiologically required nutrients for phytoplankton growth, and iron may also play a key role in the marine nitrogen cycle. In this study, we investigated the temporal and spatial distributions of dissolved iron (DFe) and Fe(II) in the surface waters of Jiaozhou Bay (JZB) from April 2 to July 26, 2017. High concentrations of DFe and Fe(II) predominantly occurred in nearshore and estuarine stations and concentrations were generally higher in April and May. The highest DFe concentration was observed along the coast of Hongdao (51.55 nmol/L) in May, while the lowest concentration was observed in the western coastal region (2.88 nmol/L) in April. The highest and lowest Fe(II) concentrations were observed in the Licun estuary (22.42 nmol/L) and outer bay (0.50 nmol/L) in May, respectively. We calculated the proportions of nitrate, nitrite, and ammonium in dissolved inorganic nitrogen (DIN) as well as the ratio of Fe(II) to DFe in all four months. The mean Fe(II)/DFe ratio was 0.48 in April, 0.43 in May, 0.69 in June, and 0.32 in July. The mean ratio of NO3 to DIN was 0.78 in April, 0.54 in May, 0.20 in June, and 0.62 in July. NO3/DIN continuously decreased in the first three months, while Fe(II)/DFe remained high, which suggests that the reduction of iron and nitrate occurred simultaneously in the surface waters of JZB.

Introduction

Iron plays an important role in marine biology and primary productivity as well as in the global carbon and nitrogen cycles (Tagliabue et al., 2017). Compared with macronutrients, for example, phosphorus and nitrogen, iron is insufficiently supplied to the oceans and is therefore a dominant limiter for primary production (Tagliabue et al., 2017). Fe(III) is typically insoluble in seawater due to its stable thermodynamic state, while Fe(II) is highly soluble and rapidly oxidizes to Fe(III) in oxidative environments (Rose and Waite, 2002).

Fe(II) is an important iron species in surface seawater due to natural influence as well as some anthropic factor (Öztürk et al., 2003). Photochemical reactions are considered to be the main source of Fe(II) in surface waters (Roy et al., 2008). In the Gulf of Aqaba in the Red Sea, the distinct seasonal pattern in Fe(II) concentrations corresponds to changes in solar irradiance, and the surface Fe(II) concentrations show significant diurnal variability (Shaked, 2008). Fe(II) concentrations were also found to decrease with depth (Shaked, 2008), indicating the dominant effect of sunlight-induced photochemical reduction on Fe(II) formation. In coastal waters, the content and distribution of Fe(II) are often influenced by human activities (Öztürk et al., 2003). Terrestrial sources, such as groundwater, rivers, atmospheric wet deposition, industrial discharge, and releases from the continental shelf, can increase Fe(II) concentrations by up to several tens of times that of open waters (Hong and Kester, 1986). Meanwhile, the eutrophication of coastal waters caused by human activities leads to the bloom of phytoplankton and eukaryotic phytoplankton have the ability to reduce Fe (III) to Fe(II) as a way to obtain iron (Maldonado and Price, 2001).

The other way that may influence the path of Fe(III) reduction is the activities of microorganism in low oxygen seawater. It was found that in anoxic environments microbial reduction is an important regeneration pathway for Fe(II) (Weber et al., 2006). Microorganisms that reduce Fe(III) are mostly anaerobic or facultative anaerobic, and have been isolated from various habitats such as soil, river sediment, estuarine sediment, and groundwater (Weber et al., 2006). Furthermore, some microorganisms have the ability to simultaneously reduce iron and nitrate via denitrification or dissimilatory nitrate reduction to ammonium (DNRA) (Farrenkopf et al., 1997). A previous analysis showed that the growth of Shewanella putrefaciens resulted in the simultaneous nitrogen oxide reduction and Fe(III) reduction (DiChristina, 1992). However, few field studies to date have linked the concentration of Fe(II) in seawater to nitrate reduction. Maximum Fe(II) values were found to coincide with maximum secondary nitrite values in the OMZ of the Arabian Sea (Kondo and Moffett, 2013) and nearby Persian Gulf (Moffett et al., 2007), contributing up to 50% of the dissolved iron (DFe) in the large area with high nitrite in the Arabian Sea.

Jiaozhou Bay (JZB) is a semi-enclosed bay on China's coastline. It is surrounded by the regions of Jiaozhou City, Huangdao Island, and the highly industrialized and populated Qingdao City. JZB has a surface area of 390 km2 and an average water depth of 7 m, which gradually deepens from the northwest to the southeast (Su et al., 2016). Water exchange between JZB and the Yellow Sea occurs through a 3.1 km wide channel in the southeastern bay region. The bay is, therefore, more affected by terrestrial processes as opposed to marine-based processes due to its weak water exchange capacity. In recent decades, the multi-functional bay has increasingly integrated aquaculture and port activities, as well as tourism. The nutrient structure and phytoplankton composition in JZB are, therefore, constantly changing in response to increasing coastal anthropogenic perturbations (Yuan et al., 2016). Numerous rivers surrounding the JZB, such as the Yang, Dagu, Moshui, Haibo, Loushan, Baisha, and Licun rivers, are the primary channels of discharging municipal wastewater to the bay (Su et al., 2016). Harmful algal blooms have occurred every summer since the 1990s in response to severe eutrophication in the bay. Before 2007, JZB was frequently affected by red tides caused by the large-scale bloom of Skeletonema costatum or diatoms (Yuan et al., 2016). In 2008, the outbreak of Enteromorpha during the sailing competition of the 29th Olympic Games affected the normal progress of the Games (Yuan et al., 2016). Green tides occur almost every summer in JZB and the Yellow Sea, threatening the livelihoods of coastal residents (Qi et al., 2016). It is, therefore, crucial to understand the distribution and activity of nutrient elements affecting marine phytoplankton growth, such as N, P, Si, and Fe. Although previous studies have assessed the distribution and speciation of DFe and nutrients in JZB (Ke et al., 2020; Su et al., 2016), the distribution of Fe(II), which is more available to marine phytoplankton, has not yet been reported. This study aims to explore the factors affecting the transformation and distribution of iron, as well as the coupling of nitrogen cycling and iron redox in the JZB.

Section snippets

Sample collection

Seawater was collected monthly from April 2 to July 26, 2017, during four cruises in the JZB. The sampling stations were located between 120.15–120.35°E and 36.01–36.19°N (Fig. 1).

Surface seawater samples (~2 m) were collected off a wooden skiff using acid-cleaned Teflon-coated 5 L Niskin bottles with a plastic rope. The seawater from the Niskin bottles was immediately subsampled under gravity pressure. The seawater was carefully transferred to 125 mL brown glass bottles for oxygen analysis

Distribution of DFe in JZB

The horizontal distributions of DFe in the surface waters of the JZB from the four cruises are shown in Fig. 3. The DFe concentrations showed high variability throughout the sampling period, ranging from 2.88 to 51.55 nmol/L. Lower concentrations and lower spatial variability were observed in June (Fig. 3c), while higher concentrations and larger spatial variability were observed in April (Fig 3a) and May (Fig. 3b). Higher concentrations of DFe in all four cruises were observed at the nearshore

Factors affecting DFe distribution in JZB surface waters

Marine ecosystems in semi-enclosed bays, such as JZB, are vulnerable and sensitive to anthropogenic activity. Bay coastal zones are affected by land-based pollutants (Yuan et al., 2016), resulting in the uneven horizontal distribution of water components. In this study, high DFe values were mainly observed near the shore, indicating the high impacts of human activity on the coastal ecology of the JZB (Xu et al., 2017). The bay is surrounded by highly industrialized and densely populated areas,

Conclusion

The DFe and Fe(II) concentrations in JZB surface waters were analyzed across four months. In all four cruises, high DFe and Fe(II) concentrations mainly occurred at the nearshore and estuarine stations, indicating the high influence of anthropogenic activities on JZB surface waters. The anthropogenic influence on JZB water quality was greater in spring than in summer, because JZB was mostly influenced by riverine discharge, rainfall, and phytoplankton growth during the summer rainy season.

The

Acknowledgement

This work was supported by the National Natural Science Foundation of China (No. 41876079) and the Open Fund of Key Laboratory of Science and Engineering for Marine Ecology and Environment of State Oceanic Administration (No. MESE-2018-05).

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