The role of the 'Anthropogenic Nitrogen Pump' in coastal seas

Our research has shown that nitrogen-rich terrestrial pollutants through the atmosphere and rivers exacerbate the deficiency of phosphate in coastal seas, which stimulates the utilization of dissolved organic phosphorus by phytoplankton.
Published in Earth & Environment
The role of the 'Anthropogenic Nitrogen Pump' in coastal seas
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Phytoplankton play a significant role in biogeochemical cycles of the oceans because they are primary producers. To be able to grow, they require nutrients such as nitrate, phosphate, and some essential trace metals. However, if those inorganic nutrients are in short supply, many phytoplankton species can make use of their organic counterparts commonly referred to as dissolved organic nitrogen (DON) and phosphorus (DOP), for instance. Due to human activity, the coastal seas receive significant amounts of terrestrial pollutants through processes such as atmospheric deposition and river runoff. Those pollutants can contain high concentrations of inorganic nutrients such as nitrate (NO3-), which is used in fertilisers. Like crops on land, these nutrients will fertilise phytoplankton in coastal seas with consequences not only for coastal food webs but also associated biogeochemical cycles. How they impact the latter from the local to the global scale was the main question of our work recently published in Nat. Comms. (Jin et al., 2024).   

I, Haoyu Jin, was very fortunate to have had the opportunity to join the Marine Ecology and Environmental Science Laboratory at the Ocean University of China (OUC, Qingdao), where I began my Master's and PhD studies under the guidance of Professor Huiwang Gao. The laboratory has an Atmospheric Environment Monitoring Station at the coast which allowed us to monitor the atmospheric environment including the collection of particulate matter. There are also excellent onboard incubation systems (Fig. 1) available which were highly conducive for carrying out my research.

Fig. 1: Schematic of our onboard microcosms.

The growth of marine phytoplankton is primarily limited by nitrogen and iron (Moore et al., 2013). Terrestrial pollutants, usually characterized by high concentrations of inorganic nitrogen (e.g., NO3-) but relatively low concentrations of inorganic phosphorus (e.g., PO43-), can enter the ocean through atmospheric deposition and river runoff, alleviating nitrogen limitations and therefore acting as fertilizers for phytoplankton growth in coastal seas. Although the concentration of PO43- usually is relatively low in the global surface ocean, phytoplankton can utilize DOP through a ubiquitous enzyme called alkaline phosphatase, which therefore mitigates PO43- limitation. However, as the main source of P in coastal oceans is still considered to be PO43-, alkaline phosphatases are more important in the open ocean where concentrations of PO43- are lower. However, for alkaline phosphatases to be active, they require essential metals such as iron and zinc, which are also scarce in the open ocean compared to coastal seas. Atmospheric transport, though, can bring these essential metals over long distances and therefore help open ocean phytoplankton to make use of DOP.  Usually, in coastal seas, those essential trace metals are higher concentrated and therefore the role of atmospheric deposition and river runoff in terms of phosphorus acquisition likely is different. Hence, we focussed our work on addressing this knowledge gap.    

Preliminary studies from our group have found that atmospheric deposition in coastal seas can significantly stimulate phytoplankton growth even under conditions where concentrations of PO43- were insufficient to support phytoplankton growth, suggesting that atmospheric deposition likely stimulates the utilization of DOP by phytoplankton (Zhang et al., 2018; Chu et al., 2018). We had a careful look at the literature and found that terrestrial pollutants such as atmospheric aerosol and riverine water are usually characterized by high concentrations of inorganic nitrogen but low concentrations of PO43-. Thus, if there is strong pollution through the atmosphere or rivers, there is a continuous transport of nutrients with a high nitrogen-to-phosphorus ratio (N:P) into coastal seas leading to a shift from nitrogen to phosphorus limitation (Kim et al., 2011). Although significant research has been conducted on the impact of anthropogenic pollutants in marine ecosystems, it was not well known as to whether anthropogenic pollutants can stimulate the utilization of DOP and if so how.

We recognized the opportunity and started with on-board microcosm experiments through participating in the Shiptime Sharing Project (2018-2020) funded by the National Natural Science Foundation of China. With the assistance of our colleagues, we joint the RV “Dongfanghong 2”, RV “Beidou”, and RV “Lanhai 101” and conducted multiple onboard microcosm experiments in the China Coastal Seas. Despite encountering difficulties during preparation and fieldwork, we successfully finished the experiments, i.e., measured chlorophyll a and alkaline phosphatase activity onboard, and conducted nutrient measurements after the field campaigns (Fig. 2). I need to express my special thanks to Professor Huiwang Gao and Dr Chao Zhang who guided me in designing the experiments and many colleagues and friends (Jianhua Qi, Jinhui Shi, Yifan Lu, Wei Guo, Di Xue, Yang Guan,  Wenshuai Li, Dihui Chen, Xue Ding, Jiamin Xie, Shijie Jia, Yansong Zhang, Hongkun Wang, Renzheng Wang and many more) who helped me in the field but also with data analyses (Fig. 3). Their encouragement and support allowed me to persevere through this challenging time because I had never done work like this ever before.

Fig. 2: Sampling of microcosm experiments (left), and Chao Zhang measuring Chlorophyll a onboard (right).

Fig. 3: Group photos of participants of Shiptime Sharing Project on the RV "Dongfanghong 2" in 2018 (left) and the RV"Beidou" in 2019 (right).

Our results indicated that under the influence of industrial and agricultural activities through atmospheric deposition and river runoff, phytoplankton utilize more nitrogen and therefore exacerbate PO43- stress in coastal seas. To alleviate this stress, they activate alkaline phosphatases to utilize DOP in coastal seas. We coined the process encompassing the input of dissolved inorganic nitrogen in coastal seas by human activity and the subsequent response of phytoplankton the "Anthropogenic Nitrogen Pump" (Fig. 4). The pump was therefore identified to make DOP an important source of phosphorus for phytoplankton growth in coastal seas. By extending our study to the global ocean, we found evidence that the "Anthropogenic Nitrogen Pump" is active in many coastal areas and therefore might contribute to the phosphorus cycle in coastal seas worldwide.

Fig. 4: Conceptual diagram of the 'Anthropogenic Nitrogen Pump'.

Although a first draft of the manuscript was available in 2021 under the guidance of Huiwang Gao and Chao Zhang, I encountered challenges with some data analyses and the process of writing up my work in English. Luckily, in 2022, I received a scholarship from the Chinese Scholarship Council (CSC) to join to the group of Prof. Thomas Mock at the University of East Anglia (UEA) in the UK. The time in his group helped me to address challenges I had faced with my data analyses, and of course being in England improved my English. Before we submitted our work, I presented my data at the joint symposium between UEA and OUC held in Norwich in October 2023 (Fig. 5). 

Fig. 5: Group photo of participants at the University of East Anglia and Ocean University of China Symposium in 2023 (left), and Haoyu Jin presenting results at this meeting (right).

With great feedback from colleagues after the meeting, we submitted our work and finally published our paper, which is also my first paper published as a first author. The six years of hard work across two different countries and many challenges finally paid off. It required funding from different sources including my followship as well as the enthusiasm, support, patience, and perseverance of my co-authors and my family to make all this possible. This is an important milestone and a new starting point in my scientific career.

 

References:

Chu, Q., Liu, Y., Shi, J., Zhang, C., Gong, X., Yao, X., ... & Gao, H. (2018). Promotion effect of Asian  dust on phytoplankton growth and potential dissolved organic phosphorus utilization in the South China Sea. Journal of Geophysical Research: Biogeosciences123(3), 1101-1116.

Kim, T. W., Lee, K., Najjar, R. G., Jeong, H. D., & Jeong, H. J. (2011). Increasing N abundance in the northwestern Pacific Ocean due to atmospheric nitrogen deposition. Science334(6055), 505-509.

Moore, C. M., Mills, M. M., Arrigo, K. R., Berman-Frank, I., Bopp, L., Boyd, P. W., ... & Ulloa, O. (2013). Processes and patterns of oceanic nutrient limitation. Nature geoscience6(9), 701-710.

Zhang, C., Gao, H., Yao, X., Shi, Z., Shi, J., Yu, Y., ... & Guo, X. (2018). Phytoplankton growth response to Asian dust addition in the northwest Pacific Ocean versus the Yellow Sea. Biogeosciences15(3), 749-765.

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