Uncovering nitrogen pollution sources and transformations with associated impacts on the sediment microbiome and ecosystem multifunctionality

Abstract

Today humans exploit nearly 50% of the Earth’s land surface with approximately half the world’s population living exclusively in coastal areas. Anthropogenic activities such as agriculture, and wastewater discharge, release numerous undesirable, nutrient-rich effluents into the coastal ocean. Although nutrients are essential, when in excess, accelerate microbial growth and associated aerobic respiration, thereby depleting oxygen concentrations. This has detrimental cascading effects on an ecosystem by fueling harmful algal blooms, pathogens and other disease vectors. Globally, coastal marine environments face tremendous pressure from urbanization, and eutrophication caused by excess nutrient inputs from wastewater discharge. Hong Kong’s marine environment is no exception and faces a long-standing eutrophication problem. Today we see a punctuated gradient of total inorganic nitrogen concentrations with more densely populated areas corresponding to higher concentrations. Yet, despite significant scientific efforts from local authorities to improve marine coastal ecosystem health, sources of nitrogen that contribute to these elevated concentrations and their associated impacts remain unknown. I utilized a dynamic approach combining nutrient chemistry and stable isotope analysis on seawater and wastewater effluents, bacterial metagenomics on marine sediments and simple cost-effective functional assays to test the following hypotheses: (a) Wastewater is the major source of nitrogen pollution in the region (b) Denitrification is the dominant source of biological nitrogen transformation (c) marine sediments in sites with high nitrogen pollution have low carbon capacity and (d) nitrogen concentrations influence ecosystem function .

To test the hypothesis that wastewater is the major source of nitrogen pollution, in Chapter 1, I conducted stable isotope analysis of wastewater effluents collected from 18 sewage treatment facilities representing 5 treatment technologies. The analysis revealed mean stable isotope values of nitrate and nitrite (δ15NNO3+NO2; 12‰) that were significantly higher than natural values (marine nitrate ~4‰) and showed no variation with treatment type. Seawater samples collected from four sites along a water quality gradient in northeast Hong Kong recorded δ15NNO3+NO2 signatures (~11‰) that closely resembled that of wastewater effluents.

To analyze the dominant sources and transformations of nitrogen in the marine environment, in Chapter 2, I measured nutrient concentrations, and conducted dual nitrate isotope analysis (δ15NNO3- and δ18ONO3-) on seawater samples collected from 76 locations along a salinity gradient from the west to the east. The analysis revealed that (1) primary sources of nitrate were wastewater effluents and groundwater discharge and (2) putative drivers of biological nitrate transformation were assimilation, nitrification and nitrogen fixation.

In Chapter 3, I conducted high-throughput sequencing on the taxonomic and functional diversity of bacterial and archaeal communities in sediments from four sites along a pollution gradient in northeast Hong Kong. This revealed (1) strong correlations with tea bag decomposition rates and (2) that eutrophic sediments have the poorest carbon storage capacity when compared to disturbed peat, mangroves, grasslands, deserts and forests.

In the fourth chapter, primary productivity, grazing intensity, predation intensity and organic matter decomposition were characterized to understand the link between nutrient enrichment and ecosystem function. Strikingly, the most polluted site recorded the lowest primary productivity, lowest predation intensity, highest rate of decomposition and lowest carbon sequestration capacity. Overall ecosystem multifunctionality also varied significantly with nutrient pollution.

Taken together, these chapters integrate standardized physical and biological observations and bioinformatics to take the vital signs of urbanization impacts on coastal ocean life. Moreover, these data make important connections between eutrophication and coastal ocean carbon storage, opening a black box for future carbon accounting in global ocean systems.