Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions

Anthropogenic activities are altering total nutrient loads to many estuaries and freshwaters, resulting in high loads not only of total nitrogen (N), but in some cases, of chemically reduced forms, notably NH4 . Long thought to be the preferred form of N for phytoplankton uptake, NH4 may actually suppress overall growth when concentrations are sufficiently high. NH4 has been well known to be inhibitory or repressive for NO3 uptake and assimilation, but the concentrations of NH 1 4 that promote vs. repress NO 3 uptake, assimilation, and growth in different phytoplankton groups and under different growth conditions are not well understood. Here, we review N metabolism first in a “generic” eukaryotic cell, and the contrasting metabolic pathways and regulation of NH4 and NO 2 3 when these substrates are provided individually under equivalent growth conditions. Then the metabolic interactions of these substrates are described when both are provided together, emphasizing the cellular challenge of balancing nutrient acquisition with photosynthetic energy balance in dynamic environments. Conditions under which dissipatory pathways such as dissimilatory NO3 / NO2 reduction to NH 1 4 and photorespiration that may lead to growth suppression are highlighted. While more is known about diatoms, taxon-specific differences in NH4 and NO 2 3 metabolism that may contribute to changes in phytoplankton community composition when the composition of the N pool changes are presented. These relationships have important implications for harmful algal blooms, development of nutrient criteria for management, and modeling of nutrient uptake by phytoplankton, particularly in conditions where eutrophication is increasing and the redox state of N loads is changing. Increasing nutrient loads are among the most significant drivers of our “ever changing world” and their adverse effects on aquatic biodiversity and ecosystem health, including eutrophication, are well documented (Cloern 2001; Anderson et al. 2002; Howarth et al. 2002; Heisler et al. 2008; Glibert et al. 2014a). Emphasis has been placed on resolving whether systems are “limited” by nitrogen (N), phosphorus (P), or both (e.g., Howarth and Paerl 2008; Schindler and Hecky 2008; Schindler et al. 2008; see Table 1 for a list of abbreviations), to inform management and support recommendations for nutrient (N or P) control and to reduce eutrophication impacts. In contrast, there has been little research and discussion on whether nutrients at non-limiting concentrations influence primary producers differentially and how these metabolic responses may vary with different chemical forms of N. Given the global patterns of greater N than P fertilizer use, the overall increasing trend is for N to be the nutrient in excess relative to P and relative to phytoplankton stoichiometric needs (e.g., Childers et al. 2011; Glibert et al. 2013, 2014a). *Correspondence: [email protected] This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 1 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 00, 2015, 00–00 VC 2015 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10203 Anthropogenic activities are altering both total nutrient loads, and they are changing the dominant form of N nutrient delivered to many coastal marine and freshwater systems. While the major oxidized form of N, nitrate (NO3 ), is the dominant N form contributing to eutrophication in many aquatic ecosystems, there are several reasons why high loads of chemically reduced forms of N, such as ammonium (NH4 ), urea, and dissolved organic nitrogen (DON) are on the increase. In the U.S., many regions converted from primary to secondary sewage treatment in the late 1970s to mid-1980s after the passage of the Federal Water Pollution Control Act (later renamed as the Clean Water Act). As a result, many large wastewater treatment plants were constructed that discharge large quantities of N as NH4 (NRC 2000). Also, global fertilizer use has generally shifted from oxidized to reduced forms of N, with urea use now>50% of global N fertilizer, surpassing NO3 as the most common N fertilizer worldwide (Glibert et al. 2006, 2014a). The development of industrialized animal agriculture in coastal areas has also resulted in significant sustained increases in NH4 availability both via direct runoff and atmospheric deposition (Burkholder et al. 2006). Aquaculture operations are a rapidly increasing source of NH4 and urea, especially fish cage aquaculture in coastal lagoons, quiet embayments and in inland waters, due to direct excretion and decomposition of undigested feed (Bouwman et al. 2013). Coastal and estuarine waters are not the only systems experiencing increases in NH4 , however. Increases in atmospheric deposition of NH 1 4 have also been significant in many nearshore and offshore waters (Aneja et al. 2003; Duce et al. 2008). It has also been predicted, and shown, that with increasing ocean acidification and climate change, NH4 oxidation may be inhibited and stratification may increase, with resulting reduction in the injection of NO3 into surface waters, together leading to Table 1. Abbreviations used although this article. AMT Ammonium transporter