Forming the primary nitrite maximum: Nitrifiers or phytoplankton?

As intermediary in a number of key biological processes, the dynamics of oceanic NO 2 concentrations have historically been used as an indicator of the balance between oxidative and reductive pathways in the marine nitrogen cycle. As appreciation of the role of NO 2 in the marine nitrogen cycle grew through the 1960s and 1970s, and data sets from different ocean basins became available, a common feature was observed in stratified water columns: a peak in NO 2 concentrations at the base of the euphotic zone, with near zero concentrations both shallower and deeper. These concentrations are significant; they commonly range between 10 and 400 nmol L21 but as high as 4,500 nmol L21. This peak in NO 2 concentration is termed the primary nitrite maximum (PNM). Since the 1960s, the mechanisms sustaining the ubiquitous PNM have remained uncertain, with available data supporting either bacterial nitrification or NO 2 release by phytoplankton. Simple box models have reproduced the PNM feature with nitrification as the source of NO 2 , whereas others have succeeded solely with phytoplankton. Conclusive identification of the mechanism(s) maintaining the PNM in the world’s oceans has yet to be achieved, but the preponderance of data supports phytoplankton excretion, with nitrification likely playing only a supporting role. Furthermore, there are a number of potentially important inconsistencies in the role of nitrification between culture studies and field observations. Biological–physical interactions are likely also important in controlling PNM formation and maintenance. Nitrite (NO 2 ) is a dynamic component of the marine nitrogen cycle that is produced and consumed by a variety of processes. These processes are both reductive and oxidative and therefore are critical in a proper interpretation of ocean nitrogen cycling. Production of NO 2 in the aerobic water column can occur via the following pathways: (1) chemoautotrophic oxidation of ammonium (NH 4 ) by ammonium oxidizing microbes, including both bacteria and archaea (Brandhorst 1959; Olson 1981b; Francis et al. 2005); (2) light-limited, incomplete assimilatory reduction of nitrate (NO 3 ) by phytoplankton (Vaccaro and Ryther 1960; Kiefer et al. 1976; Collos 1998), bacteria (Wada and Hattori 1971), and potentially archaea; and (3) photolytic reduction of NO 3 (Zafiriou and True 1979). Rapid attenuation of the high-energy, short wavelengths of light in the upper euphotic zone severely limits the importance of the latter process at the depths of the primary nitrite maximum (PNM), but it may be important during periods of convective mixing in some regions where elevated NO 2 concentrations are found throughout the euphotic zone (Lipschultz et al. 1996; AlQutob et al. 2002). Anaerobic processes, such as dissimilatory reduction of NO 3 by denitrifying bacteria or the recently discovered anaerobic ammonium oxidation (anammox) pathway (Kuypers et al. 2003), likely make minimal contributions to NO 2 concentrations (e.g., anaerobic microzones in marine snow particles) in the euphotic zones of open-ocean gyres. Oxidation of NH 4 to NO 2 2 provides energy for growth in ammonium-oxidizing organisms. Although very little is currently known about the physiological capacity of ammonium-oxidizing archaea, some Crenarcheota have recently been shown to have the capacity for ammonium oxidation (Francis et al. 2005; Konneke et al. 2005), and Murray et al. (1999) have noted temporal correlation between crenarchaeal abundance and NO 2 concentrations in the Santa Barbara Channel. This recent discovery raises the central issue of the relative role of ammonium-oxidizing bacteria (AOB) versus other ammonium-oxidizing organisms (AOO) in nitrification and hence the degree to which culture knowledge applies to the ocean. For clarity we make several distinctions in terminology with respect to AOO. In the past, ammonium oxidation was believed to be carried out solely by bacteria and thus the term AOB was used in field studies as well as in culture studies. In this review, we use the term AOB only when referring to culture work (where the organisms are known), and use the term AOO when referring to field data that generally are an unknown mix of bacterial and archaeal nitrifiers. Acknowledgments We thank all the BATS PIs and technicians past and present whose diligence and dedication has generated the data that are discussed in this manuscript. We thank Karen Casiotti and the anonymous reviewers whose comments have improved this manuscript. This research was supported by the NSF JGOFS Program, and Chemical and Biological Oceanography Programs through awards OCE-8801089, -9301950, -9617795, and -0326885. Additional support for M.W.L. was provided by NSF Chemical Oceanography Program through award OCE-0241662. This is Bermuda Biological Station Contribution 1669.