Why Is Planktonic Nitrogen Fixation So Rare in Coastal Marine Ecosystems? Insights from a Cross-Systems Approach

Abstract

The process of di-nitrogen (N₂) fixation is widespread in nature, including in many aquatic ecosystems. In lakes, N₂ fixation by planktonic cyanobacteria often contributes sufficient new nitrogen to maintain phosphorus limitation of primary production. However, it is intriguing that many estuaries and coastal marine ecosystems at salinities greater than 10 ppt are moderately to strongly N-limited despite high nutrient loading, and planktonic N₂ fixation is rarely if ever an important process. Here, we review our collaborative research on mechanisms of control of planktonic N₂ fixation in lakes and estuaries, using cross-systems and cross-scale comparative approaches. We conclude that a slower gross growth rate of planktonic cyanobacteria in seawater, coupled with a disproportionate sensitivity of heterocystous species to grazing by zooplankton, can severely constrain bloom development and so N₂ fixation in estuaries under N-depleted conditions. A slower growth rate in saline vs. freshwaters is in part a consequence of an inhibition of molybdenum uptake by sulfate; the latter is present in much higher concentrations in seawater. Molybdenum is required for N₂ fixation using the conventional form of the nitrogenase enzyme. In the chain-forming cyanobacteria that commonly form large blooms under N-depleted conditions in lakes, N₂ fixation occurs in heterocysts, which do not produce oxygen from photosynthesis. As such, energy for the N₂ fixation process must be supplied by the photosynthetic, vegetative cells. Clipping of filaments by grazing reduces the number of heterocysts that can be supported, and so further limits N₂ fixation and population growth when exogenous N is in low supply.

Roxanne Marino and Robert W. Howarth

We met in 1980 when Roxanne, newly out of college with a BS in chemistry, interviewed for a job at the MBL Ecosystems Center in Woods Hole with Bob, who was supervising his first research project after earning his PhD in the MIT/WHOI Joint Program in Oceanography. Except for a brief period when Roxanne studied at the University of Washington, we have worked together ever since. We spent many hours bonding over radioactive, sulfurous mud before moving on in 1985 to our current biogeochemical cycling study element of choice, nitrogen, still priding ourselves on being two of only a handful of ecosystem researchers who were interested in, let alone could spell, molybdenum. We enjoyed the opportunity to work at the Cary Institute of Ecosystem Studies for several months before moving to Cornell in 1985, continuing all along to enrich our shared interests in comparative ecosystems ecology and biogeochemistry. We were married in 1987 on our farm outside Trumansburg, NY. Our daughter Marina was born in 1996 and is now studying environmental science and engineering at Smith College. In 2001, Roxanne earned her Ph.D. at Cornell in the employee degree program, with Gene Likens. We have worked on a variety of other research topics beyond those described in this paper and also share a passion for applying science to environmental policy and management, and for community service. Roxanne served on the Ulysses Town Board for several years, including as Town Supervisor. Bob was the founding Editor-in-Chief of Biogeochemistry for 21 years, the President of the Coastal & Estuarine Research Federation from 2007 to 2009, and currently serves as Editor-in-Chief of Limnology and Oceanography.