Can Top-Down Controls Expand the Ecological Niche of Marine N2 Fixers?

Markus Schartau,Markus Pahlow,Wolfgang Koeve,Angela Landolfi,Andreas Oschlies,Chia-Te Chien,Christopher J. Somes,A. E. Friederike Prowe

doi:10.3389/fmicb.2021.690200

Abstract

The ability of marine diazotrophs to fix dinitrogen gas (N2) is one of the most influential yet enigmatic processes in the ocean. With their activity diazotrophs support biological production by fixing about 100–200 Tg N/year and turning otherwise unavailable dinitrogen into bioavailable nitrogen (N), an essential limiting nutrient. Despite their important role, the factors that control the distribution of diazotrophs and their ability to fix N2 are not fully elucidated. We discuss insights that can be gained from the emerging picture of a wide geographical distribution of marine diazotrophs and provide a critical assessment of environmental (bottom-up) versus trophic (top-down) controls. We expand a simplified theoretical framework to understand how top-down control affects competition for resources that determine ecological niches. Selective mortality, mediated by grazing or viral-lysis, on non-fixing phytoplankton is identified as a critical process that can broaden the ability of diazotrophs to compete for resources in top-down controlled systems and explain an expanded ecological niche for diazotrophs. Our simplified analysis predicts a larger importance of top-down control on competition patterns as resource levels increase. As grazing controls the faster growing phytoplankton, coexistence of the slower growing diazotrophs can be established. However, these predictions require corroboration by experimental and field data, together with the identification of specific traits of organisms and associated trade-offs related to selective top-down control. Elucidation of these factors could greatly improve our predictive capability for patterns and rates of marine N2 fixation. The susceptibility of this key biogeochemical process to future changes may not only be determined by changes in environmental conditions but also via changes in the ecological interactions.

Highlights

Biological N2 fixation has evolved early in Earth’s history (Falkowski, 1997), when the ocean was void of oxygen (O2) and fixed N but rich in dissolved iron (Fe2+)
The ability to fix N2 is associated with additional energetic costs that are generally understood to yield lower growth rates of N2 fixing phytoplankton as compared to their non-N2 fixing phytoplankton competitors
resource competition theory (RCT) considers the simplest case of similar mortality terms for all phytoplankton types, assuming constant specific mortality m and negligible effects of grazing

Summary

INTRODUCTION

Biological N2 fixation has evolved early in Earth’s history (Falkowski, 1997), when the ocean was void of oxygen (O2) and fixed N but rich in dissolved iron (Fe2+). RCT considers the simplest case of similar mortality terms for all phytoplankton types, assuming constant specific mortality m and negligible effects of grazing (gZ = 0; Tilman, 1980) Under these simplified assumptions, the phytoplankton with the largest maximal growth rate (μmax; or lowest nutrient half saturation constant k) will have the lowest resource requirement R∗ at equilibrium (Figure 1D, dashed blue line), and will be the superior competitor, outcompeting the slower-growing competitor (Figures 1D,E, dashed red line; Tilman, 1980). In the specific case of autotrophic diazotrophs (D) competing with faster-growing non-fixing phytoplankton (Phy), we extend the traditional bottom-up paradigm within the RCT graphical framework (Figure 1A) to include selective grazing on Phy (Figures 1B,C) This effectively expands the diazotrophs’ region of co-existence by increasing the minimum nutrient requirements, Neq and Peq, of Phy (Figures 1B,C).

DATA AVAILABILITY STATEMENT

Findings

CONCLUSION AND FUTURE PERSPECTIVES