Electron & Biomass Dynamics of Cyanothece Under Interacting Nitrogen & Carbon Limitations.

Sophie Rabouille,Lubos Polerecky,Gábor Bernát,Jan Červený,Meri Eichner,Martin Lukeš,Susanne Stephan,José Bonomi-Barufi,Jacco C Kromkamp,Takako Masuda,Eva Kotabová,Douglas A Campbell,Ondřej Prášil,Mario Giordano,Tomáš Zavřel,David J Suggett,Pascal Claquin,Kimberly Halsey,Ana Teresa Lombardi

doi:10.3389/fmicb.2021.617802

Abstract

Marine diazotrophs are a diverse group with key roles in biogeochemical fluxes linked to primary productivity. The unicellular, diazotrophic cyanobacterium Cyanothece is widely found in coastal, subtropical oceans. We analyze the consequences of diazotrophy on growth efficiency, compared to NO3–-supported growth in Cyanothece, to understand how cells cope with N2-fixation when they also have to face carbon limitation, which may transiently affect populations in coastal environments or during blooms of phytoplankton communities. When grown in obligate diazotrophy, cells face the double burden of a more ATP-demanding N-acquisition mode and additional metabolic losses imposed by the transient storage of reducing potential as carbohydrate, compared to a hypothetical N2 assimilation directly driven by photosynthetic electron transport. Further, this energetic burden imposed by N2-fixation could not be alleviated, despite the high irradiance level within the cultures, because photosynthesis was limited by the availability of dissolved inorganic carbon (DIC), and possibly by a constrained capacity for carbon storage. DIC limitation exacerbates the costs on growth imposed by nitrogen fixation. Therefore, the competitive efficiency of diazotrophs could be hindered in areas with insufficient renewal of dissolved gases and/or with intense phytoplankton biomass that both decrease available light energy and draw the DIC level down.

Highlights

While the structures and genetic regulation of the key enzymes of photosynthesis and nitrogen (N2) fixation are relatively well understood, we lack understanding of how these two processes interact, in particular under fluctuating environmental conditions
In an ocean acidification scenario with elevated pCO2 and dissolved inorganic carbon (DIC) levels (380 vs. 980 μatm pCO2, 1970 vs. 2150 μmol kg−1 DIC), increased particulate organic carbon (POC) and nitrogen (PON) production rates in Cyanothece were attributed to lowered energy costs for the concentrating mechanism (CCM) (Eichner et al, 2014)
Crocosphaera grown diazotrophically under low pCO2 treatment (180 ppm) shows a lowered growth rate compared to a high pCO2 (800 ppm), which was attributed to an ATP deficit due to the extra energy invested in the CCM (Garcia et al, 2013)

Summary

Introduction

While the structures and genetic regulation of the key enzymes of photosynthesis and nitrogen (N2) fixation are relatively well understood, we lack understanding of how these two processes interact, in particular under fluctuating environmental conditions. Autotrophic, unicellular cyanobacterial diazotrophs within the known groups B and C (UCYN-B, C; Zehr et al, 2001; Taniuchi et al, 2012) overcome nitrogenase inhibition by O2 through temporal separation of day-time photosynthesis from N2-fixation (Fay, 1992; Gallon, 1992; Bergman et al, 1997) fueled by night-time respiration of carbon reserves accumulated during previous day-time photosynthesis Despite this temporal offset, the yield of N2-fixation remains tightly dependent upon the efficiency of photosynthesis (Agawin et al, 2007; Großkopf and LaRoche, 2012; Grimaud et al, 2014). It is still unclear how reductant and energy demands are affected by the source of nitrogen and how much more costly it really is, for a diazotroph to grow on N2 vs NO3−

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