Group post: Effects of photoperiod length upon the ecophysiology of Crocosphaera watsonii

Diazotrophic phytoplankton are important contributors to the primary productivity of the world’s oceans facilitating the carbon pump and carbon sequestration in often oligotrophic regions, with an estimated global input of 100-200 Tg^-1 N y^-1. Eukaryotes such as Trichodesmium and Richelia had been previously thought as the primary open ocean N₂ fixers. However, unicellular UCYN cyanobacteria are now thought to account for ~10 % of nitrogen production in the world’s oceans.

Eco-physiology and growth dynamics of the recently characterised pelagic UCYN cyanobacteria is poorly understood with efforts focusing on temperature and nutrient concentrations found to exhibit control through enzyme kinetics and niche structure respectively. Dron et al., 2013 investigated the effect of photoperiod length (PPL) upon the carbon/nitrogen metabolism and cell cycle of the best studied culturable UCYN-B cyanobacterium Crocosphaera watsonii. It has been previously shown that 50% of C. watsonii genes exhibit a diel expression pattern. However the driver of the observed diel variation is not clear. Are cellular processes timed upon a circadian clock, or under direct control by PPL?

Continuous culture technique was employed to maintain duplicate cultures of W8501 C. watsonii in the exponential growth phase. Culture 1 was maintained under a short photoperiod (8 hr light:16 hr dark), while culture 2 was maintained under a long photoperiod (16 hr light: 8 hr dark). Irradiance followed a natural sinusoidal pattern with a maximum flux of 130 µmol quanta m^-2 s^-1 at the mid-light point. Nitrate and nitrite culture concentrations were measured every 8 hours, whilst population density and growth rates quantified every 24 hours. Nitrogen and carbon cell contents were estimated every 4 hours. DNA topology and compaction was investigated by staining DNA with Sybr-Green and quantifying the fluorescence.

Population growth (cell division) was higher for the long PPL, peaking daily at  ~10x10⁶ cells ml^-1 compared to ~6x10⁶ cells ml^-1 for the short photoperiod. Indeed cell division was so much slower for the short PPL that the dilution rate for the continuous culture had to be reduced to 0.15 day^-1 compared to 0.2 day^-1 for the long PPL.

Cell division occurred consistently in the mid-light phase for all PPLs demonstrating that C. watsonii has the ability to change the cell cycle timing to match PPL. Since N₂ fixation must occur in the dark phase it is ecologically advantageous for cell division to occur in the light-phase.

A conserved 5-6 hour time lag between the end of cell division and the onset of nitrogenase activity was identified. Most likely this time window is required to assemble and activate the enzymatic machinery for N₂ fixation, which must be separated from photosynthesis. DNA synthesis occurred in the dark phase, concomitantly with the highest rates of N₂ fixation in all three PPLs. This synchrony allows the most nitrogen to be available for DNA synthesis.

Interestingly this study identified that for C. watsonii a longer photoperiod didn’t correlate with higher carbon and nitrogen storage. Fixation and assimilation of both carbon and nitrogen was significantly lower for both the normal and long PPL compared to the short PPL. Higher carbon content at the end of the light phase may provide more energy for N₂ fixation, while higher levels of nitrogen fixation may help increase carbon fixation, both processes augmenting the other.

C. watsonii exhibited markedly different cellular energy allocation under contrasting light regimes. The physiological responses were similar under balanced and long PPLs in that rapid cell division was favoured over somatic growth (i.e. C/N storage). Conversely, under the short PPL, cell division was almost half that of the long PPL whilst favouring C/N storage and somatic growth. It is possible that this plastic response is an adaptation to changing environmental conditions, perhaps seasonal changes. The range of C. watsonii extends ~40 °N and 30 °S, with marked seasonal variability in PPL. When conditions are unfavourable, somatic growth may be favoured to increase cell stores facilitating population survival during the winter, whilst in summer when the photoperiod is long, high cell division is favoured and the population blooms. This study identified that as much as 80 % of nitrogen fixed by C. watsonii is lost to the ambient water. The reason behind this wastefulness is unknown, but is undoubtedly a vital nitrogen input into often nitrogen limited ocean waters.

This paper was a useful contribution to the study of C. watsonii and the significance of photoperiod length upon their ecophysiology. However, just a single strain of C. watsonii was investigated and it would be informative to know if different ecotypes exist within distinct water bodies. For example, would a warm water equatorial strain lack the adaptability of its poleward brothers in preference to faster proliferation rates? Given the possibility of intraspecies variability within bacteria, it would be wise to express caution when inferring the results from this study upon other species as well.

Matthew Zietz, Freya Radford, and Jack Jones

Primary reference:

Dron, A., Rabouille, S., Claquin, P., Talec, A., Raimbault, V., & Sciandra, A. (2013). Photoperiod length paces the temporal orchestration of cell cycle and carbon‐nitrogen metabolism in Crocosphaera watsonii. Environmental microbiology, 15(12), 3292-3304.