About sulfur

Sulfur is a fundamental element for all living organisms, as well as for the phytoplankton, as it is a constituent of many of the biological molecules they need. In the latter, it is acquired from the external environment as sulphate and internalized in the cell, in which it is activated with the consumption of ATP and it is reduced two times with the production of sulphide, useful for the biosynthesis of cysteine, ​​by which is possible the production of sulfurylated polysaccharides, proteins and lipids.

Credit: Giordano & Prioretti, 2016. The Physiology of Microalgae pp 185-209

Sulfur in the oceanic environment has not always had the current concentrations equal to 28 – 30 mM, considered the historical maximums (indicated by the red hexagon at the top), but has undergone strong fluctuations. We will consider the increase in oceanic sulphate that occurred between the end of the Paleozoic and the beginning of the Mesozoic with concentrations equal to 13 – 27 mM. In conjunction with the increase in oceanic sulphate, there was the radiation of phytoplanktonic organisms defined as the red lineage of plastid, i.e. those generated by secondary, tertiary or quaternary endosymbiosis from red algae represented in the graph by dinoflagellates, coccolithophorids and diatoms.

Therefore, in the study that I personally conducted during my experimental thesis, three representative species were chosen such as Tetraselmis suecica (green microalgae, evolved at oceanic sulphate concentrations below 10 mM), Dunaliella salina (green microalgae, evolved in concentration of oceanic sulphate slightly higher than the first species) and Phaeodactylum tricornutum the only representative species of microalgae of the red lineage, a diatom evolved at concentrations of oceanic sulphate between 13 and 27 mM.

Credit: Maria Bruno

What we wanted to investigate is if the physiological response of microalgae is different depending on whether they have evolved at a lower oceanic concentration of sulphate (such as the two green microalgae) or higher (such as Phaeodactylum tricornutum). In fact, according to the sulphate facilitation hypothesis, the increase of oceanic sulphate is not separated from the phytoplanktonic radiation of the organisms of the red lineage since they have a lower Carbon / Sulfur ratio.

The cultivation conditions of the mircoalgae were the control one (25 mM sulphate concentration in the medium) and a sulphate deficiency condition equal to 60 mM.

The physiological changes that were observed were much more evident in Phaeodactylum tricornutum, which showed a decrease in growth, an increase in cell weight, content of proteins and lipids, and a decrease in the band intensity of antenna proteins and Rubisco (viewed through SDS page) when cultivated in sulphate deficiency. The increase of proteins in P. tricornutum in condition of sulfate deficiency is justified by the increase in cellular nitrogen (major constituent of proteins). In addition, an increase in Carbon, allocated mostly in lipids, was also observed as previously mentioned. In fact, this species is defined as oleaginous, and by its nature under stressful conditions, it tends to accumulate the C within the reserve lipids (more than carbohydrates). As for the element of interest – sulfur, it increases under sulphate deficiency per cell. However, this data is soon explained by the subsequent Carbon / Sulfur ratio reported. 

C / S ratio for all the species
Credit: Maria Bruno

This ratio increases under sulphate deficiency, which indicates the actual lower quotas of S in sulphate deficient cells. In fact, remember that the sulphate deficient cells grow less, so they divide less, therefore, they weigh more and tend to retain an apparently higher portion of sulfur.

Despite the profound reorganization of the elements and macromolecules within the cell, the photosynthetic efficiency remains unchanged even in Phaeodactylum tricornutum. The allocation of resources, even with this stressful condition, remains as unaltered as possible along the electron transport chain, which allows the photosynthetic process, indicating the strict need for the latter to function properly.

Electron transport chain
Credit: Essays Biochem (2016) 60 (3): 255–273.

 

According to these studies, sulfur deficiency leads to a much deeper reorganization of cellular elements in Phaeodactylum tricornutum, the only species belonging to the red linage of plastid. There is thus a lower efficiency in the use of sulphate in this species, precisely because it has always had a high abundance of it in the oceanic environment. This is in accordance with the sulphate facilitation hypothesis, according to which the increase of oceanic sulphate is not disjoint and indeed has favored the phytoplanktonic radiation of the red lineage microalgae.

In conclusion, this element is to be considered one of the factors, together with others, biotic and abiotic, which determined the phytoplanktonic radiation of the organisms of the red lineage of the plastid, as well as the current phytoplankton composition.


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