Dynamic macromolecular composition and high exudation rates in Prochlorococcus

Abstract

Every living cell is composed of macromolecules such as proteins, DNA, RNA, and pigments. The ratio between these macromolecular pools depends on the allocation of resources within the organism to different physiological requirements, and in turn affects biogeochemical cycles of elements such as carbon, nitrogen, and phosphorus. Here, we present detailed measurements of the macromolecular composition of Prochlorococcus MIT9312, a representative strain of a globally abundant marine primary producer, as it grows and declines due to nitrogen starvation in laboratory batch cultures. As cells reached stationary stage and declined, protein per cell decreased by $ 30% whereas RNA per cell and pigments per cell decreased by $ 75%. The decline stage was associated with the appearance of chlorotic cells, which had higher forward scatter (a proxy for cell size) but lower chlorophyll autofluorescence, as well as with changes in photosynthetic pigment composition. Specifically, during culture decline divinyl-chlorophyll-like pigments emerged, which were not observed during exponential growth. These divinyl-chlorophyll-like pigments were also observed in natural samples from the Eastern Mediterranean. Over 90% of the carbon fixed by Prochlorococcus MIT9312 (but not of a different strain, NATL2A) was released into the growth media under these laboratory conditions. Variations in RNA/protein indicate that, broadly defined, the macromolecular composition of Prochlorococcus MIT9312 is more similar to eukaryotic phytoplankton than to marine heterotrophic bacteria, possibly due to the significant investment in photosynthetic machinery of phototrophs.

Single-cell measurements and modelling reveal substantial organic carbon acquisition by Prochlorococcus

“…Furthermore, organic carbon uptake contributes ~80% at HOT and 54% at EqPac of the total production below the depth where the contribution of mixotrophy is greater than photosynthesis, broadly consistent with the isotopic inference from the deep photic zone in the Mediterranean. We note that this model does not take into account exudation of organic carbon by Prochlorococcus , which is not well constrained experimentally and would probably reduce the inferred growth rates at the surface 40 – 43 . Indeed, mixotrophy (uptake of glucose and amino acids) has been observed in surface Prochlorococcus 9 , 10 , suggesting that our estimate provides a lower bound of the contribution of mixotrophy to integrated Prochlorococcus production.…”

“…It is known that Prochlorococcus can assimilate amino acids 9 and therefore the stoichiometry of the heterotrophic contribution might alter the interpretations. However, it is also known that Prochlorococcus can exude amino acids 40 , which might cancel out the effects on the stoichiometry of Prochlorococcus .…”

Modeling Photosynthesis and Exudation in Subtropical Oceans

“…The excretion of dissolved organic carbon (DOC) in nutrient replete, exponentially growing phytoplankton is low, E 2% of total gross carbon fixation (López-Sandoval et al, 2013). However, recent studies show that Prochlorococcus, an abundant pico-cyanobacterium found in oligotrophic ocean regions and which only have a moderate ability for photoacclimation, can excrete a large fraction of fixed C under nutrient-limited conditions (Bertlisson et al, 2005;Cailliau et al, 1996;Kulk et al, 2011;Roth-Rosenberg et al, 2021;Szul et al, 2019;Thompson et al, 2018). Thus exudation is more likely significant in the oligotrophic surface ocean where there is persistent nutrient limitation and light-saturating conditions.…”

Testing the growth rate and translation compensation hypotheses in marine bacterioplankton

“…The higher values for Prochlorococcus NATL2A compared to Prochlorococcus MIT9312 are in agreement with the difference in size between the two strains (Cermak et al, 2017). The RNA quotas for MIT9312 are somewhat lower than previously reported (~1–6 fg/cell compared with ~9 fg/cell for MIT9312; Roth‐rosenberg et al, 2020; and ~3–4 fg/cell for MED4; Casey et al, 2022).…”