Fermentation pathways and their interactions with photosynthesis in the marine diatom T. pseudonana: proteomic and biophysics approaches

The glycolysis associated with mitochondrial oxidative phosphorylation is the process by which the vast majority of eukaryotes produces ATP from sugar. Under hypoxic or anoxic conditions, fermentation pathways allow to maintain glycolytic activity by reducing alternative electron acceptors (other than O2) while generating various fermentation by-products. Anaerobic fermentation and photosynthesis coexist when organisms experience hypoxia or anoxia in their natural environment (e.g. marine sediments, eutrophic waters). In photosynthetic microeukaryotes, the detailed study of anaerobic metabolic pathways is limited to few freshwater model organisms such as Chlamydomonas reinhardtii (1). Based a previous genomic survey, Thalassiosira pseudonana, a centric marine diatom would contain a large variety of fermentation pathways (2). In our work, we studied the fermentation pathways and their interactions with photosynthesis in T. pseudonana. We first show that there are different waves of protein expression during the first 24 hours in anoxia in the dark. Several fermentative metabolites are also detected (H2, succinate), and our data suggest the existence of a bacterial fermentative pathway leading to butyrate production. The availability in photosynthetic electron acceptors is reduced but not null after 24h in anoxia. This suggests that at least one fermentative pathway is able to reoxidize photosynthetic electron acceptors, as it was previously shown for hydrogenase activity in C. reinhardtii (3). Finally, by comparing PSI and PSII activity, we evidence that a high and transient cyclic electron flow (CEF) around PSI is key to resume PSII electron transfer in anoxic condition. Overall, our results reveal regulatory mechanisms (CEF and fermentation pathways) that may help T. pseudonana cope with hypoxic or anoxic environments.

References:

(1) Muller, M. et al. (2012). Microbiol Mol Biol Rev, 76, 444-495

(2) Atteia et al. (2013). Biochim Biophys Acta - Bioenerg 1827: 210–223

(3) Godaux et al. (2013). Int. J. Hydrog. Energy, 38: 1826-1836