Chloroplast-mitochondria cross-talk in diatoms

Abstract

Diatoms are unicellular, mainly photosynthetic, eukaryotes living within elaborate silicified cell walls and believed to be responsible for around 40% of global primary productivity in the oceans. Their abundance in aquatic ecosystems is such that they have on different occasions been described as the insects, the weeds, or the cancer cells of the ocean. In contrast to higher plants and green algae which derive from a primary endosymbiosis, diatoms are now believed to originate from a serial secondary endosymbiosis involving both green and red algae and a heterotrophic exosymbiont host. As a consequence of their dynamic evolutionary history, they appear to have red algal-derived chloroplasts empowered largely by green algal proteins, working alongside mitochondria derived from the non-photosynthetic exosymbiont. This review will discuss the evidence for such an unusual assemblage of organelles in diatoms, and will present the evidence implying that it has enabled them with unorthodox metabolisms that may have contributed to their profound ecological success.

Nitrate Reductase Knockout Uncouples Nitrate Transport from Nitrate Assimilation and Drives Repartitioning of Carbon Flux in a Model Pennate Diatom

“…Given the closely juxtaposed organelles, four plastid membranes and confined cytosolic spaces of P. tricornutum (Apt et al, 2002;Prihoda et al, 2012), an association between NR, plasma membrane transporters, and vacuolar membrane transporters may form as the proteins coalesce under specific conditions to facilitate the flux of NO 3 2 from the environment into and out of the vacuole. It remains to be determined whether free NO 3 2 is ever resident in the cytosol and whether, upon transport into the cell, it is either immediately reduced and transported into the chloroplasts or pumped into the vacuole.…”

High Light Acclimation in the Secondary Plastids Containing Diatom Phaeodactylum tricornutum is Triggered by the Redox State of the Plastoquinone Pool

“…One explanation might be based on the very unusual electron fluxes in diatoms, which are still far from being understood. These include the following: (1) a vivid exchange of electrons between the electron transport chains of chloroplasts and mitochondria (Prihoda et al, 2012); (2) a cyclic electron transfer in PSII (Lavaud et al, 2002b;Onno Feikema et al, 2006;Lavaud et al, 2007); (3) a chlororespiration process that can modify the redox balance of the quinones and of PQ (Jakob et al, 1999;Dijkman and Kroon, 2002;Grouneva et al, 2009;Cruz et al, 2011); and (4) a recombination of Q A 2 and Q B 2 with the oxidized states of the manganese cluster in the PSII core induced by conformational changes (Eisenstadt et al, 2008). Therefore, an additional switch provided by the acceptor side of PSII (Q A and Q B ) might help, in combination with the redox state of the PQ pool, to sort the different electron flows and to fine-tune the synthesis of xanthophylls and the transcription of light-responsive genes like LHCX, depending on the source of electrons.…”

A Hard Day's Night: Diatoms Continue Recycling Photosystem II in the Dark

“…The diatoms, like other chlorophyll a/c organisms, have a triply layered thylakoid organization (Gibbs, 1962;Drum, 1963;Lepetit et al, 2012) that may place kinetic limitations upon access of the FtsH protease (Komenda et al, 2012) to PSII, in contrast to the single layer thylakoid arrangement in cyanobacteria, or the grana/stroma thylakoid organization of higher plants. The 1-2 ATP per peptide bond to drive chloroplastic protein degradation (Nixon et al, 2010;Raven, 2011;Komenda et al, 2012;Campbell et al, 2013) in the dark must derive from the tight coupling of chloroplastic and mitochondrial ATP and amino acid metabolism in diatoms Prihoda et al, 2012;Bailleul et al, 2015). This dark PsbA turnover capacity is particularly evident in the small, coastal strain T. pseudonana in this study.…”

“…Marine diatoms are major oceanic primary producers (Field et al, 1998;Armbrust, 2009) with distinctive biooptical (Key et al, 2010) and metabolic (Armbrust, 2004;Allen et al, 2011;Hopkinson et al, 2011) characteristics, including tight metabolic coupling between their chloroplasts and mitochondria (Prihoda et al, 2012;Bailleul et al, 2015). Like all oxygenic photoautotrophs, diatoms use Photosystem II (PSII) to photooxidize water and generate the reductant that supports their biological productivity.…”

“…Given recent findings of ATP shuttling between mitochondria and chloroplasts (Prihoda et al, 2012;Bailleul et al, 2015) to drive CO 2 fixation in diatoms, we hypothesized that dark repair of PSII, supported by respiration, could confer an advantage upon marine diatoms, which thrive in fluctuating light environments (MacIntyre et al, 2000;Lavaud et al, 2007). We thus measured pools of PSII active , and the degradation and synthesis rates of key PSII proteins across diel cycles (Chisholm and Costello, 1980) and growth light levels.…”