mRNA localization, reaction centre biogenesis and thylakoid membrane targeting in cyanobacteria

Abstract

The thylakoid membranes of cyanobacteria form a complex intracellular membrane system with a distinctive proteome. The sites of biogenesis of thylakoid proteins remain uncertain, as do the signals that direct thylakoid membrane-integral proteins to the thylakoids rather than to the plasma membrane. Here, we address these questions by using Fluorescent in situ Hybridisation to probe the subcellular location of mRNA molecules encoding core subunits of the photosystems in two cyanobacterial species. These mRNAs cluster at thylakoid surfaces mainly adjacent to the central cytoplasm and the nucleoid, in contrast to mRNAs encoding proteins with other locations. Ribosome association influences the distribution of the photosynthetic mRNAs on the thylakoid surface, but thylakoid affinity is retained in the absence of ribosome association. However, thylakoid association is disrupted in a mutant lacking two mRNA-binding proteins, which likely play roles in targeting photosynthetic proteins to the thylakoid membrane.

Probing the biogenesis pathway and dynamics of thylakoid membranes

“…4 c, 4d ), our results indicate that the initial steps of RC47 assembly occur predominantly in these newly generated thylakoid fragments. In a very recent study, we have revealed that the mRNA molecules encoding the core subunits of PSI and PSII clustered at the thylakoid surfaces that are mainly adjacent to the central cytoplasm 66 . We showed that the locations of mRNA molecules correspond to the sites of translation.…”

“…In addition to the orders of assembly of photosynthetic complexes, our study also provides clues about the de novo membrane integration and assembly sites of photosynthetic complexes and the dynamics of their subcellular locations. The thylakoid membranes 63 , thylapse membrane domains 15 or PratA-defined membrane (PDM) regions 56,[64][65][66] in Synechocystis, and the translation zones in the chloroplast of Chlamydomonas 67,68 have been proposed to be the principal sites for the initial biogenesis and/or assembly of photosynthetic complexes, in particular PSII. Our confocal images showed explicitly that during the initial stages of thylakoid biogenesis, compared to other photosynthetic complexes, PSII complexes exhibited a greater accumulation on one longitudinal side of the Synechoccoccus cell, where the newly synthesized thylakoid fragments appear (Fig.…”

Probing the biogenesis pathway and dynamics of thylakoid membranes

“…In addition to the assembly orders of photosynthetic complexes, our study also provides clues about the de novo membrane integration and assembly sites of photosynthetic complexes and the dynamics of their subcellular locations. The thylakoid membranes 63 , thylapse membrane domains 15 or PratA-defined membrane (PDM) regions 56,[64][65][66] in Synechocystis, and the translation zones in the chloroplast of Chlamydomonas 67,68 have been proposed to be the principal sites for the initial biogenesis and/or assembly of photosynthetic complexes, in particular PSII. Our confocal images showed explicitly that at the initial step of thylakoid biogenesis, compared to other photosynthetic complexes, PSII complexes exhibited a greater accumulation on one longitudinal side of the Synechoccoccus cell where the newly synthesized thylakoid fragments appear (Fig.…”

The temperature-regulated DEAD-box RNA helicase CrhR interactome: Autoregulation and photosynthesis-related transcripts

“…Functionally, the prime targets of CrhR interaction were consistently observed to include transcripts associated with photosynthesis, light harvesting or directly encoding core photosystem proteins ( Table 1 ). A role in the biology of photosynthesis-relevant mRNAs would further be consistent with the demonstrated localization of ribosome-associated CrhR at the thylakoid membrane (Rosana et al ., 2016) and also the observation that psbA and psaA mRNAs are transported to the thylakoid membrane and possibly translated by thylakoid-associated ribosomes (Tyystjärvi et al ., 2001; Mahbub et al ., 2020). These findings point to a possible involvement of CrhR in physiological secondary structure rearrangements of the identified mRNAs that could influence translation on thylakoid membrane associated ribosomes.…”