Supramolecular structure of stacked and unstacked regions of the photosynthetic membranes of Prochloron sp., a prokaryote

Abstract

Freeze-fracture replicas of the photosynthetic prokaryote Prochioron sp., collected at Coconut Island, Hawaii,show that the thylakoids are differentiated into stacked and unstacked regions much like the thylakoids of green algae and higher plants. On the exoplasmic (E) fracture face, the particle density is greater in stacked regions (Q3100 particles/,gm2) than in unstacked regions (t925 particles/,gmV). On the complementary protoplasmic (P) fracture face, the particle density is lower in stacked regions (Q2265 particles/,gm than in unstacked regions (;4980 particles/1sm2). typical closed thylakoids. As in the cyanobacteria, the thylakoids are the only observable membrane system in the cytoplasm and they are not enclosed by an envelope membrane. The thylakoids of Prochloron differ from those of the cyanobacteria in that they lack detectable phycobilisomes, large (n-300 A) aggregates of phycobiliproteins localized on the thylakoid surface. Most significantly for the present work, thin sections of Prochloron suggest that there are some areas of close appression ("stacked regions") between adjacent thylakoids. The freezefracture electron microscopy presented here provides evidence that morphologically differentiated stacked and unstacked regions similar to those found in the chloroplasts of green algae and higher plants occur in the thylakoids of Prochloron. MATERIALS AND METHODSProchloron was collected at Coconut Island, Oahu, Hawaii, as described (8). Green colonies of didemnid ascidians, Diplosoma virens, were collected from shallow waters. Green spherical cells, identified as Prochloron, were released from the ascidians by gently pressing on the colonies with a pasteur pipette while flushing the surface with sea water. Cells were centrifuged, then rinsed in filtered sea water and prepared on location for freeze-fracturing in one of three ways: (i) Cells were sedimented and samples of the pellet were applied to copper support discs. The disc and sample were plunged into liquid Freon 22 and quickly transfered to liquid nitrogen. (ii) Five milliliters of 70% glycerol/30% sea water (vol/vol) The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact.

Cryo-Electron Tomography Reveals the Comparative Three-Dimensional Architecture ofProchlorococcus, a Globally Important Marine Cyanobacterium

“…The lumen is consistently less dense than the cytoplasmic space. Although this tight packing of the internal membranes is possible because Prochlorococcus lacks phycobilisomes, the structure and organization of these membranes are distinct from those of other chlorophyll a/b-containing cyanobacteria (11,28) in that the membrane layers are arranged uniformly and are not interspersed throughout the central cytoplasm. In contrast, MED4 possesses a less extensive internal membrane system, with only two to four mem- brane bands apposed to the cell membrane in one or two regions of the cell and sometimes extending around the entire cell periphery (Fig.…”

“…A key structure in the Prochlorococcus cell is the intracytoplasmic membrane system. In cyanobacteria, these membranes are critical for photosynthesis as well as other fundamental metabolic processes (11,23,28,31,44,45,51). When grown under identical conditions of irradiance level (10 mol photons m Ϫ2 s Ϫ1 ), temperature (21°C), and nutrients, MIT9313 synthesizes a more extensive network of internal membranes than MED4.…”

Species concepts and speciation factors in cyanobacteria, with connection to the problems of diversity and classification

“…Prochlorococcus, Prochlorothrix, and Prochloron are cyanobacteria that additionally produce chlorophyll b (the typical pigment of green algae and land plants) and lack phycobilisomes (Giddings et al 1980;Burger-Wiersma et al 1986;Miller et al 1988;Chisholm et al 1992;Hess et al 1996;Pinevich et al 1997;Kauff and Büdel 2011). On this basis and due to a psbA gene based phylogenetic analysis, they were considered strictly associated with the chloroplast of green algae and terrestrial plants (Morden and Golden 1989).…”

Unique Thylakoid Membrane Architecture of a Unicellular N2-Fixing Cyanobacterium Revealed by Electron Tomography

“…In contrast, other strains, such as some of those in the genus Cyanothece, have thylakoid membranes that appear to be arranged in a radial pattern within the cell, like spokes of a wheel, but still parallel to each other (Porta et al, 2000). Regardless of their overall arrangement, thylakoid membranes are typically separated from each other by a space sufficient for a double row of phycobilisomes, large light-harvesting antenna complexes, to fit between the membranes (Mullineaux, 1999), but have been reported with appressed regions in a few strains, including Prochloron (Giddings et al, 1980) and Acaryochloris marina (Marquardt et al, 2000;Chen et al, 2009).…”