Ultrastructural Characterization of the Prokaryotic Symbiosis in “Chlorochromatium aggregatum”

Abstract

The phototrophic consortium "Chlorochromatium aggregatum" currently represents the most highly developed interspecific association of bacteria and consists of green sulfur bacteria, so-called epibionts, surrounding a central, motile, chemotrophic bacterium. In order to identify subcellular structures characteristic of this symbiosis, consortia were studied by a combination of high-resolution analytical scanning electron microscopy, transmission electron microscopy, and three-dimensional reconstruction and image analyses. Epibionts are interconnected and to a lesser extent are also connected with the central bacterium, by electron-dense, hair-like filaments. In addition, numerous periplasmic tubules extend from the outer membrane of the central bacterium and are in direct contact with the outer membrane of the epibionts. In each epibiont cell, the attachment site to the central bacterium is characterized by the absence of chlorosomes and an additional 17-nm-thick layer (epibiont contact layer [ECL]) attached to the inner side of the cytoplasmic membrane. The ECL is only occasionally observed in pure cultures of the epibiont, where it occurs in about 10 to 20% of the free-living cells. A striking feature of the central bacterium is the presence of one or two hexagonally packed flat crystals (central bacterium crystal [CBC]) per cell. The CBC reaches 1 microm in length, is 35 nm thick, and consists of bilayers of subunits with a spacing of 9 nm. A detailed model for consortia is presented, summarizing our conclusions regarding (i) cohesion of the cells, (ii) common periplasmic space between the central bacterium and the epibiont, (iii) ECL as a symbiosis-specific structure, and (iv) formation of the interior paracrystalline structures, central bacterium membrane layer, and CBC.

Metabolic analysis of Chlorobium chlorochromatii CaD3 reveals clues of the symbiosis in ‘Chlorochromatium aggregatum’

“…If the theoretical difficulties described above can be overcome, we propose that the b-proteobacterium diffuses 2-oxoglutarate to the Chlorobia via their shared periplasm (Wanner et al, 2008). Figure 4 summarizes what this study proposes, where in free-living state Chl.…”

“…Ultrastructural characterizations of 'C. aggregatum' suggest that there is a common periplasmic space between both bacteria (Wanner et al, 2008). This would facilitate the diffusion of 2-oxoglutarate from the central bacterium to the chlorobia.…”

“…chlorochromatii CaD3 in symbiotic state where 2-oxoglutarate (2-OG) is assimilated by the b-proteobacterium and diffused to Chl. chlorochromatii CaD3 through the shared periplasm that is, periplasmic tubules (Wanner et al, 2008). 2-oxoglutarate interacts with the PII and NifA proteins, stimulating the expression of the nif operon (Op.…”

Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria

“…This type of cooperative interaction is very widespread among both Bacteria and Archaea and is frequently based on the reciprocal exchange of certain metabolites (Schink, 2002;McInerney et al, 2008;Sieuwerts et al, 2008;Morris et al, 2013). For those cases, where the interaction partners have been studied in more detail, characteristic features such as the loss of essential biosynthetic functions (McInerney et al, 2007) or the formation of physical attachment structures (Ishii et al, 2005;Wanner et al, 2008) have been reported that may have arisen as specific adaptations to the symbiotic lifestyle. Unfortunately, the obligate interdependence of both partners makes it often difficult to study this type of interactions under laboratory conditions (Nauhaus et al, 2002;Pernthaler et al, 2008;McCutcheon and Moran, 2012).…”

Brevitalea aridisoli, B. deliciosa and Arenimicrobium luteum, three novel species of Acidobacteria subdivision 4 (class Blastocatellia) isolated from savanna soil and description of the novel family Pyrinomonadaceae

“…For scanning electron microscopy cells were fixed chemically with glutaraldehyde and further processed as described previously (Wanner et al, 2008). To exclude artefacts due to shrinking of cells during the chemical fixation procedure for imaging of ultrathin sections cells were highpressure frozen and cryosubstituted as described previously (Wanner et al, 2008).…”