Abstract
Background‘Chlorochromatium aggregatum’ is a phototrophic consortium, a symbiosis that may represent the highest degree of mutual interdependence between two unrelated bacteria not associated with a eukaryotic host. ‘Chlorochromatium aggregatum’ is a motile, barrel-shaped aggregate formed from a single cell of ‘Candidatus Symbiobacter mobilis”, a polarly flagellated, non-pigmented, heterotrophic bacterium, which is surrounded by approximately 15 epibiont cells of Chlorobium chlorochromatii, a non-motile photolithoautotrophic green sulfur bacterium.ResultsWe analyzed the complete genome sequences of both organisms to understand the basis for this symbiosis. Chl. chlorochromatii has acquired relatively few symbiosis-specific genes; most acquired genes are predicted to modify the cell wall or function in cell-cell adhesion. In striking contrast, ‘Ca. S. mobilis’ appears to have undergone massive gene loss, is probably no longer capable of independent growth, and thus may only reproduce when consortia divide. A detailed model for the energetic and metabolic bases of the dependency of ‘Ca. S. mobilis’ on Chl. chlorochromatii is described.ConclusionsGenomic analyses suggest that three types of interactions lead to a highly sophisticated relationship between these two organisms. Firstly, extensive metabolic exchange, involving carbon, nitrogen, and sulfur sources as well as vitamins, occurs from the epibiont to the central bacterium. Secondly, ‘Ca. S. mobilis’ can sense and move towards light and sulfide, resources that only directly benefit the epibiont. Thirdly, electron cycling mechanisms, particularly those mediated by quinones and potentially involving shared protonmotive force, could provide an important basis for energy exchange in this and other symbiotic relationships.
Highlights
IntroductionSymbiotic interactions between bacteria and eukaryotes are common and can be mutualistic (for example, between nitrogen-fixing Rhizobium spp. and legumes [1] or between sulfur-oxidizing Gamma- or Epsilonbacteria and marine invertebrates [2]) or parasitic (for example, bacterial pathogens and human hosts)
Symbiotic interactions between bacteria and eukaryotes are common and can be mutualistic or parasitic
311 open reading frame (ORF) (15%), most of which encode proteins with unidentified functions, have no homologs in genomes of other green sulfur bacteria (GSB), which are not known to be involved in phototrophic consortia (Table S1 in Additional file 2)
Summary
Symbiotic interactions between bacteria and eukaryotes are common and can be mutualistic (for example, between nitrogen-fixing Rhizobium spp. and legumes [1] or between sulfur-oxidizing Gamma- or Epsilonbacteria and marine invertebrates [2]) or parasitic (for example, bacterial pathogens and human hosts). Ten morphologically distinct types are known, and most are barrelshaped, motile aggregates comprising two cell types: a central bacterium, which is a single, non-pigmented, and heterotrophic cell carrying a single polar flagellum; and approximately 15 to >40 epibionts, which are greenor brown-colored green sulfur bacteria (GSB) [10,11,12] (Figure 1; Figure S1 in Additional file 1). The epibiont of “Chlorochromatium aggregatum”, Chlorobium (Chl.) chlorochromatii strain CaD3, is not obligately symbiotic It has been isolated and grown axenically, and physiological characterization showed that Chl. chlorochromatii is similar to other free-living GSB isolates [14]. Compared to free-living close relatives, “Ca. S. mobilis” has apparently undergone massive gene loss and is probably no longer capable of independent growth
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