Genomic analysis reveals key aspects of prokaryotic symbiosis in the phototrophic consortium “Chlorochromatium aggregatum”

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.

Better together: engineering and application of microbial symbioses

“…determined that the β-proteobacterium depends largely on the photosynthetic epibionts for energy through metabolic coupling and, potentially, electron transfer. [15] The β-proteobacterium has a reduced genome in comparison to free-living relatives but gains photosensitive motility despite its inability to do photosynthesis indicating increased evolutionary fitness when with its epibionts. [15] The roles in microbial communities are not always well defined.…”

Endosymbiosis before eukaryotes: mitochondrial establishment in protoeukaryotes

“…Providing transportation for the other party to find resources Chlorochromatium aggregatum: the motile central Betaproteobacterium transports its nonmotile photosynthetic epibionts towards light [177], while the epibionts provide energy for the host [155] The slime mould Dictyostelium can set aside and distribute with its spores phagocytized Burkholderia cells to colonize new habitats and provide food for the new colony [103] Indirect benefits and costs Secondary effects that stem from the primary relationship, but manifest only occasionally or are comparably smaller in effect Metabolic exchange: the metabolite is the primary benefit, while the host also has access to an alternative metabolic pathway within the symbiont for energy harnessing. Metabolically diverse symbioses (e.g., biofilms), provide the benefit of robustness against harsh or fluctuating conditions [199].…”

“…Control mechanisms are not only important for selecting the most beneficial partner but also to avoid asynchronous reproduction of the partners. In some cases, cell-cycle synchronization of host and symbiont might happen before internalization: in Chlorochromatium aggregatum the host and its epibionts seem to divide synchronized and orchestrated [155,156]; however, the mechanisms are unclear. After internalization of the partner, synchronization becomes even more important.…”

Eukaryogenesis, how special really?

“…Processes of evolution in which entities from different lineages can be bound together in the creation of new community-level reproductive individuals are not uncommon, and such symbiotic entities occur at hierarchical levels above that of the cell, sometimes among exclusively eukaryotic partners. Although there are some aspects of the eukaryotic condition that have not been documented in higher-level egalitarian alliances (e.g., gene transfer between partners), even these aspects are not unique to mitochondria and plastids, as both the Paulinella and "Chlorochromatium aggregatum" cases show (21,44).…”