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

Abstract

A symbiotic association occurs in 'Chlorochromatium aggregatum', a phototrophic consortium integrated by two species of phylogenetically distant bacteria composed by the green-sulfur Chlorobium chlorochromatii CaD3 epibiont that surrounds a central b-proteobacterium. The nonmotile chlorobia can perform nitrogen and carbon fixation, using sulfide as electron donors for anoxygenic photosynthesis. The consortium can move due to the flagella present in the central b-protobacterium. Although Chl. chlorochromatii CaD3 is never found as free-living bacteria in nature, previous transcriptomic and proteomic studies have revealed that there are differential transcription patterns between the symbiotic and free-living status of Chl. chlorocromatii CaD3 when grown in laboratory conditions. The differences occur mainly in genes encoding the enzymatic reactions involved in nitrogen and amino acid metabolism. We performed a metabolic reconstruction of Chl. chlorochromatii CaD3 and an in silico analysis of its amino acid metabolism using an elementary flux modes approach (EFM). Our study suggests that in symbiosis, Chl. chlorochromatii CaD3 is under limited nitrogen conditions where the GS/GOGAT (glutamine synthetase/glutamate synthetase) pathway is actively assimilating ammonia obtained via N 2 fixation. In contrast, when free-living, Chl. chlorochromatii CaD3 is in a condition of nitrogen excess and ammonia is assimilated by the alanine dehydrogenase (AlaDH) pathway. We postulate that 'Chlorochromatium aggregatum' originated from a parasitic interaction where the N 2 fixation capacity of the chlorobia would be enhanced by injection of 2-oxoglutarate from the b-proteobacterium via the periplasm. This consortium would have the advantage of motility, which is fundamental to a phototrophic bacterium, and the syntrophy of nitrogen and carbon sources.

Metagenomic Characterization of <i>Candidatus</i> Smithella cisternae Strain M82_1, a Syntrophic Alkane-Degrading Bacteria, Enriched from the Shengli Oil Field

“…All genes required for the β-oxidation of long-chain fatty acids were identified, in which multiple ORFs encoding acyl-CoA dehydrogenase ( 16 ) and enoyl-CoA hydratase ( 12 ) were also detected ( Fig. 3 , Table S7 ), and this is consistent with our previous findings ( 19 ).…”

Chlorobaculum tepidum Modulates Amino Acid Composition in Response to Energy Availability, as Revealed by a Systematic Exploration of the Energy Landscape of Phototrophic Sulfur Oxidation

“…Prior studies of C. tepidum indicate that glutamine synthase/glutamine aminotransferase (GS/GOGAT) is the main route of ammonium assimilation in C. tepidum (49), which would be expected to contribute to free pools of glutamate and glutamine. Alanine dehydrogenase (ADH) has been suggested as an alternative ammonium assimilation pathway in "Chlorobium chlorochromatii" (50), which is consistent with our observation of an extractable alanine pool. This is further supported by C. tepidum transcriptome sequencing data (51), which showed that genes for GS/GOGAT (CT1411, CT0401, CT0402) and ADH (CT0650, CT0706) were expressed at similar levels.…”

Better together: engineering and application of microbial symbioses

“…[11] c. Division of labor is accomplished in C. aggregatum with the green sulfur photosynthesizing and the β-proteobacterium providing light-sensitive motility. [91,[13][14][15] d. Bacterial symbionts have been shown to contribute multiple processes the lichen Lobaria pulmonaria. [92,18] e. Potential roles of different organisms in methanogenic communities were determined by Embree et al demonstrating division of labor within the community.…”