Photosynthetic Apparatus in Roseateles depolymerans 61A Is Transcriptionally Induced by Carbon Limitation

Abstract

Production of a photosynthetic apparatus in Roseateles depolymerans 61A, a recently discovered freshwater ␤-Proteobacterium showing characteristics of aerobic phototrophic bacteria, was observed when the cells were subjected to a sudden decrease in carbon sources (e.g., when cells grown with 0.1 to 0.4% Casamino Acids were diluted or transferred into medium containing <0.04% Casamino Acids). Accumulation of bacteriochlorophyll (BChl) a was observed in the presence of oxygen and was enhanced under semiaerobic conditions (2% oxygen) but was reduced in the presence of light. Similarly to what has been reported regarding some aerobic phototrophic bacteria belonging to the ␣ subclass of the Proteobacteria, viability of the cells in the carbon source-free medium was prolonged under aerobic-light (10 W m ؊2 ) conditions, possibly due to photosynthetic energy conversion, but was not prolonged under aerobic-dark conditions. The puf operon, which encodes most of the apoproteins of light-harvesting and reaction center complexes, was sequenced, and the effect of changes in Casamino Acids concentrations, oxygen, and light on its expression was estimated by the accumulation of its mRNA. The expression of the puf operon was induced by the decrease in carbon sources, similarly to what was observed for the accumulation of BChl a under aerobic and semiaerobic conditions (>0.2% O 2 ), and was reduced in the presence of light. Transcription of the R. depolymerans puf operon is considered to be controlled by changes in carbon nutrients in addition to oxygen tension and light intensity.Purple phototrophic bacteria are taxonomically affiliated with the ␣, ␤, and ␥ subclasses of the class Proteobacteria. Many of the species grow both heterotrophically under aerobic-dark conditions and phototrophically under anaerobic-light conditions. The production of a photosynthetic apparatus in most of these phototrophic species is reduced under aerobic conditions (18). On the other hand, some species, the so-called aerobic phototrophic bacteria (e.g., Erythrobacter longus and Roseobacter denitrificans), do not grow phototrophically under anaerobic-light conditions, whereas they produce a photosynthetic apparatus under aerobic conditions (31, 41). Aerobic phototrophic bacteria had been reported only for the ␣ subclass of the Proteobacteria (31, 41) until the discovery of Roseateles depolymerans, which belongs to the ␤ subclass of the Proteobacteria (34).Although the presence of photochemical activity has been clarified in some species of aerobic phototrophic bacteria, they do not grow on light as a sole energy source (14,31,36,38). However, stimulation of growth in the presence of light has been reported for R. denitrificans, Erythromicrobium hydrolyticum, and Acidisphaera rubrifaciens (13,15,42). It has also been suggested for R. denitrificans, Bradyrhizobium strain BTAi 1, and A. rubrifaciens that the preservation of viability is improved by the presence of light in the absence of nutrients (9,15,29). While these observations have been reported f...

Evidence for the Ubiquity of Mixotrophic Bacteria in the Upper Ocean: Implications and Consequences

“…For Cyanobacteria, mixotrophy was previously described by Rippka in 1972 (66), and some years later aerobic photo-"organo"-heterotrophic bacteria containing Bchl-a were isolated by Shiba and coworkers (75). Since then, many more bacteria using a mixotrophic metabolism have been identified and affiliated with various phyla, i.e., Chloroflexi (61), Cyanobacteria (see, for example, references 7, 49, 54, 66, and 95), and Proteobacteria (71,76,85). These bacteria embody a wide genetic and functional diversity, as shown in many isolates of Cyanobacteria (see, for example, references 7, 49, 54, 66, and 95) and AAnPB (see reviews in references 64 and 91).…”

“…However, none of the AAnPB isolates has yet been grown autotrophically, and the key enzyme of the Calvin cycle, ribulosebisphosphate carboxylase, has not been found in any AAnPB species (93). Nonetheless, light stimulation of CO 2 uptake was detected in several species (33,77,78,85). Although the degree of CO 2 fixation seems too low for purely autotrophic growth, it could provide additional organic carbon intermediates for an otherwise purely heterotrophic metabolism.…”

Environmental Biology of the Marine Roseobacter Lineage

“…The synthesis of bchla is completely inhibited even by very low light intensities. The amount of bchla produced in the dark is generally about 10 % or less of that in anaerobic anoxygenic phototrophs, and in some species it depends strongly on nutrient composition, salt concentration, and unknown stress factors (10,12,101). Synthesis of bchla and can even be transiently completely suppressed like in Roseovarius tolerans (3,58).…”

Aerobic Anoxygenic Photosynthesis in Roseobacter Clade Bacteria from Diverse Marine Habitats

“…It is completely suppressed by light. In addition, oxygen concentration and carbon limitation have been shown to be involved in Roseateles depolymerans photosynthesis (34). It might be expected that production of Bchl a can be induced in most of the isolates that have pufLM genes if the "right" conditions are found.…”