Mixotrophic growth of bacteriochlorophyll a-containing members of the OM60/NOR5 clade of marine gammaproteobacteria is carbon-starvation independent and correlates with the type of carbon source and oxygen availability
© Spring and Riedel; licensee BioMed Central Ltd. 2013
Received: 29 January 2013
Accepted: 16 May 2013
Published: 24 May 2013
Populations of aerobic anoxygenic photoheterotrophic bacteria in marine environments are dominated by members of the Roseobacter lineage within the Alphaproteobacteria and the OM60/NOR5 clade of gammaproteobacteria. A wealth of information exists about the regulation of pigment production and mixotrophic growth in various members of the Roseobacter clade, but a detailed knowledge about aerobic bacteriochlorophyll a-containing gammaproteobacteria is still limited to one strain of the species Congregibacter litoralis.
The production of photosynthetic pigments and light-dependent mixotrophic growth was analysed in Luminiphilus syltensis DSM 22749T, Chromatocurvus halotolerans DSM 23344T and Pseudohaliea rubra DSM 19751T, representing three taxonomically diverse strains of bacteriochlorophyll a-containing gammaproteobacteria affiliated to the OM60/NOR5 clade. In these strains the expression of a photosynthetic apparatus depended mainly on the type of carbon source and availability of oxygen. The effect of illumination on pigment expression varied significantly between strains. In contrast to Chromatocurvus halotolerans, pigment production in Luminiphilus syltensis and Pseudohaliea rubra was repressed by light of moderate intensities, probably indicating a higher sensitivity to light-induced oxidative stress. The efficiency of using light for mixotrophic growth did not correlate with the cellular level of photosynthetic pigments, but depended mainly on the type of metabolized substrate with malate being the optimal carbon source in most cases.
Oligotrophic growth conditions or carbon limitation were not required for light-dependent mixotrophic growth in members of the OM60/NOR5 clade. The ability of using light as energy source and the fine tuning of photosynthesis gene expression depended mainly on the type of carbon source and oxygen availability, which indicates that the regulation of pigment production is controlled by the cellular redox state. While light has the main impact on the regulation of photosynthetic pigments in photoheterotrophic representatives of the Roseobacter lineage this was not the case in strains of the OM60/NOR5 clade.
Aerobic anoxygenic photoheterotrophic bacteria are found in large numbers in upper ocean waters and marine sediments [1–3]. Populations of this functional group in marine ecosystems are dominated by representatives belonging to the Roseobacter clade within the class Alphaproteobacteria and the OM60/NOR5 clade within the Gammaproteobacteria[4, 5]. Due to their high abundance in oceans, aerobic anoxygenic photoheterotrophs can play a significant role in the marine carbon cycle. It was estimated that up to 5.7% of the total phototrophic energy flow in open ocean waters could rely on bacteriochlorophyll a (BChl a)-based photophosphorylation [6, 7]. The prevalence of aerobic anoxygenic photoheterotrophy in marine ecosystems is probably based on two reasons: First, the utilization of light for mixotrophic growth enhances biomass formation under conditions of carbon limitation and gives aerobic anoxygenic photoheterotrophs a selective advantage against obligate chemoheterotrophic bacteria. Secondly, utilization of solar energy by aerobic anoxygenic photoheterotrophs is largely independent from photoinhibition, which is caused by high light-intensities in surface waters and reduces the chlorophyll a-based photosynthetic activity of oxygenic photoautotrophs .
In order to verify both assumptions, it is of interest to elucidate which factors control the expression of the photosynthetic apparatus in cells of aerobic anoxygenic photoheterotrophs and how the energy yield generated by light-harvesting correlates with the environmental conditions. The regulation of pigment production and light-dependent growth in members of the Alphaproteobacteria has been analysed previously in numerous studies [8–13]. In most of these studies exposure to light was identified as major factor that negatively controls the expression level of photosynthetic pigments. In a study about the transcriptional response of Dinoroseobacter shibae to changing light regimes the repression of pigment synthesis in the light coincided with a response to oxidative stress that was traced back to the formation of singlet oxygen at the photosynthetic apparatus. It was assumed that in response to the oxidative stress caused by the interaction of light with photosynthetic pigments a repression of the photosynthetic pigment production is induced by the transcriptional modulator TspO . In contrast, the corresponding knowledge about BChl a-containing aerobic gammaproteobacteria belonging to the OM60/NOR5 clade is still quite sparse due to the low number of available pure cultures and their fastidious growth in defined media. Previously, it was shown that in the aerobic gammaproteobacterium Congregibacter litoralis (C. litoralis) anoxygenic photophosphorylation depends on the carbon source and incubation conditions , but not on the carbon concentration, which is in contradiction to the finding of Cho et al. , who analysed the mixotrophic growth of the marine gammaproteobacterium HTCC2080 and found a positive correlation with very low nutrient concentrations. In another study a correlation of the pigment production in Chromatocurvus halotolerans (C. halotolerans) with the salinity of the used medium was found . The reported results are however difficult to compare, because the experimental setups were not consistent. In order to broaden our knowledge on the mixotrophic growth behaviour of aerobic BChl a-containing gammaproteobacteria it would be therefore desirable to analyse various strains of this clade using the same study design. In the present work, three taxonomically diverse strains of the gammaproteobacterial OM60/NOR5 clade were analysed applying the same methods as developed previously for C. litoralis, so that the obtained results can be compared with existing data. The phylogenetic positions of these strains are as follows: Luminiphilus syltensis (L. syltensis) DSM 22749T is affiliated to the NOR5-1 lineage of the OM60/NOR5 clade and related to the strain HTCC2080, Pseudohaliea rubra (P. rubra) DSM 19751T is closely related to C. litoralis and belongs to the NOR5-3 lineage, whereas C. halotolerans DSM 23344T is associated with the NOR5-3 branch, but does not belong to it . The physiological and genotypic differences between these strains have been described in an accompanying paper by Spring et al. .
Results and discussion
The production of photosynthetic pigments is influenced by the type of carbon source and oxygen availability
Numerous independent experiments were performed to determine the influence of oxygen availability and carbon concentration on pigment expression using media containing various amounts of carbon source and/or different concentrations of oxygen in the head space gas atmosphere. Similar results were obtained upon cultivation in closed serum bottles, if either the oxygen concentration was reduced at a constant substrate concentration or the substrate concentration increased at a constant oxygen concentration. Thus, the pigmentation in these strains depended on the carbon/oxygen balance. For each analysed strain results of a representative experiment are shown in Figure 1B. It can be deduced that in all tested strains pigment expression is repressed when oxygen is limiting growth. The same result was obtained previously with C. litoralis. Hence, the reduction of pigment expression in the presence of growth-limiting oxygen concentrations is a conserved trait in all BChl a-containing members of the OM60/NOR5 clade studied so far. On the other hand, there was some variability in the effect of an oxygen excess or carbon limitation on pigmentation among different strains upon growth in batch cultures. A high oxygen to carbon ratio decreased the production of pigments in C. litoralis, P. rubra and L. syltensis, whereas it had no significant negative effect on the pigmentation of C. halotolerans. Nevertheless, a stimulation of pigment production in the tested strains was never observed by a lowering of the concentrations of carbon sources to 1 – 2 mM in order to imitate oligotrophic growth conditions. In addition, amounts of the essential nutrients ammonium, phosphate and iron were always in excess, which did not seem to have a negative effect on pigment production, at least in batch cultures.
Interestingly, no effect of substrate utilization or oxygen concentration on pigment production was found in several members of the Roseobacter clade that were studied in this respect [10, 11], which may be due to the use of different regulatory pathways or a more stable cellular redox state in these bacteria compared to members of the OM60/NOR5 clade.
Utilization of light for mixotrophic growth depends on the metabolized substrate
The growth response of the tested strains in defined media containing DL-malate as single substrate are shown in Figure 2B, D and F. In all three strains an increase in growth yield could be determined, which was on a dry weight basis around 14% in L. syltensis, 47% in C. halotolerans and 54% in P. rubra. Thus, in cultures of L. syltensis yeast extract stimulated not only the production of photosynthetic pigments, but also light-dependent mixotrophic growth. In P. rubra the stimulatory effect of light on growth with malate as sole carbon source could be partly due to an acceleration of the transportation of this substrate into the cell, which would explain that the generation time was shortened by half in cultures growing with malate in the light compared to darkness. Thus, in some strains of the OM60/NOR5 clade the energy generated from light could be partly used to facilitate the uptake of distinct substrates, instead of enhancing their assimilation as assumed for most aerobic anoxygenic photoheterotrophic bacteria studied so far .
For L. syltensis and P. rubra also growth curves with pyruvate were determined, because in both strains this substrate was more efficiently metabolized than malate (data not shown). However, no significant light-dependent increase in growth yield was found for L. syltensis and P. rubra upon incubation with pyruvate as sole carbon source, albeit photosynthetic pigments in amounts comparable to mixotrophically growing strains were produced, so that it can be assumed that during utilization of pyruvate no energy could be gained from the harvested light. Obviously, the metabolized substrate has a large impact on the efficiency of mixotrophic growth in members of the OM60/NOR5 clade, whereas the abundance of photosynthetic pigments does not correlate directly with the energy yield of photophosphorylation. Interestingly, no significant relationship between the cellular BChl a concentration and the photosynthetic competence in aerobic photoheterotrophic alphaproteobacteria could be found in a recent study by Sato-Takabe et al.  using a fluorescence induction and relaxation technique.
Effect of light on pigment production is variable among strains
The ratio of photosynthetic pigments depends on the redox conditions
Possible influence of terminal oxidases on the regulation of pigment production
Complex substrates, the stringent response and the concept of oligotrophy
In L. syltensis pigment expression and photophosphorylation could be stimulated by the addition of yeast extract, whereas in P. rubra and C. litoralis complex nutrients had a negative effect. An ambiguous situation was obtained in C. halotolerans, because pigment expression could be stimulated by the combination of yeast extract and Tween 80, whereas yeast extract alone had a negative effect. It is known that yeast extract contains various compounds of different reduction levels, hence it is possible that L. syltensis utilizes other yeast extract derived carbon sources than C. litoralis or that different metabolic pathways are used for the same substrates leading to different intracellular redox states affecting regulatory pathways controlling pigment production. An excess of complex nutrients influences not only the level of pigmentation, but affects also the tendency for aggregation and cell morphology of the studied strains  and it seems that the intensity of these effects correlates with the observed repression of pigment production, which is most pronounced in C. litoralis and P. rubra. Thus, this finding implies the participation of a global regulatory network in the expression of photosynthesis genes in some members of the OM60/NOR5 clade. In most gammaproteobacteria a deprivation of amino acids or carbon starvation leads to a global change in gene expression known as stringent response, which is mediated by the enzymes RelA and SpoT . In fact, a stimulating effect of the guanosine 3′, 5′-bisdiphosphate (ppGpp) related stringent response on phototrophic growth of the alphaproteobacterium Rhodobacter capsulatus has been revealed . Hence, various effects of the stringent response on the expression of photosynthetic pigments in members of the OM60/NOR5 clade could offer an explanation for the observed differences upon growth in nutrient rich complex media.
The observation that supplementation of media with complex nutrients in amounts of around 1 g/l stimulated the production of photosynthetic pigments in several strains of the OM60/NOR5 clade contradicts their designation as obligate oligotrophic photoheterotrophs as originally proposed by Cho et al. . In general, a distinction of marine bacteria in obligate or facultative oligotrophs on the one hand and copiotrophs on the other hand is quite difficult to verify. According to the definition of Ishida et al.  obligate oligotrophs cannot grow in media containing above around 0.3 g/l carbon, which would be an inherent characteristic of these strains. However, inhibition of growth on nutrient rich media may have several reasons, especially if strains are analysed that were freshly isolated from the environment. In most cases the optimal growth conditions and traits of novel isolates are unknown, so that a lack of growth in nutrient rich media may be caused by impurities of highly concentrated substrates, harmful metabolic endproducts, activation of lysogenic phages or simply inappropriate incubation conditions. It can be assumed that most bacteria isolated from seawater inhabit oligotrophic niches, so that the observed differences of various marine bacteria in the response to high nutrient concentrations could be just based on variations of the time period required to adapt to the elevated nutrient concentrations used in laboratory media to achieve high growth yields. The existing distinguishable growth response of most members of the Roseobacter clade on the one hand, which are easily isolated and cultivated on nutrient rich media and the more fastidious representatives of the OM60/NOR5 clade on the other hand could thus be based on effects reflecting different strategies of gene regulation and adaptation. A similar conclusion was drawn earlier by Schut et al. , who stated that obligate oligotrophy can be understood as a transient characteristic observed in cells that are taken directly from an extremely substrate-limited natural environment.
We propose that the specific regulation of photosynthesis genes in members of the OM60/NOR5 clade depends on a redox-sensitive repressor encoded by the ppsR gene, which has been detected within the photosynthesis superoperon in most genome-sequenced photoheterotrophic proteobacteria [18, 26, 27], including C. litoralis, L. syltensis and P. rubra (unpublished data). The PpsR dependent regulation could be either independent from other involved regulatory pathways that influence pigment expression or PpsR represents a terminal effector that interacts with various sensors for diverse environmental stimuli, like for instance a single domain BLUF protein sensing blue light or a yet unknown sensor of membrane-bound lipoquinone reduction. Recently, it could be shown that the PpsR repressor of Rhodobacter capsulatus has heme sensing activity . According to this study the binding of free heme to PpsR has an influence on operator affinity, which depends on the target sequence. This effect could explain the linear dependence of the BChl a/spirilloxanthin ratio on the cellular redox state in cells of L. syltensis and C. litoralis. A discrimination between operators controlling bacteriochlorophyll and carotenoid synthesis would be possible, if in L. syltensis and C. litoralis the proportion of PpsR with bound heme is influenced by the cellular redox state.
In addition to the postulated specific regulation by a redox-sensitive regulatory protein a signalling pathway controlling global gene expression might be involved in the expression of photosynthesis genes. An indication for two different modes of regulation could be that in L. syltensis and C. litoralis the ratio of BChl a to spirilloxanthin correlates reliably with the estimated cellular redox state, but is quite independent of the overall level of pigment expression (Figure 4). The proposed global regulation of pigment production could be based for example on the activity of a cbb3-type oxidase which has been shown to control the production of photosynthetic pigments in a Rhodobacter species . Alternatively, the second messenger (p)ppGpp responsible for inducing and maintaining the stringent response in most gammaproteobacteria could promote the expression of photosynthesis genes in response to the limited availability of complex nutrients.
Furthermore, our results indicate that the mechanisms regulating pigmentation in strains from different lineages of aerobic photoheterotrophic gammaproteobacteria are quite similar to the well-studied regulatory pathways in facultatively anaerobic photoheterotrophic purple bacteria . In both cases the intracellular redox state plays a major role in pigment expression and photoheterotrophic growth [19, 20]. The only main difference to the regulation in facultative anaerobic photosynthetic purple bacteria appears to be the absence of an energy-intensive redox-balancing system based on the fixation of carbon dioxide or nitrogen (so far no genes encoding enzymes of both pathways were detected in obligately aerobic anoxygenic photoheterotrophic bacteria), which prevents the decrease of the intracellular redox state to suboptimal levels for photosynthesis under reducing conditions. In conclusion, we postulate that in obligately aerobic anoxygenic photoheterotrophic gammaproteobacteria a decrease of the intracellular redox state is used to sense a surplus of suitable carbon sources, which makes a photosynthetic apparatus redundant. On the other hand, the type of regulation in most BChl a-containing members of the Roseobacter clade seems to be fundamentally different, because in these species the expression level of the photosynthetic apparatus is almost exclusively controlled by light.
Used strains, media and cultivation conditions
The following reference strains were taken from the DSMZ culture collection and used in this study: Luminiphilus syltensis DSM 22749T, Chromatocurvus halotolerans DSM 23344T (= EG19T), Pseudohaliea rubra DSM 19751T (= CM41_15aT) and Congregibacter litoralis DSM 17192T (= KT71T). Pseudohaliea rubra CM41_15aT was deposited in the DSMZ by the Laboratoire Arago, Université Pierre et Marie Curie (Banyuls-sur-Mer, France) under the conditions of a Material Transfer Agreement. For routine cultivation all strains were grown in SYPHC medium at 28°C . Replacing of pyruvate in SYPHC medium with 10 mM DL-malate resulted in SYMHC medium. SYM medium was obtained, if the supplementary amino acids L-histidine and L-cysteine were omitted. The preparation of defined media for growth on single carbon sources and the generation of various gas atmospheres in batch cultures has been described elsewhere [15, 18]. A 40 W incandescent bulb was used as light source for the determination of growth curves in the light. For the illumination of cultures with light of distinct wavelengths LED lamps were used emitting blue, green and red visible light with peak wavelengths of 627, 518 and 466 nm, respectively. All used chemicals were obtained from Sigma-Aldrich (Taufkirchen, Germany) and complex nutrients from DIFCO BBL (Becton Dickinson; Heidelberg, Germany).
Determination of growth, cellular pigmentation and cytochromes
The absorbance values of growing cultures were determined in a Thermo Scientific BioMate 6 split beam UV/visible spectrophotometer using 1 cm light path disposable cuvettes and water as blank. The A660nm reading was used to estimate the cell density. The cellular dry weight of grown cultures was determined by overnight freeze-drying of cell pellets harvested by centrifugation. Expression of the light-harvesting complex in L. syltensis was estimated by determining the A870nm to A660nm ratio, for cultures of C. litoralis and C. halotolerans a ratio of A880nm to A660nm was used and for P. rubra a ratio of A820nm to A660nm. Photosynthetic pigments were extracted from wet cell pellets using a mixture of acetone/methanol (7:2) as described previously . The concentrations of bacteriopheophytin a, bacteriochlorophyll a and spirilloxanthin in the acetone/methanol extracts were determined from the absorbance values obtained at 747, 771 and 475 nm, respectively, using the spectral reconstruction method of van der Rest and Gingras .
The detection and identification of various cytochrome types was done as reported previously .
Semiquantitative detection of transcripts using PCR
RNA was isolated from cultures of C. litoralis DSM 17192T that were grown to early stationary phase under various incubation conditions. A culture volume equivalent to a cell suspension of one ml with an A660nm of approx. 1.0 was diluted with two volumes of RNAprotect Bacteria Reagent (Qiagen; Hilden, Germany), then cells were harvested by centrifugation. The cell pellet was frozen at −20°C overnight and subsequently used for the extraction of RNA using the Qiagen RNeasy Midi Kit including the optional on-column DNase digestion. In most cases this procedure yielded ca. 10 μg of extracted total RNA as determined by photometric analysis at 260 nm. Despite the applied on-column DNase treatment small quantities of genomic DNA could still be detected in the purified RNA samples by PCR amplification. Hence, an additional DNase treatment in solution was applied to obtain DNA-free RNA.
Oligonucleotides used for the amplification of gene fragments from C. litoralis DSM 17192 T with PCR or semiquantitative RT-PCR
Protein encoded by the target gene
Product size (bp)
CAT CAC TTC GGC GAG TTC TT
RNA polymerase omega subunit
AGA AGA TTG CCT TGA GTC CG
GAC AGT CGG TTT GAT TGC AG
CAT GCG GTG TTG TAA GTT GC
AAG CAG ACC GAG TGG ACC TA
Photosynthetic reaction centre cytochrome c subunit
GTG CCT TCT CAG ACT CCG TC
ATA TCC ACT TTG GCA CCA GC
Caa3-type cytochrome c oxidase subunit 1
GTG AAG AGC ACA AGG AAG CC
CTT ATC ACC GTC GTC TGG GT
Cbb3-type cytochrome oxidase CcoN subunit
GTG TAG TGC AGG TGG TGT GG
TR was supported by the DFG Transregio-SFB 51 Roseobacter.
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