Interaction of fructose with the glucose permease of the cyanobacterium Synechocystis sp. strain PCC 6803

Flores, Enrique; Schmetterer, Georg

doi:10.1128/jb.166.2.693-696.1986

Cited by 53 publications

(61 citation statements)

References 17 publications

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“…It is worth noting that the high-affinity K s constant of Pro1404 for glucose is 3,000-fold lower than the one described for the glucose transporters of model freshwater cyanobacteria, with K s constants in the millimolar range (3,19,20).…”

Section: Resultsmentioning

confidence: 99%

Prochlorococcus can use the Pro1404 transporter to take up glucose at nanomolar concentrations in the Atlantic Ocean

Muñoz-Marín

Luque

Zubkov

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

115

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Prochlorococcus is responsible for a significant part of CO 2 fixation in the ocean. Although it was long considered an autotrophic cyanobacterium, the uptake of organic compounds has been reported, assuming they were sources of limited biogenic elements. We have shown in laboratory experiments that Prochlorococcus can take up glucose. However, the mechanisms of glucose uptake and its occurrence in the ocean have not been shown. Here, we report that the gene Pro1404 confers capability for glucose uptake in Prochlorococcus marinus SS120. We used a cyanobacterium unable to take up glucose to engineer strains that express the Pro1404 gene. These recombinant strains were capable of specific glucose uptake over a wide range of glucose concentrations, showing multiphasic transport kinetics. The K s constant of the high affinity phase was in the nanomolar range, consistent with the average concentration of glucose in the ocean. Furthermore, we were able to observe glucose uptake by Prochlorococcus in the central Atlantic Ocean, where glucose concentrations were 0.5-2.7 nM. Our results suggest that Prochlorococcus are primary producers capable of tuning their metabolism to energetically benefit from environmental conditions, taking up not only organic compounds with key limiting elements in the ocean, but also molecules devoid of such elements, like glucose.high-affinity glucose transport | marine cyanobacteria | multiphasic uptake kinetics C yanobacteria is a phylum of the bacterial domain distinguishable by their unique capacity to perform oxygenic photosynthesis. This process, which relies on the existence of two photosystems and a chain of electron transporters, enables these organisms to use light energy and electrons from water to produce reductant molecules and fix atmospheric CO 2 to synthesize carbon compounds. Cyanobacteria probably arose on Earth billions of years ago (1), and prolonged evolutionary divergence has made them very diverse in terms of morphology, metabolism, and lifestyle.

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Section: Resultsmentioning

confidence: 99%

Prochlorococcus can use the Pro1404 transporter to take up glucose at nanomolar concentrations in the Atlantic Ocean

Muñoz-Marín

Luque

Zubkov

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

115

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“…The R values of all key amino acids were below 0.05 for both nitrogen-fixation and nitratesufficient conditions, suggesting that a large fraction of the carbon in the biomass had originated from CO 2 fixation. In contrast, glucose is the most favourable carbon source for Synechocystis species (Yang et al, 2002), and the R values ( Baalen, 1978;Flores & Schmetterer, 1986;Schmetterer, 1990). So far, the presence of a glucose transporter in Cyanothece 51142 has not been rigorously verified.…”

Section: Discussion Carbon Substrate Utilization and Regulationmentioning

confidence: 99%

Mixotrophic and photoheterotrophic metabolism in Cyanothece sp. ATCC 51142 under continuous light

et al. 2010

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The unicellular diazotrophic cyanobacterium Cyanothece sp. ATCC 51142 (Cyanothece 51142) is able to grow aerobically under nitrogen-fixing conditions with alternating light-dark cycles or continuous illumination. This study investigated the effects of carbon and nitrogen sources on Cyanothece 51142 metabolism via 13 C-assisted metabolite analysis and biochemical measurements. Under continuous light (50 mmol photons m "2 s "1 ) and nitrogen-fixing conditions, we found that glycerol addition promoted aerobic biomass growth (by twofold) and nitrogenasedependent hydrogen production [up to 25 mmol H 2 (mg chlorophyll) "1 h "1 ], but strongly reduced phototrophic CO 2 utilization. Under nitrogen-sufficient conditions, Cyanothece 51142 was able to metabolize glycerol photoheterotrophically, and the activity of light-dependent reactions (e.g. oxygen evolution) was not significantly reduced. In contrast, Synechocystis sp. PCC 6803 showed apparent mixotrophic metabolism under similar growth conditions. Isotopomer analysis also detected that Cyanothece 51142 was able to fix CO 2 via anaplerotic pathways, and to take up glucose and pyruvate for mixotrophic biomass synthesis. INTRODUCTIONRising concerns about global warming due to the greenhouse effect have renewed research focused on the biological capture of CO 2 . Cyanobacteria have versatile metabolic capabilities, which allow them to grow under autotrophic, heterotrophic and mixotrophic conditions (Bottomley & Van Baalen, 1978;Eiler, 2006;Yang et al., 2002). More importantly, some cyanobacteria can capture solar energy to fix nitrogen and generate H 2 , thereby serving as a source of biofertilizer and biofuel, while simultaneously consuming atmospheric CO 2 (Bernat et al., 2009;Dutta et al., 2005;Fay, 1992;Madamwar et al., 2000;Tamagnini et al., 2007;Tuli et al., 1996). Cyanothece sp. ATCC 51142 (Cyanothece 51142), a unicellular diazotrophic cyanobacterium, is able to grow aerobically under nitrogen-fixing conditions and has been recognized as contributing to the marine nitrogen cycle. The recent sequencing of the Cyanothece 51142 genome and its transcriptional analysis have uncovered the diurnally oscillatory metabolism of the bacterium in alternating light-dark cycles (photosynthesis during the day and nitrogen fixation at night) (Stöckel et al., 2008;Toepel et al., 2008;Welsh et al., 2008). In general, cyanobacteria use spatial or temporal separation of oxygen-sensitive nitrogen fixation and oxygen-evolving photosynthesis as a strategy for diazotrophic growth (Benemann & Weare, 1974;Fay, 1992). Interestingly, Cyanothece 51142 demonstrates simultaneous N 2 fixation and O 2 evolution under continuous-light conditions, though it appears to be unicellular (Colon-Lopez et al., 1997;Huang & Chow, 1986). For example, a recent study of the transcriptional and translational regulation of continuously illuminated Cyanothece has revealed a strong synthesis capability for nitrogenase and circadian expression of 10 % of its genes (Toepel et al., 2008). Furthermore, Cyanothece str...

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“…The addition of OMG (1 mM) or 6-deoxy-D-glucose (1 mM) to a low-C02- grown culture had no effect on the subsequent rate of bicarbonate uptake. Fructose, although capable of supporting the photoheterotrophic growth of many cyanobacteria (25), is inhibitory for Synechocystis PCC 6803 (6). The evidence suggests that fructose is transported into the cells via the glucose transporter (6,30).…”

Section: Chemicalsmentioning

confidence: 98%

“…Fructose, although capable of supporting the photoheterotrophic growth of many cyanobacteria (25), is inhibitory for Synechocystis PCC 6803 (6). The evidence suggests that fructose is transported into the cells via the glucose transporter (6,30). Toxicity may arise from the lethal synthesis and accumulation ofphosphorylated intermediates that cannot be further metabolized.…”

Section: Chemicalsmentioning

confidence: 98%

Bicarbonate Concentration by Synechocystis PCC6803

Bloye¹,

Silman²,

Mann³

et al. 1992

Plant Physiol.

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The ability of the cyanobacterium Synechocystis PCC6803 to transport inorganic carbon in the form of bicarbonate rapidly decreased following a shift from bicarbonate-limited growth to either excess bicarbonate supply or to photoheterotrophic growth on glucose. Nonmetabolizable analogs of glucose did not exert this effect. The rate at which the bicarbonate uptake rate declined was too rapid to be accounted for by dilution of the activity by culture growth and suggested that posttranslational modification may be involved. Several proteins that were unphosphorylated during bicarbonate-limited growth became phosphorylated during the shifts to high CO2 conditions and to photoheterotrophic growth. A similar alteration in the profile of phosphopolypeptides was observed following a shift into the dark. The changes in protein phosphorylation were not blocked by chloramphenicol or rifampicin.The primary metabolic mode of cyanobacteria is photoautotrophy, although some species are also capable of photoheterotrophic and/or chemoheterotrophic growth at the expense of one or more carbohydrates, such as glucose and fructose (25). The affinity of cyanobacterial Rubiscos for CO2 is relatively low; in the presence of 02 the effective Km (C02) is about 600 ,M (21). Growth of many species of cyanobacteria, although not all (1O), under conditions of low CO2 concentration results in the induction of a bicarbonate-concentrating system (2,14). A number of changes in polypeptide composition are observed during adaptation to growth under low CO2 conditions (18). The system operates to increase the intracellular concentration of CO2 that is available to Rubisco so that the enzyme functions at close to CO2 saturation (2, 9). The role and location of carbonic anhydrase has been the subject of much speculation and a recent model has located carbonic anhydrase and Rubisco activity exclusively in the carboxysome (24). Recent work by Price and Badger (22,23) indicated that carbonic anhydrase is probably located within the carboxysomes and converts bicarbonate (the species transported) to CO2 within a relatively gas-tight environment ( 14). requiring phenotype, because CO2 is now partitioned away from Rubisco by the carboxysome coat (22).The concentration of Ci2 within the cell is an energydemanding process, and, consequently, one would expect it to be tightly regulated. In particular, it is pertinent to ask whether other nutritional factors apart from the CO2 regimen can affect the expression of the Ci-concentrating system and also whether the system is specifically inactivated during transitions to conditions under which Ci transport is no longer necessary. In this study, the effect of photoheterotrophic growth on the bicarbonate transport system and the possible role of protein phosphorylation in adapting to altered growth conditions are investigated. MATERIALS AND METHODS Maintenance of and Growth of Cyanobacterial CulturesStock cultures of Synechocystis PCC 6803 were routinely maintained on BG 11 agar slopes (25) containing 1.5% (w/...

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Interaction of fructose with the glucose permease of the cyanobacterium Synechocystis sp. strain PCC 6803

Cited by 53 publications

References 17 publications

Prochlorococcus can use the Pro1404 transporter to take up glucose at nanomolar concentrations in the Atlantic Ocean

Prochlorococcus can use the Pro1404 transporter to take up glucose at nanomolar concentrations in the Atlantic Ocean

Mixotrophic and photoheterotrophic metabolism in Cyanothece sp. ATCC 51142 under continuous light

Bicarbonate Concentration by Synechocystis PCC6803

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