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

Abstract

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...

Variations in the Rhythms of Respiration and Nitrogen Fixation in Members of the Unicellular Diazotrophic Cyanobacterial Genus Cyanothece

“…However, some of the strains (Tables I and II) showed significantly higher nitrogenase activity, suggesting that glycerol is being metabolized in the cells and can be used as a source of reductants. On a similar note, Feng et al (2010) showed that Cyanothece sp. ATCC 51142 could metabolize Glc, but this carbon source did not contribute to biomass production.…”

“…Unlike Cyanothece sp. ATCC 51142, which utilizes glycerol for the production of biomass (Feng et al, 2010), the other Cyanothece spp. strains did not exhibit any significant difference in growth rate when grown in the presence of glycerol (data not shown).…”

High rates of photobiological H2 production by a cyanobacterium under aerobic conditions

“…4b). In this context, we have recently shown that Cyanothece 51142 uses glycerol as the sole carbon source when cells are grown under photomixotrophic conditions in the presence of glycerol 25 .…”

Dissolved Organic Matter Influences N2 Fixation in the New Caledonian Lagoon (Western Tropical South Pacific)

“…As evidence accumulates, it seems that the ability of using DOM as an alternative source of nutrients under limiting situations is common in various planktonic groups (Stoecker et al, 2017). Among marine diazotrophs, unicellular cyanobacteria such as Cyanothece have been reported to grow on glycerol (Feng et al, 2010), and filamentous diazotrophs such as Trichodesmium may obtain as much carbon from amino acids assimilation as from CO 2 fixation in the field . Non-cyanobacterial and nonphotosynthetic diazotrophs require external sources of DOM as energy sources (Riemann et al, 2010).…”