Mechanisms of inorganic carbon acquisition in twoEuglenaspecies

Abstract

The mechanism of inorganic carbon uptake was examined in Euglena gracilis Klebs. and the acidophilic species Euglena mutabilis Schmitz. Both species, whether grown in acidic (pH 3.5) or alkaline (pH 7.5) media lack external carbonic anhydrase. Acid-grown E. gracilis was shown to have no capacity for bicarbonate transport, but transport was induced on transfer to alkaline medium (pH 7.5) in the light over a period of 8 h. In contrast, acid-grown E. mutabilis appears to have no capacity for bicarbonate transport even at neutral pH. The overall internal pH of the cells was determined by equilibration with 14C-labelled benzoic acid over the pH range 3.5–5.0 and with 14C-labelled 5,5-dimethyloxazolidine-2,4-dione over the range pH 5.5–7.5. The acidophilic species maintains an internal pH range of 6.6–6.8 in an external pH range of 3.5–5.5, whereas the acid-tolerant species E. gracilis maintains a neutral internal pH in an external pH range of 3.5–7.5. Measurement, by mass spectrometry, of the fluxes of CO2 and O2 in photosynthesizing cells at pH 3.5 demonstrated a rapid uptake of CO2 by both species that was completely blocked by iodoacetamide, an inhibitor of CO2 fixation. Uptake of CO2 by E. gracilis, grown at pH 7.5, was not completely inhibited by iodoacetamide and O2 evolution was sustained when the cells reached the CO2 compensation concentration, indicating a direct uptake of bicarbonate. These data indicate that the acidophilic species, E. mutabilis, takes up CO2 by diffusion, whereas the acid-tolerant species, E. gracilis, takes up CO2 by diffusion at acid pH levels but has some capacity for active bicarbonate uptake when grown at alkaline pH levels.Key words: acidophilic alga, acidotolerant alga, bicarbonate uptake, CO2 uptake, Euglena gracilis, Euglena mutabilis, internal pH.

High-CO2 Response Mechanisms in Microalgae

“…CCM can be induced by an artificially produced strong limitation in CO 2 supply in large-scale photobioreactors where dCO 2 is consumed via photosynthesis (Yun & Park, 1997). In some microalgae, the supply of CO 2 , not bicarbonate, is strongly limited at alkaline pHs in closed culture systems and such a limitation may be a factor or signal for inducing CCM (Colman & Balkos, 2005;Diaz & Maberly, 2009;Verma et al, 2009). The euglenophyte Euglena mutabilis and an acid-tolerant strain of Chlamydomonas do not induce CCM under any conditions (Balkos & Colman, 2007;Colman & Balkos, 2005), suggesting that photosynthetic carbon fixation is not limited by CO 2 supply even under ambient atmospheric conditions.…”

“…In some microalgae, the supply of CO 2 , not bicarbonate, is strongly limited at alkaline pHs in closed culture systems and such a limitation may be a factor or signal for inducing CCM (Colman & Balkos, 2005;Diaz & Maberly, 2009;Verma et al, 2009). The euglenophyte Euglena mutabilis and an acid-tolerant strain of Chlamydomonas do not induce CCM under any conditions (Balkos & Colman, 2007;Colman & Balkos, 2005), suggesting that photosynthetic carbon fixation is not limited by CO 2 supply even under ambient atmospheric conditions. These results indicate that there is species-specific variation in the induction mechanism of CCM depending on physiological and ecological conditions (for review, see Giordano et al, 2005;Raven, 2010).…”

“…Photosynthesis in acidic environment, the influence by ocean acidification, and the effect of O 2 on photorespiration are also deeply associated with high-CO 2 -induced phenomena. Some microalgal species have been isolated mainly from acidic environments where only CO 2 is predominant and supplied to algal cells as a substrate for photosynthesis (Balkos & Colman, 2007;Colman & Balkos, 2005;Diaz & Maberly, 2009;Verma et al, 2009; for review see Raven, 2010). Three synurophyte algae, Synura petersenii, Synura uvella, and Tessellaria volvocina, have been studied in detail for the DIC uptake mechanism and show unique photosynthetic properties (Bhatti & Coleman, 2008).…”

Inorganic carbon acquisition by eukaryotic algae: four current questions

“…By contrast, the characterization of another species as having a CCM, valuable though the information is, could be characterized as finding 'more of the same' unless the CCM is further characterized since eukaryotic CCMs are polyphyletic (Badger et al 1998;Giordano et al 2005;Falkowski and Raven 2007). Colman and Balkos (2005) examined two species of the euglenophycean Euglena. While Euglena mutabilis showed no evidence of a CCM under any condition and, therefore, always depended on diffusive exchange of CO 2 , the acid-tolerant Euglena gracilis expressed a CCM based on active influx of HCO 3 -when grown at alkaline pH values.…”

“…the treboxophycean Coccomyxa, the euglenophycean Euglena and the ulvophycean Caulerpa) have some species invariably relying on diffusive fluxes of CO 2 while others can express CCMs Colman 2005, 2008;Colman and Balkos 2005;Raven et al 2005a;Kevekordes et al 2006;Diaz and Maberly 2009;Maberly et al 2009). Although CO 2 diffusion to Rubisco is probably the ancestral state for eukaryotic algae, it is clear that some cases of diffusive CO 2 exchange are derived: an example is the species of Caulerpa with one of more of C 3 -like photosynthetic gas exchange, the absence of a pyrenoid and a very negative d 13 C values (i.e.…”