The presence of chlorophyll b in Synechocystis sp. PCC 6803 disturbs tetrapyrrole biosynthesis and enhances chlorophyll degradation

Both chlorophyll (Chl) a and b accumulate in the light in a Synechocystis sp. PCC 6803 strain that expresses higher plant genes coding for a light-harvesting complex II protein and Chl a oxygenase. This cyanobacterial strain also lacks photosystem (PS) I and cannot synthesize Chl in darkness because of the lack of chlL. When this PS I-less/chlL^-/lhcb⁺/cao⁺ strain was grown in darkness, small amounts of two unusual tetrapyrroles, protochlorophyllide (PChlide) b and pheophorbide (pheide) b, were identified. Accumulation of PChlide b trailed that of PChlide a by several days, suggesting that PChlide a is an inefficient substrate of Chl a oxygenase. The presence of pheide b in this organism suggests a breakdown of Chl b via a pathway that does not involve conversion to a-type pigments. When the PS I-less/chlL^- control strain was grown in darkness, Chl degradation was much slower than in the PS I-less/chlL^-/lhcb⁺/cao⁺ strain, suggesting that the presence of Chl b leads to more rapid turnover of Chl-binding proteins and/or a more active Chl degradation pathway. Levels and biosynthesis kinetics of Chl and of its biosynthetic intermediates are very different in the PS I-less/chlL^-/lhcb⁺/cao⁺ strain versus in the control. Moreover, when grown in darkness for 14 days, upon the addition of δ-aminolevulinic acid, the level of magnesium-protoporphyrin IX increased 60-fold in the PS I-less/chlL^-/lhcb⁺/cao⁺ strain (only ∼2-fold in the PS I-less/chlL^- control strain), whereas the PChlide and protoheme levels remained fairly constant. We propose that a b-type PChlide, Chl, or pheide in the PS I-less/chlL^-/lhcb⁺/cao⁺ strain may bind to tetrapyrrole biosynthesis regulatory protein(s) (for example, the small Cab-like proteins) and thus affect the regulation of this pathway.