The occurrence of the chloroplast pyrenoid is correlated with the activity of a CO₂-concentrating mechanism and carbon isotope discrimination in lichens and bryophytes

Abstract

The organic-matter carbon isotope discrimination (Δ) of lichens with a wide range of photobiont and/or cyanobiont associations was used to determine the presence or absence of a carbon-concentrating mechanism (CCM). Two groups were identified within the lichens with green algal photobionts. One group was characterised by low, more C₄-like Δ values (Δ < 15‰), the other by higher, more C₃-like Δ values (Δ > 18‰). Tri-partite lichens (lichens with a green alga as the primary photobiont and cyanobacteria within internal or external cephalodia) occurred in both groups. All lichens with cyanobacterial photobionts had low Δ values (Δ < 15‰). The activity of the CCM, organic-matter Δ values, on-line Δ values and gas-exchange characteristics correlated with the presence of a pyrenoid in the algal chloroplast. Consistent with previous findings, lichens with Trebouxia as the primary photobiont possessed an active CCM while those containing Coccomyxa did not. Organic Δ values for lichens with Stichococcus as the photobiont varied between 11 and 28‰. The lichen genera Endocarpon and Dermatocarpon (Stichococcus + pyrenoid) had C₄-like organic Δ values (Δ = 11 to 16.5‰) whereas the genus Chaenotheca (Stichococcus — pyrenoid) was characterised by high C₃-like Δ values (Δ = 22 to 28‰), unless it associated with Trebouxia (Δ = 16‰). Gas-exchange measurements demonstrated that Dermatocarpon had an affinity for CO₂ comparable to those species which possessed the CCM, with K_0.5 = 200–215 μ1 · 1⁻¹, compensation point (Γ) = 45–48 μl · l⁻¹, compared with K_0.5 = 195 μ1 · 1⁻¹, Γ = 44μ1 · 1⁻¹ for Trebouxioid lichens. Furthermore, lichens with Stichococcus as their photobiont released a small pool (24.2 ± 1.9 to 34.2 ± 2.5 nmol · mg⁻¹ Chl) of inorganic carbon similar to that released by Trebouxioid lichens [CCM present, dissolved inorganic carbon (DIC) pool size = 51.0 ± 2.8 nmol · mg⁻¹ Chl]. Lichens with Trentepohlia as photobiont did not possess an active CCM, with high C₃-like organic Δ values (Δ = 18‰ to 23‰). In particular, Roccella phycopsis had very high on-line Δ values (Δ = 30 to 33‰), a low affinity for CO₂ (K_0.5 = 400 μ1 · 1⁻¹,Γ = 120 μ1 · ⁻¹) and a negligible DIC pool. These responses were comparable to those from lichens with Coccomyxa as the primary photobiont with Nostoc in cephalodia (organic Δ = 17 to 25‰, on-line Δ = 16 to 21‰, k_0.5 = 388 μ1 · 1⁻¹, Γ = 85 μ1 · 1⁻¹, DIC pool size = 8.5 ± 2.4 nmol · mg⁻¹ Chl). The relative importance of refixation of respiratory CO₂ and variations in source isotope signature were considered to account for any variation between on-line and organic Δ. Organic Δ was also measured for species of Anthocerotae and Hepaticae which contain pyrenoids and/or Nostoc enclosed within the thallus. The results of this screening showed that the pyrenoid is correlated with low, more C₄-like organic Δ values (Δ = 7 to 12‰ for members of the Anthocerotae with a pyrenoid compared with Δ = 17 to 28‰ for the Hepaticae with and without Nostoc in vesicles) and confirms that the pyrenoid plays a fundamental role in the functioning of the CCM in microalgal photobionts and some bryophytes.