Anaerobic energy dissipation by glycosylated carotenoids in the green sulfur bacterium Chlorobaculum tepidum

Abstract

Carotenoids are linear polyenes and universal pigment molecules that support natural photosynthesis by light harvesting and photoprotection. Some carotenoids are glycosylated at the end of their polyene backbone, which does not clearly affect their photochemical and optical properties. In green sulfur bacteria (GSBs), which are obligate photosynthetic anaerobes, carotenoid glycosides are specifically bound to the photosynthetic reaction center (RC) complex. The other non-glycosylated carotenoids with the same polyene backbone are located in the chlorosome, which is an extra-large light-harvesting organelle. The current study isolated a mutant strain, ΔcruC, that lacks the gene responsible for carotenoid glycosylation in the model GSB species Chlorobaculum tepidum. We examined the effects of the mutation on photosynthetic growth and energy transfer reactions. The ΔcruC mutant cells grew significantly slower than the wild-type (WT) cells under high light conditions. Energy transfer reactions were delayed between bacteriochlorophyll (BChl) a of the RC complex, despite no obvious effect observed on the organization of photosynthetic apparatuses. Kinetic analyses revealed that almost half of the excitation energy of BChl a was constitutively quenched in the WT RC complex, even under a strictly anaerobic environment. The ΔcruC mutant strain phenotype clearly indicates that glycosylated carotenoids serve as energy dissipating, not light harvesting, pigments in C. tepidum. The current understanding of natural photosynthesis is that any energy dissipation mechanisms should be to avoid generation of reactive oxygen species, which are sensitized by the triplet-excited state of chlorophylls. However, these results indicate that carotenoid glycosides found in GSB may also serve a previously unidentified function for anaerobic energy dissipation.