Phylogeny of Anoxygenic Photosynthesis Based on Sequences of Photosynthetic Reaction Center Proteins and a Key Enzyme in Bacteriochlorophyll Biosynthesis, the Chlorophyllide Reductase

Photosynthesis is a key process for the establishment and maintenance of life on earth, and it is manifested in several major lineages of the prokaryote tree of life. The evolution of photosynthesis in anoxygenic photosynthetic bacteria is of major interest as these have the most ancient roots of photosynthetic systems. The phylogenetic relations between anoxygenic phototrophic bacteria were compared on the basis of sequences of key proteins of the type-II photosynthetic reaction center, including PufLM and PufH (PuhA), and a key enzyme of bacteriochlorophyll biosynthesis, the light-independent chlorophyllide reductase BchXYZ. The latter was common to all anoxygenic phototrophic bacteria, including those with a type-I and those with a type-II photosynthetic reaction center. The phylogenetic considerations included cultured phototrophic bacteria from several phyla, including Proteobacteria (138 species), Chloroflexi (five species), Chlorobi (six species), as well as Heliobacterium modesticaldum (Firmicutes), Chloracidobacterium acidophilum (Acidobacteria), and Gemmatimonas phototrophica (Gemmatimonadetes). Whenever available, type strains were studied. Phylogenetic relationships based on a photosynthesis tree (PS tree, including sequences of PufHLM-BchXYZ) were compared with those of 16S rRNA gene sequences (RNS tree). Despite some significant differences, large parts were congruent between the 16S rRNA phylogeny and photosynthesis proteins. The phylogenetic relations demonstrated that bacteriochlorophyll biosynthesis had evolved in ancestors of phototrophic green bacteria much earlier as compared to phototrophic purple bacteria and that multiple events independently formed different lineages of aerobic phototrophic purple bacteria, many of which have very ancient roots. The Rhodobacterales clearly represented the youngest group, which was separated from other Proteobacteria by a large evolutionary gap.

Complete Genome Sequence of the Photoautotrophic and Bacteriochlorophyll e-Synthesizing Green Sulfur Bacterium Chlorobaculum limnaeum DSM 1677T

ABSTRACT Chlorobaculum limnaeum DSM 1677T is a mesophilic, brown-colored, chlorophototrophic green sulfur bacterium that produces bacteriochlorophyll e and the carotenoid isorenieratene as major pigments. This bacterium serves as a model organism in molecular research on photosynthesis, sulfur metabolism, and bacteriochlorophyll biosynthesis. We report here the complete genome sequence.

Three classes of oxygen-dependent cyclase involved in chlorophyll and bacteriochlorophyll biosynthesis

The biosynthesis of (bacterio)chlorophyll pigments is among the most productive biological pathways on Earth. Photosynthesis relies on these modified tetrapyrroles for the capture of solar radiation and its conversion to chemical energy. (Bacterio)chlorophylls have an isocyclic fifth ring, the formation of which has remained enigmatic for more than 60 y. This reaction is catalyzed by two unrelated cyclase enzymes using different chemistries. The majority of anoxygenic phototrophic bacteria use BchE, an O2-sensitive [4Fe-4S] cluster protein, whereas plants, cyanobacteria, and some phototrophic bacteria possess an O2-dependent enzyme, the major catalytic component of which is a diiron protein, AcsF. Plant and cyanobacterial mutants in ycf54 display impaired function of the O2-dependent enzyme, accumulating the reaction substrate. Swapping cyclases between cyanobacteria and purple phototrophic bacteria reveals three classes of the O2-dependent enzyme. AcsF from the purple betaproteobacterium Rubrivivax (Rvi.) gelatinosus rescues the loss not only of its cyanobacterial ortholog, cycI, in Synechocystis sp. PCC 6803, but also of ycf54; conversely, coexpression of cyanobacterial cycI and ycf54 is required to complement the loss of acsF in Rvi. gelatinosus. These results indicate that Ycf54 is a cyclase subunit in oxygenic phototrophs, and that different classes of the enzyme exist based on their requirement for an additional subunit. AcsF is the cyclase in Rvi. gelatinosus, whereas alphaproteobacterial cyclases require a newly discovered protein that we term BciE, encoded by a gene conserved in these organisms. These data delineate three classes of O2-dependent cyclase in chlorophototrophic organisms from higher plants to bacteria, and their evolution is discussed herein.

Elucidation of the preferred routes of C8-vinyl reduction in chlorophyll and bacteriochlorophyll biosynthesis

The step in (bacterio)chlorophyll biosynthesis at which the vinyl group at the C8 position is reduced, forming an ethyl group, has been disputed. Results from species utilizing unrelated reductases suggest that C8-vinyl chlorophyllide is the preferred substrate for both enzymes.