Stereochemical conversion of C3‐vinyl group to 1‐hydroxyethyl group in bacteriochlorophyll c by the hydratases BchF and BchV: adaptation of green sulfur bacteria to limited‐light environments

Abstract

SummaryPhotosynthetic green sulfur bacteria inhabit anaerobic environments with very low-light conditions. To adapt to such environments, these bacteria have evolved efficient light-harvesting antenna complexes called as chlorosomes, which comprise self-aggregated bacteriochlorophyll c in the model green sulfur, bacterium Chlorobaculum tepidum. The pigment possess a hydroxy group at the C3 1 position that produces a chiral center with R-or S-stereochemistry and the C3 1 -hydroxy group serves as a connecting moiety for the self-aggregation. Chlorobaculum tepidum carries the two possible homologous genes for C3-vinyl hydratase, bchF and bchV. In the present study, we constructed deletion mutants of each of these genes. Pigment analyses of the bchFinactivated mutant, which still has BchV as a sole hydratase, showed higher ratios of S-epimeric bacteriochlorophyll c than the wild-type strain. The heightened prevalence of S-stereoisomers in the mutant was more remarkable at lower light intensities and caused a red shift of the chlorosomal Q y absorption band leading to advantages for light-energy transfer. In contrast, the bchV-mutant possessing only BchF showed a significant decrease of the S-epimers and accumulations of C3-vinyl BChl c species. As transcriptional level of bchV was upregulated at lower light intensity, the Chlorobaculum tepidum adapted to low-light environments by control of the bchV transcription.

Stereoselective C3‐substituent modification and substrate channeling by oxidoreductase BchC in bacteriochlorophyll a biosynthesis

“…The BchF and BchV enzymes from Cba. tepidum were prepared as described previously , and soluble fraction of the lysate of E. coli transformed to produce BchF or BchV enzymes was used in this experiment. BchF or BchV in 50 m m Tris‐HCl buffer (pH 7.8) was incubated with BchC on ice for 10 min, then used for the coupled assays.…”

“…One is dehydrogenation of the C7=C8 double bond by Chlide a oxidoreductase (COR), resulting in the formation of a bacteriochlorin ring . The other two steps are hydration of the 3‐vinyl (3V) group by BchF (hydratase) and oxidation of the resultant 3‐(1‐hydroxyethyl) (3HE) group by BchC (oxidoreductase) to introduce the 3‐acetyl (3Ac) group (3‐CH=CH 2 → 3‐C*H(OH)CH 3 → 3‐COCH 3 ) . Since the 3HE group introduced by BchF becomes a substrate for oxidation by BchC, the order cannot be inverted; BchF‐catalyzed hydration must be followed by BchC‐catalyzed oxidation.…”

“…tepidum producing BChl c besides BChl a carries two homologs of BchF in purple bacterium . BChl c biosynthesis requires the 3V‐hydration step and the second BchF homolog named BchV has been considered as a BChl c ‐specific hydratase .…”

BciD Is a Radical S-Adenosyl-l-methionine (SAM) Enzyme That Completes Bacteriochlorophyllide e Biosynthesis by Oxidizing a Methyl Group into a Formyl Group at C-7

“…Previous studies showed that one gene in this cluster, cruB, encodes a ␥-carotene cyclase that is essential for the synthesis of ␤-carotene and isorenieratene, carotenoids that are uniquely and nearly universally produced by brown-colored GSB (42). This gene cluster also includes a third homolog of bchF and bchV, genes that encode C-3 vinyl hydratases (21,(27)(28)(29).…”

“…BchQ and BchR methylate the resulting product at the C-8 2 and C-12 1 positions, respectively, to produce a family of related homologs (18). These methylation homologs are then hydroxylated at C-3 1 by BchF or BchV to produce bacteriochlorophyllide (BChlide) d (21,(27)(28)(29), and in BChl c-producing strains, they are subsequently methylated by BchU at C-20 to produce BChlide c homologs (12,30,31). Finally, the BChlide c or BChlide d homologs are esterified with farnesol pyrophosphate by BchK to produce BChl c or BChl d homologs with differing numbers of methyl groups (20).…”