Evolution of a new chlorophyll metabolic pathway driven by the dynamic changes in enzyme promiscuous activity

• Published in: Plant and cell physiology Vol. 55; no. 3; pp. 593 - 603
• Main Authors: Ito, Hisashi, Tanaka, Ayumi
• Format: Journal Article
• Language: English
• Published: Japan 01.03.2014
• Subjects: Biological Evolution; Chlorophyll - metabolism; Cyanobacteria - metabolism; Synechocystis - metabolism; Vinyl Compounds - metabolism; Promiscuous activity; Chlorophyll biosynthesis; Pathway evolution; Synechocystis; Divinyl chlorophyll
• ISSN: 0032-0781; 1471-9053
• DOI: 10.1093/pcp/pct203

Organisms generate an enormous number of metabolites; however, the mechanisms by which a new metabolic pathway is acquired are unknown. To elucidate the importance of promiscuous enzyme activity for pathway evolution, the catalytic and substrate specificities of Chl biosynthetic enzymes were examined. In green plants, Chl a and Chl b are interconverted by the Chl cycle: Chl a is hydroxylated to 7-hydroxymethyl chlorophyll a followed by the conversion to Chl b, and both reactions are catalyzed by chlorophyllide a oxygenase. Chl b is reduced to 7-hydroxymethyl chlorophyll a by Chl b reductase and then converted to Chl a by 7-hydroxymethyl chlorophyll a reductase (HCAR). A phylogenetic analysis indicated that HCAR evolved from cyanobacterial 3,8-divinyl chlorophyllide reductase (DVR), which is responsible for the reduction of an 8-vinyl group in the Chl biosynthetic pathway. In addition to vinyl reductase activity, cyanobacterial DVR also has Chl b reductase and HCAR activities; consequently, three of the four reactions of the Chl cycle already existed in cyanobacteria, the progenitor of the chloroplast. During the evolution of cyanobacterial DVR to HCAR, the HCAR activity, a promiscuous reaction of cyanobacterial DVR, became the primary reaction. Moreover, the primary reaction (vinyl reductase activity) and some disadvantageous reactions were lost, but the neutral promiscuous reaction (NADH dehydrogenase) was retained in both DVR and HCAR. We also show that a portion of the Chl c biosynthetic pathway already existed in cyanobacteria. We discuss the importance of dynamic changes in promiscuous activity and of the latent pathways for metabolic evolution.