Elucidating the origins of phycocyanobilin biosynthesis and phycobiliproteins

Terrestrial ecosystems and human societies depend on oxygenic
photosynthesis, which began to reshape our atmosphere approximately 2.5
billion years ago. The earliest known organisms carrying out oxygenic
photosynthesis are the cyanobacteria, which use large complexes of
phycobiliproteins as light-harvesting antennae. Phycobiliproteins rely on
phycocyanobilin (PCB), a linear tetrapyrrole (bilin) chromophore, as the
light-harvesting pigment that transfers absorbed light energy from
phycobilisomes to the chlorophyll-based photosynthetic apparatus.
Cyanobacteria synthesize PCB from heme in two steps: A heme oxygenase
converts heme into biliverdin IXα (BV), and the ferredoxin-dependent bilin
reductase (FDBR) PcyA then converts BV into PCB. In the current work, we
examine the origins of this pathway. We demonstrate that PcyA evolved from
pre-PcyA proteins found in nonphotosynthetic bacteria and that pre-PcyA
enzymes are active FDBRs that do not yield PCB. Pre-PcyA genes are
associated with two gene clusters. Both clusters encode bilin-binding
globin proteins, phycobiliprotein paralogs that we designate as BBAGs
(bilin biosynthesis-associated globins). Some cyanobacteria also contain
one such gene cluster, including a BBAG, two V4R proteins, and an
iron–sulfur protein. Phylogenetic analysis shows that this cluster is
descended from those associated with pre-PcyA proteins and that
light-harvesting phycobiliproteins are also descended from BBAGs found in
other bacteria. We propose that PcyA and phycobiliproteins originated in
heterotrophic, nonphotosynthetic bacteria and were subsequently acquired
by cyanobacteria.