Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina

Abstract

Acaryochloris marina is a unique cyanobacterium that is able to produce chlorophyll d as its primary photosynthetic pigment and thus efficiently use far-red light for photosynthesis. Acaryochloris species have been isolated from marine environments in association with other oxygenic phototrophs, which may have driven the niche-filling introduction of chlorophyll d. To investigate these unique adaptations, we have sequenced the complete genome of A. marina. The DNA content of A. marina is composed of 8.3 million base pairs, which is among the largest bacterial genomes sequenced thus far. This large array of genomic data is distributed into nine single-copy plasmids that code for >25% of the putative ORFs. Heavy duplication of genes related to DNA repair and recombination (primarily recA) and transposable elements could account for genetic mobility and genome expansion. We discuss points of interest for the biosynthesis of the unusual pigments chlorophyll d and alpha-carotene and genes responsible for previously studied phycobilin aggregates. Our analysis also reveals that A. marina carries a unique complement of genes for these phycobiliproteins in relation to those coding for antenna proteins related to those in Prochlorococcus species. The global replacement of major photosynthetic pigments appears to have incurred only minimal specializations in reaction center proteins to accommodate these alternate pigments. These features clearly show that the genus Acaryochloris is a fitting candidate for understanding genome expansion, gene acquisition, ecological adaptation, and photosystem modification in the cyanobacteria.

Fig. 1.

Circular representation of the A. marina chromosome and plasmids. The different rings represent (from outer to inner) all genes and insertion elements, color-coded by functional category (rings 1 and 2), deviation from average GC content (ring 3), and GC skew (ring 4). All plasmids are represented at ×10 scale for visualization except pREB9 at ×500. Color codes are as follows: turquoise, small-molecule biosynthesis; yellow, central or intermediary metabolism; orange, energy metabolism; red, signal transduction; light blue, DNA metabolism; blue, transcription; purple, protein synthesis/fate; dark green, surface-associated features; gray, miscellaneous features; pink, phage and insertion elements; light green, unknown function; dark gray, conserved hypothetical proteins; black, hypothetical proteins; and brown, pseudogenes.

Fig. 2.

Phylogenetic relationship of CAO superfamily proteins constructed using maximum-likelihood. Acaryochloris sequences are listed by their locus tag. Note that the phylogenetic space between Prochlorococcus and plant CAO enzymes includes a number of undescribed proteins implicated in degradation of aromatic ring molecules including chlorophyll.

Fig. 3.

A schematic of the putative carotenoid biosynthesis pathway in Acaryochloris. The reaction catalyzed by CrtR passes through the intermediate β-cryptoxanthin.

Fig. 4.

The relationship between the usage of PBPs and accessory CBPs in cyanobacteria. Green diamonds represent Prochlorococcus species, blue triangles represent marine Synechococcus species, a red square represents Acaryochloris, and black circles represent all other cyanobacteria. Points including two or more species are bordered in black.