Abstract
All characterized members of the ubiquitous genus Acaryochloris share the unique property of containing large amounts of chlorophyll (Chl) d, a pigment exhibiting a red absorption maximum strongly shifted towards infrared compared to Chl a. Chl d is the major pigment in these organisms and is notably bound to antenna proteins structurally similar to those of Prochloron, Prochlorothrix and Prochlorococcus, the only three cyanobacteria known so far to contain mono- or divinyl-Chl a and b as major pigments and to lack phycobilisomes. Here, we describe RCC1774, a strain isolated from the foreshore near Roscoff (France). It is phylogenetically related to members of the Acaryochloris genus but completely lacks Chl d. Instead, it possesses monovinyl-Chl a and b at a b/a molar ratio of 0.16, similar to that in Prochloron and Prochlorothrix. It differs from the latter by the presence of phycocyanin and a vestigial allophycocyanin energetically coupled to photosystems. Genome sequencing confirmed the presence of phycobiliprotein and Chl b synthesis genes. Based on its phylogeny, ultrastructural characteristics and unique pigment suite, we describe RCC1774 as a novel species that we name Acaryochloris thomasi. Its very unusual pigment content compared to other Acaryochloris spp. is likely related to its specific lifestyle.
Highlights
All characterized members of the ubiquitous genus Acaryochloris share the unique property of containing large amounts of chlorophyll (Chl) d, a pigment exhibiting a red absorption maximum strongly shifted towards infrared compared to Chl a
RCC1774 totally lacks Chl d and possesses both Chls a and b with a b/a ratio of ∼0.16, a value in the range of those reported previously in natural Prochloron spp. populations (0.08-0.3950–53) and Prochlorothrix spp. isolates (0.05–0.1454,55); RCC1774 is the fourth ‘green oxyphotobacterium’ described to date. These organisms belong to distinct genera that are widely dispersed across the cyanobacterial radiation (Fig. 1 and Supplementary Fig. S1), suggesting that the ability to synthesize Chl b has been acquired at least five times independently during the evolution of Cyanobacteria, if one accounts the endosymbiotic ancestor of green algae that is often considered to be a Chl b-containing cyanobacterium[45]
The transformant instead produced [7-formyl]-Chl dP, a form of Chl unknown in nature, which these authors hypothesized was produced by the combined action of Chlide a oxygenase and the product(s) of the yet-to-be characterized gene(s) involved in Chl d biosynthesis, which was/ were not inactivated in the recombinant strain
Summary
All characterized members of the ubiquitous genus Acaryochloris share the unique property of containing large amounts of chlorophyll (Chl) d, a pigment exhibiting a red absorption maximum strongly shifted towards infrared compared to Chl a. Certain atypical cyanobacteria lack phycobilisomes and instead possess antenna complexes that are incorporated into membranes, like plants and most algae, the structure of these antennae is different between prokaryotic and eukaryotic oxyphototrophs[4,5] These atypical cyanobacteria include the Chl a/b-containing genera Prochloron and Prochlorothrix as well as Prochlorococcus, a ubiquitous marine cyanobacterium most abundant in warm oligotrophic areas and which contains divinyl derivatives of both Chl a and b6. We describe RCC1774, the type strain of a new species that is phylogenetically related to the Acaryochloris genus, but which possesses Chl a as the major photopigment as well as Chl b, zeaxanthin, β,ε-carotene and PC as main accessory pigments This is the first time that this suite of pigments is reported for a member of the Acaryochloris genus and for cyanobacteria at large. This discovery should provide interesting novel insights into the evolution of pigment synthesis in cyanobacteria
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