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 ␣-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.comparative microbial genomics ͉ photosynthesis ͉ oxygenic phototrophs ͉ evolution

Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls

“…Structural analysis revealed that photoactive Phe a forms a hydrogen bond with the C9-keto group and D1-130 residue, the latter of which is glutamic acid in many oxygenic photosynthetic organisms including spinach; however this residue is replaced by glutamine in Synechocystis and A. marina (30,31). Replacement of glutamine with glutamic acid in a Synechocystis mutant induced an up-shift of potential by 15 mV (32).…”

Deep sequencing of non-ribosomal peptide synthetases and polyketide synthases from the microbiomes of Australian marine sponges

“…and C. concentrica (Fan et al, 2012), the TEFAP approach amplified reads that form a phylogenetic clade with C domains from the marine cyanobacteria Moorea producens (Jones et al, 2011) and Acaryochloris marina (Swingley et al, 2008). Within Scopalina sp.…”

Microbial diversity of biofilm communities in microniches associated with the didemnid ascidian Lissoclinum patella

“…Another unique cyanobacterium, Acaryochloris marina, grows in biofilms on the underside of didemnid ascidians, where it uses chlorophyll (Chl) d to sustain its photosynthesis using near-infrared radiation (NIR; Kü hl et al, 2005). The A. marina type strain MBIC11017, originally isolated from L. patella, was hereafter sequenced and revealed a genome of unusually large size (Swingley et al, 2008). The relative abundance of A. marina in these epizoic microbial communities remains unknown and besides a recent genomic survey focusing on Prochloron, and its secondary metabolism (Donia et al, 2011), no further efforts have been made in studying the microbial diversity in L. patella.…”