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Photosynthetic Versatility in the Genome of Geitlerinema sp. PCC 9228 (Formerly Oscillatoria limnetica 'Solar Lake'), a Model Anoxygenic Photosynthetic Cyanobacterium - PubMed

  • ️Fri Jan 01 2016

Photosynthetic Versatility in the Genome of Geitlerinema sp. PCC 9228 (Formerly Oscillatoria limnetica 'Solar Lake'), a Model Anoxygenic Photosynthetic Cyanobacterium

Sharon L Grim et al. Front Microbiol. 2016.

Abstract

Anoxygenic cyanobacteria that use sulfide as the electron donor for photosynthesis are a potentially influential but poorly constrained force on Earth's biogeochemistry. Their versatile metabolism may have boosted primary production and nitrogen cycling in euxinic coastal margins in the Proterozoic. In addition, they represent a biological mechanism for limiting the accumulation of atmospheric oxygen, especially before the Great Oxidation Event and in the low-oxygen conditions of the Proterozoic. In this study, we describe the draft genome sequence of Geitlerinema sp. PCC 9228, formerly Oscillatoria limnetica 'Solar Lake', a mat-forming diazotrophic cyanobacterium that can switch between oxygenic photosynthesis and sulfide-based anoxygenic photosynthesis (AP). Geitlerinema possesses three variants of psbA, which encodes protein D1, a core component of the photosystem II reaction center. Phylogenetic analyses indicate that one variant is closely affiliated with cyanobacterial psbA genes that code for a D1 protein used for oxygen-sensitive processes. Another version is phylogenetically similar to cyanobacterial psbA genes that encode D1 proteins used under microaerobic conditions, and the third variant may be cued to high light and/or elevated oxygen concentrations. Geitlerinema has the canonical gene for sulfide quinone reductase (SQR) used in cyanobacterial AP and a putative transcriptional regulatory gene in the same operon. Another operon with a second, distinct sqr and regulatory gene is present, and is phylogenetically related to sqr genes used for high sulfide concentrations. The genome has a comprehensive nif gene suite for nitrogen fixation, supporting previous observations of nitrogenase activity. Geitlerinema possesses a bidirectional hydrogenase rather than the uptake hydrogenase typically used by cyanobacteria in diazotrophy. Overall, the genome sequence of Geitlerinema sp. PCC 9228 highlights potential cyanobacterial strategies to cope with fluctuating redox gradients and nitrogen availability that occur in benthic mats over a diel cycle. Such dynamic geochemical conditions likely also challenged Proterozoic cyanobacteria, modulating oxygen production. The genetic repertoire that underpins flexible oxygenic/anoxygenic photosynthesis in cyanobacteria provides a foundation to explore the regulation, evolutionary context, and biogeochemical implications of these co-occurring metabolisms in Earth history.

Keywords: anoxygenic photosynthesis; cyanobacteria; great oxidation event; nitrogenase; photosystem II D1 protein; sulfide quinone reductase.

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Figures

FIGURE 1
FIGURE 1

Metabolic schematic of Geitlerinema sp. PCC 9228. Genes for major processes [psbA1-3, sqr1, ccm, rbcLS, nifHDK, hox, arsABC, ure, urt, focA, narK, amt, glutathione S-transferase (GST)], and associated regulatory genes (arsR, ntcA, nifI1I2) are presented. Suppression of functions is indicated with red dashed lines ending in a flat line. Other interactions are indicated with black dashed lines ending with open circles. Transfer and production of key reactants and products are indicated with solid lines. Putative arsenite import is indicated with a dotted line, and anoxygenic photosynthesis-related processes have a solid blue line.

FIGURE 2
FIGURE 2

Schematic of nitrogenase genes in Geitlerinema sp. PCC 9228. nifXSU, iscA, nifHI1I2DK, fdxN, and nifENB are arranged in an apparent operon. nifV and a regulatory arsenic-related gene arsA are located upstream of the nifHDK operon.

FIGURE 3
FIGURE 3

Phylogenetic tree of psbA. Genes are colored by groups 1–4 modeled after (Cardona et al., 2015). The outgroup is a Gloeobacter kilaueensis JS psbA, which is most similar to psbD and is unable to oxidize water (Cardona et al., 2015). Purple indicates group 1, red genes belong to group 2, orange genes are members of group 3, and blue standard psbAs belong to group 4. Genetic proximity to sqr types I (green circle), II (maroon squares), and VI (blue stars) sqr genes are indicated. Fourteen psbA genes are five or fewer genes from sqr, and the largest gap is 19 genes. Geitlerinema sp. PCC 9228 has members of groups 2–4.

FIGURE 4
FIGURE 4

Phylogenetic tree of sulfide quinone reductase (sqr). Genes are colored by types I–VI modeled after (Marcia et al., 2010a). Bacterial FCSD (yellow) includes representatives of flavocytochrome c:sulfide dehydrogenase. Green sulfur bacteria have sqr belonging to types III (orange), V (light blue), IV (dark green), and VI (blue). Cyanobacterial sqr are limited to types I (light green), II (red), and VI. Proximity to psbA versions on the same contig (see Figure 3) are indicated with red circles (group 2) and brown stars (group 3). No sqr genes in this analysis were genetically proximal to groups 1 or 4 psbA genes. Geitlerinema sp. PCC 9228 has types VI and I sqr.

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