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GUN4 appeared early in cyanobacterial evolution.

ABSTRACT: Photosynthesis relies on chlorophylls, which are synthesized via a common tetrapyrrole trunk pathway also leading to heme, vitamin B12, and other pigmented cofactors. The first committed step for chlorophyll biosynthesis is insertion of magnesium into protoporphyrin IX by magnesium chelatase. Magnesium chelatase is composed of H-, I-, and D-subunits, with the tetrapyrrole substrate binding to the H-subunit. This subunit is rapidly inactivated in the presence of substrate, light, and oxygen, so oxygenic photosynthetic organisms require mechanisms to protect magnesium chelatase from similar loss of function. An additional protein, GUN4, binds to the H-subunit and to tetrapyrroles. GUN4 has been proposed to serve this protective role via its ability to bind linear tetrapyrroles (bilins). In the current work, we probe the origins of bilin binding by GUN4 via comparative phylogenetic analysis and biochemical validation of a conserved bilin-binding motif. Based on our results, we propose that bilin-binding GUN4 proteins arose early in cyanobacterial evolution and that this early acquisition represents an ancient adaptation for maintaining chlorophyll biosynthesis in the presence of light and oxygen.

SUBMITTER: Rockwell NC

PROVIDER: S-EPMC10156173 | biostudies-literature | 2023 May

REPOSITORIES: biostudies-literature

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GUN4 appeared early in cyanobacterial evolution.

Rockwell Nathan C NC Lagarias J Clark JC

PNAS nexus 20230412 5

Photosynthesis relies on chlorophylls, which are synthesized via a common tetrapyrrole trunk pathway also leading to heme, vitamin B12, and other pigmented cofactors. The first committed step for chlorophyll biosynthesis is insertion of magnesium into protoporphyrin IX by magnesium chelatase. Magnesium chelatase is composed of H-, I-, and D-subunits, with the tetrapyrrole substrate binding to the H-subunit. This subunit is rapidly inactivated in the presence of substrate, light, and oxygen, so o ...[more]

PMID: 37152672

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Project description:UNLABELLED:The "Candidatus Synechococcus spongiarum" group includes different clades of cyanobacteria with high 16S rRNA sequence identity (~99%) and is the most abundant and widespread cyanobacterial symbiont of marine sponges. The first draft genome of a "Ca. Synechococcus spongiarum" group member was recently published, providing evidence of genome reduction by loss of genes involved in several nonessential functions. However, "Ca. Synechococcus spongiarum" includes a variety of clades that may differ widely in genomic repertoire and consequently in physiology and symbiotic function. Here, we present three additional draft genomes of "Ca. Synechococcus spongiarum," each from a different clade. By comparing all four symbiont genomes to those of free-living cyanobacteria, we revealed general adaptations to life inside sponges and specific adaptations of each phylotype. Symbiont genomes shared about half of their total number of coding genes. Common traits of "Ca. Synechococcus spongiarum" members were a high abundance of DNA modification and recombination genes and a reduction in genes involved in inorganic ion transport and metabolism, cell wall biogenesis, and signal transduction mechanisms. Moreover, these symbionts were characterized by a reduced number of antioxidant enzymes and low-weight peptides of photosystem II compared to their free-living relatives. Variability within the "Ca. Synechococcus spongiarum" group was mostly related to immune system features, potential for siderophore-mediated iron transport, and dependency on methionine from external sources. The common absence of genes involved in synthesis of residues, typical of the O antigen of free-living Synechococcus species, suggests a novel mechanism utilized by these symbionts to avoid sponge predation and phage attack. IMPORTANCE:While the Synechococcus/Prochlorococcus-type cyanobacteria are widely distributed in the world's oceans, a subgroup has established its niche within marine sponge tissues. Recently, the first genome of sponge-associated cyanobacteria, "Candidatus Synechococcus spongiarum," was described. The sequencing of three representatives of different clades within this cyanobacterial group has enabled us to investigate intraspecies diversity, as well as to give a more comprehensive understanding of the common symbiotic features that adapt "Ca. Synechococcus spongiarum" to its life within the sponge host.

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GUN4 appeared early in cyanobacterial evolution.

Publications

GUN4 appeared early in cyanobacterial evolution.

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