Abstract

BackgroundCyanobacteria maintain extensive repertoires of regulatory genes that are vital for adaptation to environmental stress. Some cyanobacterial genomes have been noted to encode diversity-generating retroelements (DGRs), which promote protein hypervariation through localized retrohoming and codon rewriting in target genes. Past research has shown DGRs to mainly diversify proteins involved in cell-cell attachment or viral-host attachment within viral, bacterial, and archaeal lineages. However, these elements may be critical in driving variation for proteins involved in other core cellular processes.ResultsMembers of 31 cyanobacterial genera encode at least one DGR, and together, their retroelements form a monophyletic clade of closely-related reverse transcriptases. This class of retroelements diversifies target proteins with unique domain architectures: modular ligand-binding domains often paired with a second domain that is linked to signal response or regulation. Comparative analysis indicates recent intragenomic duplication of DGR targets as paralogs, but also apparent intergenomic exchange of DGR components. The prevalence of DGRs and the paralogs of their targets is disproportionately high among colonial and filamentous strains of cyanobacteria.ConclusionWe find that colonial and filamentous cyanobacteria have recruited DGRs to optimize a ligand-binding module for apparent function in signal response or regulation. These represent a unique class of hypervariable proteins, which might offer cyanobacteria a form of plasticity to adapt to environmental stress. This analysis supports the hypothesis that DGR-driven mutation modulates signaling and regulatory networks in cyanobacteria, suggestive of a new framework for the utility of localized genetic hypervariation.

Highlights

  • Cyanobacteria maintain extensive repertoires of regulatory genes that are vital for adaptation to environmental stress

  • A conserved subclass of Retroelements in cyanobacteria Our analysis identified 58 Diversity-generating retroelement (DGR) that include 90 target genes in 52 genomes of cyanobacteria spanning 31 different genera

  • All DGRs were identified by presence of diagnostic and essential components: an Reverse transcriptase (RT) gene; one or more Variable protein (VP) genes with variable region (VR) regions; and a Template region (TR) region

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Summary

Introduction

Cyanobacteria maintain extensive repertoires of regulatory genes that are vital for adaptation to environmental stress. Cyanobacteria are a remarkably diverse lineage, in terms of metabolisms, morphologies, and habitat distribution Perhaps most notably, this phylum contains the only prokaryotic organisms known to have evolved the capability for oxygenic photosynthesis; this trait was later acquired by eukaryotes through endosymbiosis with cyanobacteria, resulting in the formation of chloroplasts [1, 2], and Vallota-Eastman et al BMC Genomics (2020) 21:664 and motile filaments (hormogonia) [9]. Certain members of the cyanobacterial phylum possess an extensive capacity to adapt to various environmental pressures through tightly-controlled regulation of complex cellular programs for signal response This is exemplified by abilities for metabolic switching (i.e. CO2/N2 fixation), maintaining photoreceptors of various wavelength sensitivities for binary programs of circadian rhythm, and forming specialized cells which can sometimes be terminally differentiated and lead to multicellularity [9, 10]. Paralogs of these regulatory proteins are more abundant among the more complex species of cyanobacteria

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