The Widely Conserved
            <i>ebo</i>
            Cluster Is Involved in Precursor Transport to the Periplasm during Scytonemin Synthesis in
            <i>Nostoc punctiforme</i>

Klicki, Kevin; Ferreira, Daniela; Hamill, Demetra; Dirks, Blake; Mitchell, Natalie M.; García-Pichel, Ferrán

doi:10.1128/mbio.02266-18

Cited by 30 publications

(39 citation statements)

References 41 publications

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“…Aside from their distant placement in those two strains, conservation and internal shared synteny of these genes are quite conspicuous. They seem to be involved in the secretion of scytonemin monomers to the periplasm for final condensation (24). A recent contribution (25) has identified the group of satellite genes as the cyanobacterial version of a much more widespread and ancient operon, the “ ebo operon” conserved among several bacterial phyla and eustigmatophyte plastid genomes.…”

Section: Resultsmentioning

confidence: 99%

Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen

García-Pichel

Lombard

Soule

et al. 2019

mBio

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The biosynthesis of the unique cyanobacterial (oxyphotobacterial) indole-phenolic UVA sunscreen, scytonemin, is coded for in a conserved operon that contains both core metabolic genes and accessory, aromatic amino acid biosynthesis genes dedicated to supplying scytonemin’s precursors. Comparative genomics shows conservation of this operon in many, but not all, cyanobacterial lineages. Phylogenetic analyses of the operon’s aromatic amino acid genes indicate that five of them were recruited into the operon after duplication events of their respective housekeeping cyanobacterial cognates. We combined the fossil record of cyanobacteria and relaxed molecular clock models to obtain multiple estimates of these duplication events, setting a minimum age for the evolutionary advent of scytonemin at 2.1 ± 0.3 billion years. The same analyses were used to estimate the advent of cyanobacteria as a group (and thus the appearance of oxygenic photosynthesis), at 3.6 ± 0.2 billion years before present. Post hoc interpretation of 16S rRNA-based Bayesian analyses was consistent with these estimates. Because of physiological constraints on the use of UVA sunscreens in general, and the biochemical constraints of scytonemin in particular, scytonemin’s age must postdate the time when Earth’s atmosphere turned oxic, known as the Great Oxidation Event (GOE). Indeed, our biological estimate is in agreement with independent geochemical estimates for the GOE. The difference between the estimated ages of oxygenic photosynthesis and the GOE indicates the long span (on the order of a billion years) of the era of “oxygen oases,” when oxygen was available locally but not globally. IMPORTANCE The advent of cyanobacteria, with their invention of oxygenic photosynthesis, and the Great Oxidation Event are arguably among the most important events in the evolutionary history of life on Earth. Oxygen is a significant toxicant to all life, but its accumulation in the atmosphere also enabled the successful development and proliferation of many aerobic organisms, especially metazoans. The currently favored dating of the Great Oxidation Event is based on the geochemical rock record. Similarly, the advent of cyanobacteria is also often drawn from the same estimates because in older rocks paleontological evidence is scarce or has been discredited. Efforts to obtain molecular evolutionary alternatives have offered widely divergent estimates. Our analyses provide a novel means to circumvent these limitations and allow us to estimate the large time gap between the two events.

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Section: Resultsmentioning

confidence: 99%

Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen

García-Pichel

Lombard

Soule

et al. 2019

mBio

Self Cite

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“…Answering the question as to why the ebo operon has been retained by some eustigmatophytes but lost by others awaits identification and functional characterization of the metabolite putatively synthesized by the suite of enzymes encoded by the ebo operon. Very recently, a genetic study of the ebo operon in the cyanobacterium Nostoc punctiforme indicated that the product of the Ebo proteins-mediated pathway is critical for the export of a precursor of the natural sunscreen scytonemin from the cytoplasm into the periplasm (Klicki et al. 2018).…”

Section: Resultsmentioning

confidence: 99%

Plastid Genomes and Proteins Illuminate the Evolution of Eustigmatophyte Algae and Their Bacterial Endosymbionts

Ševčíková

Yurchenko

Fawley

et al. 2019

Genome Biology and Evolution

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Eustigmatophytes, a class of stramenopile algae (ochrophytes), include not only the extensively studied biotechnologically important genus Nannochloropsis but also a rapidly expanding diversity of lineages with much less well characterized biology. Recent discoveries have led to exciting additions to our knowledge about eustigmatophytes. Some proved to harbor bacterial endosymbionts representing a novel genus, Candidatus Phycorickettsia, and an operon of unclear function (ebo) obtained by horizontal gene transfer from the endosymbiont lineage was found in the plastid genomes of still other eustigmatophytes. To shed more light on the latter event, as well as to generally improve our understanding of the eustigmatophyte evolutionary history, we sequenced plastid genomes of seven phylogenetically diverse representatives (including new isolates representing undescribed taxa). A phylogenomic analysis of plastid genome-encoded proteins resolved the phylogenetic relationships among the main eustigmatophyte lineages and provided a framework for the interpretation of plastid gene gains and losses in the group. The ebo operon gain was inferred to have probably occurred within the order Eustigmatales, after the divergence of the two basalmost lineages (a newly discovered hitherto undescribed strain and the Pseudellipsoidion group). When looking for nuclear genes potentially compensating for plastid gene losses, we noticed a gene for a plastid-targeted acyl carrier protein that was apparently acquired by horizontal gene transfer from Phycorickettsia. The presence of this gene in all eustigmatophytes studied, including representatives of both principal clades (Eustigmatales and Goniochloridales), is a genetic footprint indicating that the eustigmatophyte–Phycorickettsia partnership started no later than in the last eustigmatophyte common ancestor.

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“…The use of mutants and confocal autofluorescence microscopy indicated that the ebo gene cluster functions in the export of scytonemin monomers to the periplasm for final oxidative dimerization (Klicki et al. 2018). A study of desiccation tolerance indicated that N. punctiforme strain M‐15 tolerated desiccation and freeze‐thawing (Inoue‐Sakamoto et al.…”

mentioning

confidence: 99%

Shotgun metagenomics and microscopy indicate diverse cyanophytes, other bacteria, and microeukaryotes in the epimicrobiota of a northern Chilean wetland Nostoc (Cyanobacteria)

Satjarak

Graham

Piotrowski

et al. 2020

Journal of Phycology

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Prokaryotic Nostoc, one of the world's most conspicuous and widespread algal genera (similar to eukaryotic algae, plants, and animals) is known to support a microbiome that influences host ecological roles. Past taxonomic characterizations of surface microbiota (epimicrobiota) of free‐living Nostoc sampled from freshwater systems employed 16S rRNA genes, typically amplicons. We compared taxa identified from 16S, 18S, 23S, and 28S rRNA gene sequences filtered from shotgun metagenomic sequence and used microscopy to illuminate epimicrobiota diversity for Nostoc sampled from a wetland in the northern Chilean Altiplano. Phylogenetic analysis and rRNA gene sequence abundance estimates indicated that the host was related to Nostoc punctiforme PCC 73102. Epimicrobiota were inferred to include 18 epicyanobacterial genera or uncultured taxa, six epieukaryotic algal genera, and 66 anoxygenic bacterial genera, all having average genomic coverage ≥90X. The epicyanobacteria Geitlerinemia, Oscillatoria, Phormidium, and an uncultured taxon were detected only by 16S rRNA gene; Gloeobacter and Pseudanabaena were detected using 16S and 23S; and Phormididesmis, Neosynechococcus, Symphothece, Aphanizomenon, Nodularia, Spirulina, Nodosilinea, Synechococcus, Cyanobium, and Anabaena (the latter corroborated by microscopy), plus two uncultured cyanobacterial taxa (JSC12, O77) were detected only by 23S rRNA gene sequences. Three chlamydomonad and two heterotrophic stramenopiles genera were inferred from 18S; the streptophyte green alga Chaetosphaeridium globosum was detected by microscopy and 28S rRNA genes, but not 18S rRNA genes. Overall, >60% of epimicrobial taxa were detected by markers other than 16S rRNA genes. Some algal taxa observed microscopically were not detected from sequence data. Results indicate that multiple taxonomic markers derived from metagenomic sequence data and microscopy increase epimicrobiota detection.

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The Widely Conserved ebo Cluster Is Involved in Precursor Transport to the Periplasm during Scytonemin Synthesis in Nostoc punctiforme

Cited by 30 publications

References 41 publications

Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen

Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen

Plastid Genomes and Proteins Illuminate the Evolution of Eustigmatophyte Algae and Their Bacterial Endosymbionts

Shotgun metagenomics and microscopy indicate diverse cyanophytes, other bacteria, and microeukaryotes in the epimicrobiota of a northern Chilean wetland Nostoc (Cyanobacteria)

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