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

ABSTRACT 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. Compa...

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Autores principales:	Ferran Garcia-Pichel, Jonathan Lombard, Tanya Soule, Sean Dunaj, Steven H. Wu, Martin F. Wojciechowski
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	UV photobiology cyanobacteria deep evolution secondary metabolism Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/dc1a5ac515754f9c8a664e400ff4ecad
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spelling	oai:doaj.org-article:dc1a5ac515754f9c8a664e400ff4ecad2021-11-15T15:55:25ZTiming the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen10.1128/mBio.00561-192150-7511https://doaj.org/article/dc1a5ac515754f9c8a664e400ff4ecad2019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00561-19https://doaj.org/toc/2150-7511ABSTRACT 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.Ferran Garcia-PichelJonathan LombardTanya SouleSean DunajSteven H. WuMartin F. WojciechowskiAmerican Society for MicrobiologyarticleUV photobiologycyanobacteriadeep evolutionsecondary metabolismMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	UV photobiology cyanobacteria deep evolution secondary metabolism Microbiology QR1-502
spellingShingle	UV photobiology cyanobacteria deep evolution secondary metabolism Microbiology QR1-502 Ferran Garcia-Pichel Jonathan Lombard Tanya Soule Sean Dunaj Steven H. Wu Martin F. Wojciechowski Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen
description	ABSTRACT 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.
format	article
author	Ferran Garcia-Pichel Jonathan Lombard Tanya Soule Sean Dunaj Steven H. Wu Martin F. Wojciechowski
author_facet	Ferran Garcia-Pichel Jonathan Lombard Tanya Soule Sean Dunaj Steven H. Wu Martin F. Wojciechowski
author_sort	Ferran Garcia-Pichel
title	Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen
title_short	Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen
title_full	Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen
title_fullStr	Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen
title_full_unstemmed	Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen
title_sort	timing the evolutionary advent of cyanobacteria and the later great oxidation event using gene phylogenies of a sunscreen
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/dc1a5ac515754f9c8a664e400ff4ecad
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Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen

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