UV radiation limited the expansion of cyanobacteria in early marine photic environments

Mloszewska, Aleksandra M.; Cole, Devon B.; Planavsky, Noah J.; Kappler, Andreas; Whitford, Denise S.; Owttrim, George W.; Konhauser, Kurt O.

doi:10.1038/s41467-018-05520-x

Cited by 48 publications

(26 citation statements)

References 68 publications

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“…Phlogopite is in the middle in terms of Fe content and would transmit more visible light than biotite but still attenuate an adequate amount of UVR. This effect of Fe on UVR attenuation and microbial protection is broadly consistent with recent studies on the role of Fe on UV attenuation [41, 42], which showed the importance of Fe(III) on UV attenuation. In our study, both Fe(II) and Fe(III) contents increased from muscovite to phlogopite to biotite, thus, it remains unclear what form of Fe, Fe(II) or Fe(III) is more important in UV attenuation.…”

Section: Discussionsupporting

confidence: 91%

“…The earliest rocks with signs of life are the Isua Greenbelt formation, which points to the existence of cyanobacteria as long ago as 3.7 Ga [89], indicating that phyllosilicates would have been readily available to protect such organisms when they emerged under intense UV irradiation. Recent studies [41, 42] have shown the importance of solid-form Fe(III) (in the forms of Fe oxides or Fe(III)-Si precipitates) in shielding UVR, but these oxidized forms of Fe are unlikely abundant in a reducing early earth environment. Instead, Fe(II) minerals would be more abundant.…”

Section: Discussionmentioning

confidence: 99%

“…Studies have shown that Fe-bearing minerals are efficient in protecting microorganisms against UVR [41, 42], because iron is an efficient absorber of such radiation [43]. Indeed, biotite, one particular member of the mica family, has been studied for its role as a potential habitat for cyanobacteria, because this mineral contains Fe in the structure.…”

Section: Introductionmentioning

confidence: 99%

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Phyllosilicates as protective habitats of filamentous cyanobacteria Leptolyngbya against ultraviolet radiation

Kugler

Dong

2019

PLoS ONE

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Phototrophic cyanobacteria are limited in growth locations by their need for visible light and must also cope with intermittent ultraviolet radiation (UVR), especially in extreme environments such as deserts and on early Earth. One survival method for cyanobacteria is growing endolithically within minerals such as micas, gypsum, and quartz minerals. However, the capability of different mica minerals to protect cyanobacteria from UVR, while at the same time allowing transmission of photosynthetically active radiation (PAR), has only been minimally examined. In this study, we performed laboratory incubation experiments to demonstrate that a model filamentous cyanobacterium, Leptolyngbya sp., can colonize micas, such as muscovite, phlogopite, and biotite. After inoculation experiments confirmed that these cyanobacteria grew between the sheets of mica, Leptolyngbya sp. colonies were exposed to UVB and UVC for up to 24 hrs, and the level of survival was determined using chlorophyll a and carotenoid assays. Of the three micas investigated, muscovite, being an Fe-poor and Al-rich mica, provided the least attenuation of UVR, however it transmitted the most visible light. Fe-rich biotite provided the best UVR shielding. Phlogopite, apparently because of its intermediate amount of Fe, showed the greatest ability to shield UVR while still transmitting an adequate amount of visible light, making it the ideal habitat for the cyanobacterium. Upon exposure to UVR, significant shifts in several important fatty acids of the cyanobacterium were detected such as linolenic acid and oleic acid, 18:3ω3 and 18:1ω9c, respectively. These cellular changes are interpreted to be a consequence of UVR and other accessory stress (such as O 3 ).

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Phyllosilicates as protective habitats of filamentous cyanobacteria Leptolyngbya against ultraviolet radiation

Kugler

Dong

2019

PLoS ONE

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“…It has been shown experimentally, using the marine planktonic cyanobacterium Synechococcus sp. 7002 as model organism, that the possible toxic effects of high iron concentrations in the Archean ocean could have been cancelled by the high silica concentrations that were present in this ocean too (Mloszewska et al 2015). This fact could have facilitated the adaptation of early cyanobacteria to ferruginous conditions by reducing toxic levels of bioavailable iron.…”

Section: Discussionmentioning

confidence: 99%

Assessing the effects of ultraviolet radiation on the photosynthetic potential in Archean marine environments

Avila-Alonso

Baetens

Cárdenas

et al. 2016

International Journal of Astrobiology

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In this work, the photosynthesis model presented by Avila et al. in 2013 is extended and more scenarios inhabited by ancient cyanobacteria are investigated to quantify the effects of ultraviolet (UV) radiation on their photosynthetic potential in marine environments of the Archean eon. We consider ferrous ions as blockers of UV during the Early Archean, while the absorption spectrum of chlorophyll a is used to quantify the fraction of photosynthetically active radiation absorbed by photosynthetic organisms. UV could have induced photoinhibition at the water surface, thereby strongly affecting the species with low light use efficiency. A higher photosynthetic potential in early marine environments was shown than in the Late Archean as a consequence of the attenuation of UVC and UVB by iron ions, which probably played an important role in the protection of ancient free-floating bacteria from high-intensity UV radiation. Photosynthetic organisms in Archean coastal and ocean environments were probably abundant in the first 5 and 25 m of the water column, respectively. However, species with a relatively high efficiency in the use of light could have inhabited ocean waters up to a depth of 200 m and show a Deep Chlorophyll Maximum near 60 m depth. We show that the electromagnetic radiation from the Sun, both UV and visible light, could have determined the vertical distribution of Archean marine photosynthetic organisms

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“…7) involved the sequential acquisition of a complex set of innovations [66] over the course of hundreds of millions of years [63,64]. Finally, in the case of cyanobacteria, the first accumulation of oxygen also led to the eventual emergence of an ozone layer [25], which filtered out damaging UV radiation and allowed cyanobacteria to continue their expansion [288]. Thus, the size of habitats available to cyanobacteria and photosynthetic eukaryotes and their ability to fill those habitats in general thus likely increased in tandem during the rise of continents.…”

Section: Fe 3+mentioning

confidence: 99%

Evolution of cellular metabolism and the rise of a globally productive biosphere

Braakman

2019

Preprint

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The metabolic processes of cells and chemical processes in the environment are fundamentally intertwined and have evolved in concert over billions of years. Here I argue that intrinsic properties of cellular metabolism imposed central constraints on the historical trajectories of biopsheric productivity and atmospheric oxygenation. Photosynthesis depends on iron, but iron is highly insoluble under the aerobic conditions produced by oxygenic photosynthesis. These counteracting constraints led to two major stages of Earth oxygenation. Cyanobacterial photosynthesis drove a major biospheric expansion near the Archean-Proterozoic boundary but subsequently remained largely restricted to continental boundaries and shallow aquatic environments, where weathering inputs made iron more accessible. The anoxic deep open ocean was rich in free iron during the Proterozoic, but this iron remained effectively inaccessible since a photosynthetic expansion would have quenched its own supply. Near the Proterozoic-Phanerozoic boundary, bioenergetic innovations allowed eukaryotic photosynthesis to expand into the deep open oceans and onto the continents, where nutrients are inherently harder to come by. Key insights into the ecological rise of eukaryotic photosynthesis emerge from analyses of marine Synechococcus and Prochlorococcus, abundant marine picocyanobacteria whose ancestors colonized the oceans in the Neoproterozoic. The reconstructed evolution of Prochlorococcus reveals a sequence of innovations that ultimately produced a form of photosynthesis more like that of green plant cells than other cyanobacteria. Innovations increased the energy flux of cells, thereby enhancing their ability to acquire sparse nutrients, and as by-product also increased the production of organic carbon waste. Some of these organic waste products in turn had the ability to chelate iron and make it bioavailable, thereby indirectly pushing the oceans through a transition from an anoxic state rich in free iron to an oxygenated state with organic carbon-bound iron. The periods of Earth history around cyanobacteria- and eukaryote-driven biospheric expansions share several other parallels. Both epochs have also been linked to major carbon cycle perturbations and global glaciations, as well as changes in the nature of mantle convection and plate tectonics. This suggests the dynamics of life and Earth are intimately intertwined across many levels and that general principles governed Neoarchean and Neoproterozoic transitions in these coupled dynamics.

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UV radiation limited the expansion of cyanobacteria in early marine photic environments

Cited by 48 publications

References 68 publications

Phyllosilicates as protective habitats of filamentous cyanobacteria Leptolyngbya against ultraviolet radiation

Phyllosilicates as protective habitats of filamentous cyanobacteria Leptolyngbya against ultraviolet radiation

Assessing the effects of ultraviolet radiation on the photosynthetic potential in Archean marine environments

Evolution of cellular metabolism and the rise of a globally productive biosphere

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