Phyllosilicates as protective habitats of filamentous cyanobacteria Leptolyngbya against ultraviolet radiation

Abstract

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 ).

A critical review of mineral–microbe interaction and co-evolution: mechanisms and applications

“…Negatively charged microbial cells attach not only to a positively charged mineral surface but also to a negatively charged one, because they need nutrients from minerals and their cell walls possess specific functional groups to form chemical bonds with the mineral surface [ 6 ]. Once attached, the amount of structural Fe in minerals is an important parameter in determining the extent of the UV shielding capacity [ 9 ]. Many minerals have the ability to offer protection against various environmental stresses, but the physicochemical factors that determine the level of protection have not been systematically evaluated, which is important for understanding microbial survival strategies in extreme environments, early Earth and on extraterrestrial planets.…”

“…Montmorillonite can interact with fatty acids to form protocells with the abilities of growth and division [ 94 ]. After life origination around 3.7 Ga [ 95 ], minerals continued to serve as protectants of life itself [ 8 , 9 , 96 ].…”

Gloeobacter and the implications of a freshwater origin of Cyanobacteria

“…A potential constraint on photosynthesis before the Global Oxidation Event (GOE) was the greater UV flux, and especially UVC (< 280 nm), in the absence of stratospheric ozone as a UV screen (Cockell & Raven 2007;Zerkle et al 2012;Mioszewska et al 2018;Kugler & Dong 2019). Photosynthetically active radiation, i.e.…”

“…Photosynthetically active radiation, i.e. ( 380)-400-700 (-730) nm is required for oxygenic photosynthesis, so any screening of UV must still allow the photosynthetic light-harvesting pigments to be supplied with photosynthetically active radiation (Cockell & Raven 2007;Zerkle et al 2012;Mioszewska et al 2018;Kugler & Dong 2019;Garcia-Pichel et al 2019). A possible global screening mechanism is a UV-absorbing organic atmospheric haze with lifetime of individual molecules increased by the absence of oxidation by atmospheric O 2 (Zerkle et al 2012).…”

“…Marine, and probably freshwater ecosystems, would have had dissolved Fe 2+ as a UV screen before oxidation by O 2 to Fe 2+ , although some Fe 2+ would be removed by anoxygenic photosynthesis using Fe 2+ as electron donor. On land and in marine and freshwater microbial mats, phyllosilicates (Fe + Si) could act as a local UV refuge for cyanobacteria with UV absorbed to a greater extent than photosynthetically active radiation (Mioszewska et al 2018;Kugler & Dong 2019). This is a special case of endo-or hypolithic UV refuges (Cockell & Raven 2007).…”