Probing the in vivo biosynthesis of scytonemin, a cyanobacterial ultraviolet radiation sunscreen, through small scale stable isotope incubation studies and MALDI-TOF mass spectrometry

Scytonemin is a dimeric indole phenolic pigment found in the sheaths of many cyanobacteria. This pigment absorbs UV radiation protecting subtending cyanobacterial cells from harmful effects. Based on scytonemin's unique chemical structure, the pathway to its biosynthesis is uncertain, thus motivating the current investigation. Herein, we report the incorporation of both tyrosine and tryptophan into scytonemin, and provide in vivo data supporting the tryptophan origin of the ketone carbon involved in the condensation of the two biosynthetic precursors. This study also reports on the new use of a small-scale, MALDI-TOF mass spectrometry technique to monitor the incorporation of isotopically labeled tyrosine during scytonemin biosynthesis.     

Effects of periodic desiccation on the synthesis of the UV-screening compound, scytonemin, in cyanobacteria

Scytonemin is an ultraviolet radiation (UVR)-screening compound synthesized by some sheathed cyanobacteria exposed to high solar and sky radiation. It is primarily produced in response to UVA radiation, but certain environmental stresses can enhance synthesis. This study focuses on the effects of periodic desiccation on scytonemin synthesis in three desiccation-tolerant cyanobacterial strains, Nostoc punctiforme PCC 73102, Chroococcidiopsis CCMEE 5056 and Chroococcidiopsis CCMEE 246. Nostoc punctiforme and Chroococcidiopsis CCMEE 5056 exposed to UVA radiation produced more concentrated scytonemin screens when experiencing periodic desiccation (i.e. 1 day desiccated for every 2 days hydrated) than when continuously hydrated. A more concentrated scytonemin screen would reduce the amount of UVR damage accrued when cells are desiccated and metabolically inactive. This might allow the cyanobacteria to allocate more energy to systems other than UVR damage repair during rehydration, which would facilitate recovery. The scytonemin screen is extremely stable, remaining largely intact in the sheaths of desiccated N. punctiforme even when continuously exposed to UVA radiation for about 2 months. In contrast to the above findings, scytonemin synthesis in Chroococcidiopsis CCMEE 246, a strain that produces scytonemin constitutively under low visible light (no UVA), was partially inhibited by periodic desiccation.     

SCYTONEMIN, A CYANOBACTERIAL SHEATH PIGMENT, PROTECTS AGAINST UVC RADIATION: IMPLICATIONS FOR EARLY PHOTOSYNTHETIC LIFE

During the Precambrian, ultraviolet (UV) radiation reaching the Earth's surface, including UVC wavelengths (190–280 nm), was considerably higher than present because of the lack of absorbing gases (e.g. O₂ and O₃) in the atmosphere. High UV flux would have been damaging to photosynthetic organisms exposed to solar radiation. Nevertheless, fossil evidence indicates that cyanobacteria-like ancestors may have evolved as early as 3.5 × 10⁹ yr ago, and were common in shallow marine habitats by 2.5 × 10⁹ years ago. Scytonemin, a cyanobacterial extracellular sheath pigment, strongly absorbs UVC radiation. Exposure to high-irradiance conditions caused cells to synthesize scytonemin and resulted in decreased UVC inhibition of photosynthetic carbon uptake. It was further demonstrated that scytonemin alone was sufficient for substantial protection against UVC damage. This represents the first experimental demonstration of biological protection against UVC radiation in cyanobacteria. These results suggest that scytonemin may have evolved during the Precambrian and allowed colonization of exposed, shallow-water and terrestrial habitats by cyanobacteria or their oxygenic ancestors.     

The cyanobacterial UV-absorbing pigment scytonemin displays radical-scavenging activity

Scytonemin is a 544-Da hydrophobic pigment that can absorb UV-A radiation. It is present in cyanobacterial sheaths and is thought to function as a UV protectant. In this study, scytonemin was purified from the terrestrial cyanobacterium Nostoc commune, and its radical-scavenging activity was characterized. The purified scytonemin quenched an organic radical in vitro and accounted for up to 10% of the total activity of an ethanol extract of N. commune. These results suggest that the extracellular UV-absorbing pigment scytonemin has multiple roles, functioning as a UV sunscreen and an antioxidant relevant to anhydrobiosis in N. commune.     

Chlorophyll f distribution and dynamics in cyanobacterial beachrock biofilms

Chlorophyll (Chl) f, the most far‐red (720–740 nm) absorbing Chl species, was discovered in cyanobacterial isolates from stromatolites and subsequently in other habitats as well. However, the spatial distribution and temporal dynamics of Chl f in a natural habitat have so far not been documented. Here, we report the presence of Chl f in cyanobacterial beachrock biofilms. Hyperspectral imaging on cross‐sections of beachrock from Heron Island (Great Barrier Reef, Australia), showed a strong and widely distributed signature of Chl f absorption in an endolithic layer below the dense cyanobacterial surface biofilm that could be localized to aggregates of Chroococcidiopsis‐like unicellular cyanobacteria packed within a thick common sheath. High‐pressure liquid chromatography‐based pigment analyses showed in situ ratios of Chl f to Chl a of 5% in brown‐pigmented zones of the beachrock, with lower ratios of ~0.5% in the black‐ and pink‐pigmented biofilm zones. Enrichment experiments with black beachrock biofilm showed stimulated synthesis of Chl f and Chl d when grown under near‐infrared radiation (NIR; 740 nm), with a Chl f to Chl a ratio increasing 4‐fold to 2%, whereas the Chl d to Chl a ratio went from 0% to 0.8%. Enrichments grown under white light (400–700 nm) produced no detectable amounts of either Chl d or Chl f. Beachrock cyanobacteria thus exhibited characteristics of far‐red light photoacclimation, enabling Chl f ‐containing cyanobacteria to thrive in optical niches deprived of visible light when sufficient NIR is prevalent.     

Responses of aquatic algae and cyanobacteria to solar UV-B

Continuous depletion of the stratospheric ozone layer has resulted in an increase in solar ultraviolet-B (UV-B; 280–315 nm) radiation reaching the Earth's surface. The consequences for aquatic phototrophic organisms of this small change in the solar spectrum are currently uncertain. UV radiation has been shown to adversely affect a number of photochemical and photobiological processes in a wide variety of aquatic organisms, such as cyanobacteria, phytoplankton and macroalgae. However, a number of photosynthetic organisms counteract the damaging effects of UV-B by synthesizing UV protective compounds such as mycosporine-like amino acids (MAAs) and the cyanobacterial sheath pigment, scytonemin. The aim of this contribution is to discuss the responses of algae and cyanobacteria to solar UV-B radiation and the role of photoprotective compounds in mitigating UV-B damage.     

Using absorbance and fluorescence spectra to discriminate microalgae

The utility of absorbance and fluorescence-emission spectra for discriminating among microalgal phylogenetic groups, selected species, and phycobilin- and non-phycobilin-containing algae was examined using laboratory cultures. A similarity index algorithm, in conjunction with fourth-derivative transformation of absorbance spectra, provided discrimination among the chlorophyll [Chl] a/phycobilin (cyanobacteria), Chl a/Chl c/phycobilin (cryptophytes), Chl a/Chl b (chlorophytes, euglenophytes, prasinophytes), Chl a/Chl c/fucoxanthin (diatoms, chrysophytes, raphidophytes) and Chl a/Chl c/peridinin (dinoflagellates) spectral classes, and often between}among closely related phylogenetic groups within a class. Spectra for phylogenetic groups within the Chl a/Chl c/fucoxanthin, Chl a/Chl c/peridinin, Chl a/phycobilins and Chl a/Chl c/phycobilin classes were most distinguishable from spectra for groups within the Chl a/Chl b spectral class. Chrysophytes/diatoms/raphidophytes and dinoflagellates (groups within the comparable spectral classes, Chl a/Chl c/fucoxanthin and Chl a/Chl c/peridinin, respectively) displayed the greatest similarity between/among groups. Spectra for phylogenetic groups within the Chl a/Chl c classes displayed limited similarity with spectra for groups within the Chl/phycobilin classes. Among the cyanobacteria and chlorophytes surveyed, absorbance spectra of species possessing dissimilar cell morphologies were discriminated, with the greatest range of differentiation occurring among cyanobacteria. Among the cyanobacteria, spectra for selected problematic species were easily discriminated from spectra from each other and from other cyanobacteria. Fluorescence-emission spectra were distinct among spectral classes and the similarity comparisons involving fourth-derivative transformation of spectra discriminated the increasing contribution of distinct cyanobacterial species and between phycobilin- and non-phycobilin-containing species within a hypothetical mixed assemblage. These results were used to elucidate the application for in situ moored instrumentation incorporating such approaches in water quality monitoring programmes, particularly those targeting problematic cyanobacterial blooms.     

Chlorophyll f production in two new subaerial cyanobacteria of the family Oculatellaceae

Chlorophyll (Chl) f was recently identified in a few cyanobacteria as the fifth chlorophyll of oxygenic organisms. In this study, two Leptolyngbya-like strains of CCNU0012 and CCNU0013 were isolated from a dry ditch in Chongqing city and a brick wall in Mount Emei Scenic Area in China, respectively. These two strains were described as new species: Elainella chongqingensis sp. nov. (Oculatellaceae, Synechococcales) and Pegethrix sichuanica sp. nov. (Oculatellaceae, Synechococcales) by the polyphasic approach based on morphological features, phylogenetic analysis of 16S rRNA gene and secondary structure comparison of 16S-23S internal transcribed spacer domains. Both strains produced Chl a under white light (WL) but additionally induced Chl f synthesis under far-red light (FRL). Unexpectedly, the content of Chl f in P. sichuanica was nearly half that in most Chl f-producing cyanobacteria. Red-shifted phycobiliproteins were also induced in both strains under FRL conditions. Subsequently, additional absorption peak beyond 700 nm in the FRL spectral region appeared in these two strains. This is the first report of Chl f production induced by FRL in the family Oculatellaceae. This study not only extended the diversity of Chl f-producing cyanobacteria but also provided precious samples to elucidate the essential binding sites of Chl f within cyanobacterial photosystems.     

The response regulator Npun_F1278 is essential for scytonemin biosynthesis in the cyanobacterium Nostoc punctiforme ATCC 29133

Following exposure to long‐wavelength ultraviolet radiation (UVA), some cyanobacteria produce the indole‐alkaloid sunscreen scytonemin. The genomic region associated with scytonemin biosynthesis in the cyanobacterium Nostoc punctiforme includes 18 cotranscribed genes. A two‐component regulatory system (Npun_F1277/Npun_F1278) directly upstream from the biosynthetic genes was identified through comparative genomics and is likely involved in scytonemin regulation. In this study, the response regulator (RR), Npun_F1278, was evaluated for its ability to regulate scytonemin biosynthesis using a mutant strain of N. punctiforme deficient in this gene, hereafter strain Δ1278. Following UVA radiation, the typical stimulus to initiate scytonemin biosynthesis, Δ1278 was incapable of producing scytonemin. A phenotypic characterization of Δ1278 suggests that aside from the ability to produce scytonemin, the deletion of the Npun_F1278 gene does not affect the cellular morphology, cellular differentiation capability, or lipid‐soluble pigment complement of Δ1278 compared to the wildtype. The mutant, however, had a slower specific growth rate under white light and produced ~2.5‐fold more phycocyanin per cell under UVA than the wildtype. Since Δ1278 does not produce scytonemin, this study demonstrates that the RR gene, Npun_F1278, is essential for scytonemin biosynthesis in N. punctiforme. While most of the evaluated effects of this gene appear to be specific for scytonemin, this regulator may also influence the overall health of the cell and phycobiliprotein synthesis, directly or indirectly. This is the first study to identify a regulatory gene involved in the biosynthesis of the sunscreen scytonemin and posits a link between cell growth, pigment synthesis, and sunscreen production.     

PIGMENT AND PHOTOSYNTHETIC RESPONSES OF OSCILLATORIA AGARDHII (CYANOPHYTA) TO PHOTON FLUX DENSITY AND SPECTRAL QUALITY1

The effects of photon flux density (PFD) and spectral quality on biomass, pigment content and composition, and the photosynthetic activity of Oscillatoria agardhii Gomont were investigated in steady-state populations. For alterations of PFD, chemostat populations were exposed to 50, 130 and 230 μmol photons·m^?2·s^?1 of photosynthetic active radiation (PAR). Decreases in biomass, chlorophyll a (Chl a) and c-phycocyanin (CPC) contents, and CPC: Chl a and CPC: carotenoid content was not altered. Increases in the relative abundances of myxoxanthophyll and zeaxanthin and deceases in the relative abundances of echinenone and β-carotene within the carotenoid pigments coincided with increasing PFD. Increases in Chl a-specific photosynthetic rates and maxima and decreases in biomass-specific photosynthetic rates and maxima with increasing PFD were attributed to increased light harvesting by carotenoids per unit Chl a and reduction in total pigment content, respectively. Responses to spectral quality were tested by exposing chemostat populations to a gradient of spectral transmissions at 50 μmol photons·m^?2·s^?1 PAR. Biomass differences among populations were likely attributable to the distinct absorption of the PAR spectrum by Chl a, CPC, and carotenoids. Although pigment contents were not altered by spectral quality, relative abundances of zeaxanthin and echinenone in the carotenoid pigments increased in populations exposed to high-wavelength PAR. The population adapted to green light possessed a greater photosynthetic maximum than populations adapted to other spectral qualities.     

Effects of nitrogen source on the synthesis of the UV-screening compound, scytonemin, in the cyanobacterium Nostoc punctiforme PCC 73102

The effects of nitrogen source (N(2), NO(3)(-) and NH(4)(+)) on scytonemin synthesis were investigated in the heterocystous cyanobacterium Nostoc punctiforme PCC 73102. With the required UVA radiation included, Nostoc synthesized three to seven times more scytonemin while fixing nitrogen than when utilizing nitrate or ammonium. A similar increase in scytonemin synthesis occurred when nitrate or ammonium became depleted by growth and Nostoc switched to diazotrophic metabolism with the differentiation of heterocysts. In addition, UVA-exposed cultures grown in medium with both NO(3)(-) and NH(4)(+) synthesized some scytonemin but synthesis increased when NH(4)(+) was depleted and growth had become dependent on NO(3)(-) reduction. Although the mechanism is unclear, these results suggest that the greater the restriction in nitrogen accessibility, the greater the production of scytonemin. Perhaps the entire response may be an interaction between this restriction and a resultant sensitivity to UV radiation that acts as a cue for determining the level of scytonemin synthesis. Scytonemin is a stable UVR screening compound and appears to be synthesized by cyanobacteria as a long-term solution for reducing UVR exposure and damage, but mainly or solely, when metabolic activity is absent. It is likely that during metabolic resurgence, the presence of a dense scytonemin sheath would facilitate the recovery process without the need for active defenses against UV radiation.     

UV-acclimation responses in natural populations of cyanobacteria (Calothrix sp.)

Phenotypic acclimation to changing conditions is typically thought to be beneficial to organisms in the environment. UV radiation is an important parameter affecting photosynthetic organisms in natural environments. We measured the response of photosynthetic carbon fixation in populations of cyanobacteria inhabiting a hot spring following acclimation to different UV treatments. These two very closely related populations of cyanobacteria, differing in their content of the extracellular UV-screening pigment scytonemin, were acclimated in situ under natural solar irradiance modified by filters that excluded both UVA/B, only UVB or transmitted both UVA/B. Cells from each preacclimation treatment were subsequently assayed for photosynthetic performance under all UV conditions (incubation treatment) giving a two-factor experimental design for each population. No acclimation filter treatment effects were observed even after two months under different acclimation treatments. This suggests that UV photoacclimation does not occur in either of these populations, regardless of the presence of scytonemin. By contrast, cells showed significant UV-inhibition during 1 h incubations under full sun. The population with high levels of scytonemin usually had lower rates of photosynthetic carbon fixation than the scytonemin-lacking population. However, the degree of UV inhibition, especially UVA inhibition, was higher for the cells without scytonemin pigment. These results suggest that closely related natural cyanobacterial populations respond differently to natural irradiance conditions and may be adopting different strategies of UV tolerance.     

Different physiological responses of cyanobacteria to ultraviolet‐B radiation under iron‐replete and iron‐deficient conditions: Implications for underestimating the negative effects of UV‐B radiation

Iron deficiency has been considered one of the main limiting factors of phytoplankton productivity in some aquatic systems including oceans and lakes. Concomitantly, solar ultraviolet‐B radiation has been shown to have both deleterious and positive impacts on phytoplankton productivity. However, how iron‐deficient cyanobacteria respond to UV‐B radiation has been largely overlooked in aquatic systems. In this study, physiological responses of four cyanobacterial strains (Microcystis and Synechococcus), which are widely distributed in freshwater or marine systems, were investigated under different UV‐B irradiances and iron conditions. The growth, photosynthetic pigment composition, photosynthetic activity, and nonphotochemical quenching of the different cyanobacterial strains were drastically altered by enhanced UV‐B radiation under iron‐deficient conditions, but were less affected under iron‐replete conditions. Intracellular reactive oxygen species (ROS) and iron content increased and decreased, respectively, with increased UV‐B radiation under iron‐deficient conditions for both Microcystis aeruginosa FACHB 912 and Synechococcus sp. WH8102. On the contrary, intracellular ROS and iron content of these two strains remained constant and increased, respectively, with increased UV‐B radiation under iron‐replete conditions. These results indicate that iron‐deficient cyanobacteria are more susceptible to enhanced UV‐B radiation. Therefore, UV‐B radiation probably plays an important role in influencing primary productivity in iron‐deficient aquatic systems, suggesting that its effects on the phytoplankton productivity may be underestimated in iron‐deficient regions around the world.     

Identification and quantification of phytoplankton groups in lakes using new pigment ratios – a comparison between pigment analysis by HPLC and microscopy

1. Pigment analysis by high‐performance liquid chromatography (HPLC) combined with data analysis using the CHEMTAX program has proven to be a fast and precise method for determining the abundance of phytoplankton groups in marine environments. To determine whether CHEMTAX is applicable also to freshwater phytoplankton, 20 different species of freshwater algae were cultured and their pigment/chlorophyll a (Chl a) ratios determined for exponential growth at three different light intensities and for stationary growth at one light intensity. 2. The different treatments had a relatively insignificant impact on the absolute values of the diagnostic pigment/Chl a ratios, with the exception of cyanobacteria and cryptophytes for which the zeaxanthin/Chl a and alloxanthin/Chl a ratios varied considerably. 3. The pigment ratios were tested on samples collected in six different eutrophic Danish lakes during two summer periods using the CHEMTAX program to calculate the biomass of the phytoplankton groups as Chl a. The CHEMTAX‐derived seasonal changes in Chl a biomass corresponded well with the volume of the microscopically determined phytoplankton groups. More phytoplankton groups were detected by the pigment method than by the microscopic method. 4. Applying the pigment ratios developed in this study, the pigment method can be used to determine the abundance of the individual phytoplankton groups, which are useful as biological water quality indicators when determining the ecological status of freshwater lakes.     

Life in the dark: far-red absorbing cyanobacteria extend photic zones deep into terrestrial caves

Chlorophyll (Chl) f and d are the most recently discovered chlorophylls, enabling cyanobacteria to harvest near-infrared radiation (NIR) at 700–780 nm for oxygenic photosynthesis. Little is known about the occurrence of these pigments in terrestrial habitats. Here, we provide first details on spectral photon irradiance within the photic zones of four terrestrial cave systems in concert with a detailed investigation of photopigmentation, light reflectance and microbial community composition. We frequently found Chl f and d along the photic zones of caves characterized by low light enriched in NIR and inhabited by cyanobacteria producing NIR-absorbing pigments. Surprisingly, deeper parts of caves still contained NIR, an effect likely attributable to the reflectance of specific wavelengths by the surface materials of cave walls. We argue that the stratification of microbial communities across the photic zones of cave entrances resembles the light-driven species distributions in forests and aquatic environments.     

Effect of environmental factors on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium (Chroococcidiopsis sp.)

Abstract.The UV-screening pigment scytonemin is found in many species of ensheathed cyanobacteria. Past work has shown that the pigment is synthesized in response to exposure to UV-A irradiance. This study investigated the effect of other correlated stress factors including heat, osmotic and oxidative stress on the synthesis of scytonemin in a clonal cyanobacterial isolate ( Chroococcidiopsis sp.) from an epilithic desert crust. Stress experiments were carried out both in conjunction with UV-A irradiance and in isolation. Increases in both temperature and photooxidative conditions in conjunction with UV-A caused a synergistic increase in the rate of scytonemin production. In contrast, increased salt concentration under UV-A irradiance inhibited scytonemin synthesis. However, unlike the responses to temperature and oxidative stress, cells synthesized low levels of scytonemin under osmotic stress in the absence of scytonemin-inducing irradiance. These results suggest that scytonemin induction may be regulated as a part of a complex stress response pathway in which multiple environmental signals affect its synthesis.     

Changes in Pigment Composition and Photosynthetic Activity of Aquatic Fern (Azolla Microphylla Kaulf.) Exposed to Low Doses of UV-C (254 nm) Radiation

Changes in the content of pigments and rate of photosynthesis in Azolla microphylla Kaulf. fronds were measured during growth under solar and ultraviolet-C (UV-C) supplemented solar radiation. Maximum content of total chlorophyll (Chl) was observed on the 13^th day (termination of the experiment) of treatment in both control and treated plants. The treated plants had significantly lower total Chl and carotenoid contents than the control plants during the 1^st day of growth. After the 4^th day of exposure to UV-C supplemented solar radiation, the Chl and carotenoids accumulation increased in treated plants, so that the pigment concentration in the treated fronds was nearer to the control values after the 13^th day of treatment. Significant increase in UV absorbing pigments, anthocyanins, and flavonoids was observed at the 13^th day of treatment. In spite of the roughly similar photosynthetic pigment concentration, the photosynthetic activity measured as the rate of electron transport at photosystem 2 was only 65 % of the control values after 13 d of UV-C exposure. This revised version was published online in June 2006 with corrections to the Cover Date.     

LIGHT ACTION SPECTRA OF N2 FIXATION BY HETEROCYSTOUS CYANOBACTERIA FROM THE BALTIC SEA1

An on‐line, laser photo‐acoustic, trace gas detection system in combination with a stepper motor‐controlled monochromator was used to record semicontinuous light action spectra of nitrogenase activity in heterocystous cyanobacteria. Action spectra were made of cultures of Nodularia spumigena Mertens ex Bornet & Flahault, Aphanizomenon flos‐aquae Ralfs ex Bornet & Flahault, and Anabaena sp. and from field samples of a cyanobacterial bloom in the Baltic Sea. Nitrogenase activity was stimulated by monochromatic light coinciding the red and blue peaks of chl a, the phycobiliproteins phycocyanin (allophycocyanin) and phycoerythrin, and several carotenoids. Because nitrogenase is confined to the heterocyst, it was concluded that all photopigments must have been present in these cells, were involved in light harvesting and photosynthesis, and supplied the energy for N₂ fixation. The species investigated showed marked differences in their nitrogenase action spectra, which might be related to their specific niches and to their success in cyanobacterial blooms. Moreover, light action spectra of nitrogenase activity shifted during the day, probably as the result of changes in the phycobiliprotein content of the heterocyst relative to chl a. Action spectra of nitrogenase and changes in pigment composition are essential for the understanding of the competitive abilities of species and for the estimation of N₂ fixation by a bloom of heterocystous cyanobacteria.     

Widespread occurrence and unexpected diversity of red-shifted chlorophyll producing cyanobacteria in humid subtropical forest ecosystems

Discovery of red-shifted chlorophyll d and f in cyanobacteria has opened up new avenues to estimate global carbon fixation driven by far-red light. Shaded habitats in humid subtropical forest ecosystems contain an increased proportion of far-red light components relative to residual white light. After an extensive survey of shaded ecosystems within subtropical forests, wide occurrence of red-shifted chlorophyll-producing cyanobacteria was demonstrated by isolated Chl f-producing and Chl d-containing cyanobacteria. Chl f-producing cyanobacteria were classified into the genera of Aphanocapsa and Chroococcidiopsis and two undescribed genera within Leptolyngbyaceae. Newly isolated Chl d-containing Acaryochloris sp. CCNUM4 showed the closest phylogenetic relationship with Acaryochloris species isolated from marine environments. Acaryochloris sp. CCNUM4 produced Chl d as major photopigment, and Chl f-producing cyanobacteria use Chl a under white light conditions but Chl a + f under far-red light conditions. Their habitats are widely distributed in subtropical forest ecosystems and varied from mosses on limestone to macrophyte and freshwater in the streams and ponds. This study presents a significant advance in the knowledge of distribution and diversity of red-shifted chlorophyll-producing cyanobacteria in terrestrial ecosystems. The results suggest that Chl f-producing and Chl d-containing cyanobacteria might be important primary producers in far-red light dominant niches worldwide.