Light and adaptive responses in red macroalgae: an overview.
L. Talarico and G. Maranzana,
Department of Biology,University of Trieste, Via L. Giorgieri 10, I-34127 Trieste, Italy
Abstract. The most recent research shows an increased interest on algal photobiology following the modifications of light spectral composition induced by the ozone depletion in the atmosphere. The consequences of this change on the macrophytic red algae, that possess accessory light harvesting complexes, are currently uncertain. Moreover the underwater light field of coastal waters, where most macroalgae are living, has been well characterized only in the latest years. The presence and the variability of light components, such as red, far red, green, blue and ultraviolet radiations in these environments, at different depths, have arisen the question if red macroalgae are light intensity or/and light quality adapters. In this paper various adaptive responses of red algae, both in the field and under culture, are discussed in order to compare the physiological with the ecological results. From all these studies it seems to be ascertained that red algae are both intensity and light quality adapters. In particular the light quality and, overall, the modulation of the ratios between spectral components seem to play the role of photomorphogenic signals regulating algal metabolism and growth. Short and long term responses, and potential strategies and mechanisms for adaptation to light at individual, cellular and molecular levels, are discussed with special reference to the photosynthetic equipment.
Key words: light, red algae, acclimation, adaptation, growth, phycobiliproteins, photosynthetic equipment
Light is subjected to momentary, diurnal and seasonal changes both in irradiance and in spectral distribution. Underwater, both irradiance and light spectral composition can vary depending on: 1) incident solar radiation (angular distribution), 2) the inherent optical properties of the water body (absorption and scattering processes), 3) the depth of the water column, 4) the presence of dissolved organic matter (DOM), gilvinic substances, particulate matter (tripton) and plankton .
Underwater light field, pigment composition and growth
In coastal waters, where most macroalgae are living [2-5], the radiations interact also with the macrophytic components and with the type of sediments. This results into relevant variations of light spectral composition and irradiance with respect to the incident light. This has been demonstrated by measuring the downward and upward radiations on natural and simulated algal canopies both in the field and in aquaria [6-9]. Variable spectral proportions (i.e. red : far red (R:FR); blue : red (B:R); green : red (G:R); blue : green (B:G), affecting the relative pigment composition and possibly acting as photomorphogenic signals , were detected. Both downward and upward radiations were enriched by G and FR light, depending on algal composition. This fact appears to be very important in that the G:R light are the main light qualities absorbed by PSII (through phycobilisomes, the additional external antenna of red algae) and also genes encoding PBS a , b , and g subunits and linker polypetides are expressed by G and R pulses .
Furthermore variations in R:FR, and B:R ratios measured (at the end of the day) over a two-year period, in air and underwater at different depths, showed a positive correlation with the daylengths and temperatures. It was suggested for these ratios the role of signalling diurnal and annual photoperiods by Figueroa . Under laboratory conditions diurnal changes of these ratios were well correlated with diurnal changes in photosynthetic pigment content in the red algae Porphyra laciniata and Chondrus crispus .
In the field it has been demonstrated by Lüning  that seaweeds start the growth in winter and reduce it in summer. Seasonal growth was well correlated with temperature, salinity and light intensity. No nitrate or phosphate were correlable to the same extent. It is true that especially nitrate exerts direct control on growth cycle (its control is only temporaneous), but just as much as different light intensities that can be favourable or adverse. In the laboratory some brown algae (i.e. Pterigophora californica), cultured under white light simulating the annual cycle of daylength, the good synchronisation among annual cycles of daylength (even though shortened from twelve months to 6, 3 months) and new blade formation, indicated that there exist growth annual cycles regulated by the daylength . So it can be said that daylength (not temperature) is a driver for photoperiodic systems and a synchronizer for circannual systems.
By using white and monochromatic lights, alone or combined in different proportions at low and high irradiances, both short-term and long-term experiments on various species of Porphyra (P. umbilicalis, P. leucosticta, P. laciniata), Chondrus crispus, Corallina elongata, Plocamium cartilagineum, Palmaria palmata [14-19], and Audouinella saviana [21-23] indicated that both irradiance and spectral composition greatly influence pigment composition, metabolism and growth of red macroalgae. The diverse growth responses to similar radiations (especially for B and R wavelength ranges) that were observed in these species, refer to different sun-shade acclimation due to their habitats. It has been suggested that three main photoreception systems i.e B/UV light photoreceptor (BLP), green light (GPL) and R/FR light photoreceptor (phytochrome-like molecule) might be involved in such a control [19, 20].
Light Acclimation Strategies.
To survive under constantly changing light fields red algae have evolved a number of long and short term adaptation strategies, involving changes in anatomy of the thallus at individual level, changes in cell wall, differences in chloroplast morphology and thylakoid organisation at cellular level (long term adaptation), and alterations in pigmentation, in photosynthetic membrane composition and functionality at molecular level (short term acclimation).
Long term adaptation
Shade growing macroalgae have typically either larger chloroplasts with more thylakoids per chloroplast, or equally sized and organised, but much more numerous chloroplasts, than the sun-growing algae. In general red algae growing under high light have the lowest, and those growing under low light, the greatest amounts of phycobiliproteins per cell and the highest number of phycobilisomes per square micrometer , but environmental conditions, such as nutrient cycles and diurnal and annual daylength cycles, can modify the relative pigment content , the number of thylakoids and/or the amount of phycobilisomes (PBSs), when present, per square micrometer. In fact in the natural environment, biliprotein contents have seasonal variations that may be inversely related to the solar radiation, as it was seen over a three year sampling in Gracilaria verrucosa . PBSs presence and size is not constant over the annual cycle, being their formation not directly related to biliprotein content, as demonstrated for Halopythis incurvus . This means that not always to high biliprotein contents correspond well structured PBSs. On the contrary the highest amounts of these pigments appear to be a constraint for PBSs formation, as we have seen in the field  and, for example, in cultures under high green light which stimulated maximum increase of R-phycoerythrin .
The same species, i.e.Plocamium cartilagineum , living at two different depths can have same sized chloroplasts with similar number of thylakoids per chloroplast, and similar number of phycobilisomes per each thylakoid. Acclimation to lower light was achieved by a decreased thickness of the cuticle, and an icreased number of photosynthetizing cells in the cortical regions with a reduction of the medullary region, in the depth growing thalli. As regards photosynthetic pigment content the greater increase of R-phycoerythrin (R-PE), compared to the other pigments, in depth-thalli demonstrated an adaptive response to a possible G-enriched light spectrum . It is reasonable to speculate that also the different photosynthetic responses observed in Plocamium cartilagineum collected at different depths, in different seasons from the Southern North Sea , may reflect a possibly similar morphological adaptation to depth. These thalli showed high sensitivity to PAR+UV treatment. Decline of photosynthetic efficiency was observed after only five minutes of exposure and had low rate of recovery. However removal of UV-B had no effect on thalli collected from 4 m, but did improve the in vivo fluorescence of PSII, as the ratio of variable (Fv) to maximal (Fm) Fluorescence, in P. cartilagineum collected from 2 m. Unfortunately possible differences in anatomy, ultrastructure or pigment composition (PBS assembly) were not analysed in these experiments.
In contrast with Plocamium, Iridea cordata, collected during austral Summer from ice-free and ice-covered sea waters, did not show relevant differences in the organisation of the cortical and medullary regions between ice-fre and ice-covered thalli, but in the thalli living at higher irradiance were observed chloroplasts with a reduced thylakoid system with respect to those growing under ice . Both R-PE and R-phycocyanin (R-PC) contents were much higher in ice-free thalli compared to the ice-covered thalli, being R-PE the most abundant. Since biliproteins were not assembled into PBSs, functions other than light harvesting may be attributed to these pigment i.e. nitrogen reserve and possibly photoprotection. In fact, even though light fields have not been measured when thalli were collected, according to the informations provided by the Italian National Council of Research (unpublished data), in Antarctica the irradiance values measured in summer in the same site, were about five times higher in ice-free than in ice-covered water. Viceversa the much higher amount of carotenoids (CAR) in the ice-covered algae respect with the ice-free ones, reflects an accessory pigment function for CAR, in widening the absorption spectrum toward B. Also approximate indication of different light spectra, in presence or in absence of ice, was indirectly deduced from the different 498lmax/565 lmax peak relative ratios in the R-PE absorption spectra, as indicative for phycourobilin (PUB) to phycoerythrobilin (PEB) chromophore composition. In fact, the higher value (0.9) of this ratio in ice-covered thalli compared to that (0.4) of ice-free thalli may indicate an enrichment in the B, G shorter wavelengths under ice (Talarico and Maranzana unpublished data).
In Audouinella saviana, cultured under different light regimes, changes in morphology were observed mainly in the branching of the thalli, thickness of the cell wall, the number of grooves in the cell surface and the formation of reproductive structures. There were adaptations apparent at the cell walls as light intensity was increased and viceversa. These changes in thickness and grooving may be interpreted as a mechanism by which the alga increases the surface area of its cell wall that it presents to the incident light, and also a defense mechanism against excess light .
Under different light qualities growth and cell wall adaptive responses appear to be different in sun- or shade-acclimated algae. For example in Porphyra and Palmaria [14, 30], in thalli exposed to B, compared to R light grown thalli, cell wall thickness did not increase as much as under R. Growth and cell wall thickness (where abundant matrix polysaccharides were also present) were better stimulated by R light. Viceversa in Audouinella, behaving as a shade plant, B light stimulated greater increases of biomass and cell wall thickening than R light, which did not induce increments of both biomass and cell wall thickness. Furthermore structural polysaccharides were abundant in the cell wall .
Short term acclimation
Short term adaptation implies either rapid increments/decrements or the reorganisation of already existing components within (PSI and PSII reaction centres) and nearby the photosynthetic membrane (PBS insertion/detachment).
At molecular level, short term acclimation to varying light conditions involves a complex of regulatory mechanisms for rapid activation of direct/mediated biosynthetic processes, aimed at optimizing photosynthetic activity and photoprotection to prevent possible photodamage in photosynthetic membranes. Photoprotection can be achieved through dynamic photoinhibition (the main regulatory process of photosynthesis) [31, 32], through photoprotective compounds such as pigments themselves (carotenoids, chlorophylls, phycobiliproteins), PAR-transparent mycosporine-like Aminoacids (MAAS), and through detoxification from active oxygen species (H2O2, O2-, 1O2, .OH). Little is known about the capacity or inducibility of antioxidant enzyme systems in macroalgae .
Photosynthetic equipment and short term responses.
Thylakoids of red algae contain all the functional elements needed for trapping and trasducing light energy into chemical energy forms ATP and NADPH, as in higher plants. The reactions are carried out by membrane spanning protein complexes, associated cofactors and peripheral proteins. Some of these complexes PSI (PSI/bound LHCI), PSII (PSII/bound inner antennae) (and the peripheral light harvesting complex) bind Cholorophyll (CHL). CHL bound to PSII represents less than 20% of total CHL within the cell, thus the greatest CHL amount is in PSI. Other complexes, such as Cytochrome Complex (Cytb6f = PFparticles=Cyt-PSI complexes) and ATP Synthase (also known as coupling factor, CF0/CF1) do not bind CHL . In the red algae there exist supplementary external antennae, the phycobilisomes (PBSs)[21, 35, 36], that are linked to PSII through a high molecular weight core-membrane linker (LCM) carrying the chromophore Phycocyanobilin (PCB), with allophycocyanin-B (APC-B) and APC680 as energy terminal acceptors. LCM, formerly known as anchor protein, does correspond to the EF (exoplasmic fracture particles) particles seen by electron microscopy [37, 38]. They are considered CHL a-protein complex binding sites of PBS to PSII and are connecting the PBS core to the membrane-integrated PSII . Particles of 7 nm of diameter (PF protoplasmic freeze-fracture) on the stromal size, are considered PSI-cytochrome complexes .
Each PBS rod is made up by different proportions of PC and PE which are stacked in hexameric disks (double trimers (ab)3 for PC and APC and (ab)6g for R-PE) that are considered the functional units. A large number of colourless linker polypetides with various molecular weights (from 27 KDa up to 130 KDa) have been characterised. They promote face to face aggregations of PE and PC functional units and additionally cause tail to tail joining of hexameric assemblies to form larger aggregates such as the peripheral rods. These colorless proteins also serve to connect the rods to the core and to direct PBS assembly and its attachment to the thylakoid surface [40, 41].
Following the previous suggestions derived from electron microscopy studies on purified biliproteins [42-47] X-ray diffraction more recent studies on biliprotein crystal structures have confirmed that linker polypeptides are mainly located in the central cavity of the hexamers. Thus PBS consists of both pigmented phycobiliproteins (about 80% of the PBS mass) and non-pigmented (about 20%) linker polypeptides . The brilliant colors of the biliproteins originate mainly from covalently-bound, open-chain tetrapyrrole chromophores, the phycobilins, linked to the apoprotein [48, 49]. As many as three chromophores may be bound to a single a- , b- or g- subunit. Chromophores are generally bound to the polypeptide subunits (a, b or g) at conserved positions, either by one cisteynil thyoether linkage through the pyrrole ring A or by two cisteynil thyoether linkages on both the A and the D pyrrole rings . Thus they are maintained in an extended conformation by the apoprotein environment, as demostrated for C-PC in vitro. Infact when denatured, changes in the C-PC absorption spectra were observed toward the shorter wavelengths (being the 340 nm peak absorbance increased) as a result of the chromophore cyclic conformation . Cyclic chromophores have a lower visible and a higher near-UV absorbance than an extended conformation . Remarkable spectroscopic diversity exhibited by biliproteins are generated by: 1) chemically distinct chromophores with varying number of double bounds, 2) chemically distinct chromophore-protein linkages (bilins may be singly or doubly linked to the polypeptide chain), 3) distinctive chromophore environments contributed by the different polypetide chains. Other elements contributing the spectral diversities include chromophore-chromophore, chromophore-apoprotein interactions and conformational changes both in the chromophores and in the apoproteins. These latter can be reversible, as it was demonstrated by Scheer and coworkers (1995) [50-52] for the reversibly photochromic a sub-unit of phycoerythrocyanin (a-PEC) from the Cyanophyte Mastigocladus laminosus. Under B irradiation cycles, the absorption spectra of this a sub-unit showed a shift of the visible peak (absorption maximum) from about 570 nm to about 505 nm and a line broadening of the 570 nm band. These spectral changes, named photochemistry type I and type II, respectively, were due to the isomerization of the phycoviolobilin chromophore (PVB) between rings C and D, to different interactions between the chromophore (PVB) and the apoprotein of a-PEC subunit, as well as to changes in conformation of PVB-chromophore and PEC-apoprotein [51, 52]. Among the PAR wavelengths B is the most energetic radiation and thus it can induce such reversibly photochromic changes in biliproteins . It might be thought that also the shorter near-B radiations, such as the even more energetic UV wavelengths (UVA) may act in a similar way.
PBS is a highly efficient system in transferring energy to the PSII reaction centres. Any particular PBS may serve four or more PSII reaction centres . Energy is transferred, via PE ->PC-> APC, to PSII reaction centres through chromophores (PUB, PEB, PCB) differently positioned [55-57] along the transfer channel of PBS rods. The APC, forming the PBS core together with the terminal acceptors (PCB-carrying LCM and few diverse APCs), is the most stable component and it can be thought as a membrane pigment. The EF particles (10 nm of diametre), CHL-PSII binding sites, do contain APC-B and APC680 as final energy emitters. Fluorescence emission spectra of in vitro biliproteins (at ambient temperature and neutral pH) have peaks within 578-585 nm range for PE, 637-660 nm for PC and 660 nm for APC. Isolated intact PBS have final emission within 670-675 nm [40, 58]. The discrepancy between PBS final emission and APC final emission have demonstrated the existence of different APC forms (APCI and APC-B) emitting at 673-680 nm. These are strictly associated to CHL of PSII.
At low W light the number of PSI reaction centres (PF) P700 is higher than PSII reaction centres (P680) and it increases as irradiance increases. It has been demonstrated for some red algae cultured under monochromatic light that PSI/PSII was increased from 1:1 to 3:1 . This experiment indicated that under monochromatic light PSI represents a variable component of the photosynthetic membrane and that there exists a stoichiometric balance between PSI and PSII, activated selectively by l max550 (G) for PSII and l max699(R) for PSI radiations. Within PBS antenna, in contrast with APC core, R-PC and R-PE can vary considerably both in the short and the long term, depending on growth conditions such light quality and quantity, nutrient (especially nitrogen) availability, annual cycle.. .
Are red algae light quality adapters?
The red macroalgae, have been long considered only intensity adapters because in ecological studies (relating pigment content to photosynthetic rates and to vertical distribution), white and monochromatic light seemed to induce the same effect on pigment content, independent of algae distribution. On the contrary many experiments [15-19] demonstrated that different wavelength light sources, besides affecting metabolism, and growth [60-63, 12] produce finely modulated responses in the relative pigment composition, and PBSs structure [21-23]. One can reasonably say that all these red algae are much sensitive to spectral light composition. An exciting example is given by Palmaria palmata collected from Spitzbergen (Norway) and cultured in outdoor tanks exposed to natural solar radiation. Various parts of UV radiation were successively cut off by filters selective for UV different wavelength ranges (less than 295 nm, 320 nm, 400 nm respectively). The degree of photoinhibition, estimated by measuring the in vivo fluorescence of PSII (Fv to Fm ratio) during the course of the day, was clearly differentiated in different UV ranges, having the UV-B a much stronger effect than UV-A or PAR in relation to the irradiance (mW m-2 UV-B versus W m-2 UV-A). Differently from brown algae, photosynthetic efficiency (i.e. non saturated photosynthetic rate) was progressively higher (the degree of photoinhibition decreased progressively) as more of the shorter wavelengths were successively cut off. This alga was clearly selective in its regulatory processes of photosynthesis.
It would have been interesting to know more about biliprotein content, spectral features of biliproteins extracts and to test if biliproteins were free within the stroma or assembled into PBSs. In fact possible spectral changes in free-biliprotein absorption/fluorescence spectra might indicate photochromic changes both in the chromophore and/or in the apoprotein environment. To what extent the confomational changes, (that we have seen to be possibly induced by high energy wavelengths), might be involved as a mechanism for photoprotection? And also more detailed information about PBS presence/construction/detachment would have been useful, because in intact PBS, isolated from Palmaria palmata, the UV wavelengths below 300 nm, caused more disruption of phycobilisome energy transfer. This disruption was observed as a greater phycoerythrin fluorescence and less fluorescence from the phycobilisome core, than in higher UV wavelengths . Which molecular changes (different spatial and/or conformational arrangement?) have possibly occurred within PBS, to promote energy transfer disruption? If present on the thylakoid surface, in which way do the PBSs modulate the energy transfer within the transfer channel? Due to the plasticity of both PBS-complex and its biliproteic and linker components, it is reasonable to speculate that PBSs may have a potential role in photoprotection , as they do in PARnearUV light-harvesting.
Red algae are also chromatic adapters, but this assumption cannot be based only on relative pigment content changes. Adaptation to various light spectra might be based on mechanisms different from pigment relative proportions, such as photochemistry type I and type II, already seen in the a -PEC subunit of phycoerythrocyanin [51, 52]. Therefore altered pigment composition only may be not sufficiently indicative for chromatic adaptation. Ultrastructural observations are also needed to verify PBSs presence and construction, because relatively high biliprotein content does not necessarily mean well assembled and functioning antennae. It might mean also nitrogen storage or dissipation of excess energy during photoinhibition.
Chromatic adaptation and role of phycoerythrin g -subunits.
The ability to alter pigment composition of the PBS rods according to the quality of light (known as chromatic adaptation), is largely found in many but not all Cyanophyta and different adapting ways for hemidiscoidal PBSs have been described by combined biochemical and ultrastructural studies . For example in the Cyanophyte Calothrix sp. under G light, PE to PC ratio was 3 to 1 in the cell. Correspondly TEM micrograph of the isolated PBSs showed four stacks per rod. Many attempts have been made to isolate the photoreceptor regulating this process by identifying GL/RL reversible molecule(s) with no success. In early work it was thought to be the APC itself. Up to now it is known that genes encoding PBS a , b , g subunits and linker polypetides are expressed by G and R pulses  and this approach is promising for better results in identifying such a photoreceptor. Interestingly, only PE containing Cyanophytes are able to adapt chromatically, not those containing PEC which has an absorption spectrum widened towards the B-G region. In these Cyanophytes there exist inducible and constituvely expressed PEs. Only recently, g sub-units, which were previously believed to occur only in red algae, have been found to be associated with PE hexamers in Cyanophyta [64, 41]. PE complexes (forming PBS rods) contain in their central cavity either non-chromophorilated linker proteins or chromophore-bearing g subunits. An evolutionary tendency to attach as many bilins (chromophores) as possible to PE complexes, a process that involves not only the PE subunits themselves (a , b , g ) but also the linker polypetides (converting them into g sub-units), may be recognized . This capacity would account for reorganisation of PE/PC within PBS rods under certain light wavelengths (chromatic adaptation) involving the linker function of the g subunit. Consequently the modified external antenna would promote the PSII/PSI balance which accounts for the photosynthetic response. In red algae, in the unicellular Porphyridium cruentum cultured under B, for example, CHL was equally distributed between PSII and PSI so that the reaction centres were balanced, whereas the increase of G to R ratio determined a decline of PSI reaction centres and an increase of PSII . Thus there was an imbalance between PSI (CHL is mainly complexed into PSI) and PSII, resulting into a different rate of energy spillover from PSII to PSI.
In the red macroalgae, the most abundant pigment is R-PE [66, 67] with g and g subunits . The PE g units are bifunctional phycobiliproteins that act as light-harvesting phycobiliproteins and as linker-proteins . In Audouinella saviana under B, R-PE underwent spectral changes, that were interpreted as indicative of molecular rearrangements . Similarly to Cyanophytes, R-PE of red algae might play a role in adaptation to sudden irradiance and light spectral changes with its light-harvesting and linker function (through the g subunits) within PBSs. Furthermore R-PE may be considered an ecological advantage for algae living in sublittoral zones. In fact, among all the biliprotein subunits, the g- polypetyde carries the greatest number of PUB chromophores capable to extend the biliprotein absorption spectrum toward the B/G shortest wavelengths.
All these examples demonstrate how many strategies red macroalgae have adopted, to cope with drastic changes in light fields, at individual, at cellular and at molecular levels.
As regards the adaptive responses of the photosynthetic equipment, many questions are still open. The role of biliproteins assembled into PBSs at PAR low irradiances may be individuated in an enhancement of PSII activity, thus optimizing photosynthetic efficiency. Under different light qualities this antenna promotes reorganisation of intra-thylakoidal complexes by varying PSII to PSI ratios in order to balance available photon energy distribution between PSII and PSI, being the PSI the most variable within the membrane. Less clear is how these pigments (both assembled into PBSs or not) are acting when sudden photon excess and drastic photon composition changes are occurring. If the PBS basic size/shape and biliprotein composition ranges may be the result of long term light adaptation, PBS must be also a prompt system for facing a temporary white light excess or drastic spectral changes in the light components. One strategy may be similar to higher plants, where LCHII (inner antenna) is detached from the rest of PSII without a degradation of its molecular components [68, 69, 27, 34]. A reversible PBS detachment would occur with the reasonable involvement of the PBS linker polypeptides (particularly LCM and g subunits). Such event should occur contemporarily or prior than the photoprotective (photoinhibition) mechanisms within photosynthetic membrane may take place. Such event would imply an increased amount of free biliproteins within the stroma. Since these aggregates with their subunits have photochromic properties [51, 52], they might be involved to some extent in energy dissipating processes, as suggested by Lebert (1998) , to prevent the possible photodamage of the sensitive PSII as irradiance increases. By taking into account that PBS mass represents anyway some kind of selective barrier to excess light energy, if it remains attached (or dethached but intact within the stroma), another strategy might be a PBS inner regulatory mechanism, driving spatial and conformational rearrangements of chromophore-protein environments along the energy tranfer channel (with a presumable involvement of PBS-linker proteins). These rearrangements would modulate/disrupt light energy to be transferred to PSII, as demonstrated for PBSs in vitro .
To understand the photochemical processes within PBS of red algae a greater knowledge of reversibly photochromic properties of biliprotein-subunits/linkers assemblage are needed at molecular level. Moreover, further studies on their regulatory mechanisms, including the individuation of the photoreceptor(s) mediating such a regulation, are necessary. This would allow to better determine the contribution of PBSs in evaluating the photosynthetic responses to different light regimes and possibly the contribution of assembled or not assembled biliproteins in protection of the photosystems from excess energy. On this profile, combined and integrated physiological, molecular and ultrastructural approaches should be encouraged .
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