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Photosynthetic organisms have evolved a great variety of mechanisms to optimize their use of sunlight. Some of the clearest examples of adaptations can be seen by comparing photosynthesis in different species and in different individuals of the same species that grow under high and low light levels. While the adaptations of sun and shade higher plants have been relatively well studied, much less information is available on the photobionts of lichenized Ascomycetes. An important adaptation that can protect photosynthetic organisms from the potentially harmful effects of excess light is non-photochemical quenching (NPQ); NPQ can dissipate unused light energy as heat. Here we used chlorophyll fluorescence to compare the induction and relaxation of NPQ and the induction of electron transport (rETR) in collections of the same lichen species from exposed and from more shaded locations. All species have trebouxioid photobionts and normally grow in more exposed microhabitats but can also be readily collected from more shaded locations. Shade forms display generally higher NPQ, presumably to protect lichens from occasional rapid increases in light that occur during sunflecks. Furthermore, the NPQ of shade forms relaxes quickly when light levels are reduced, presumably to ensure efficient photosynthesis after a sunfleck has passed. The maximal relative electron transport rate is lower in shade than sun collections, probably reflecting a downregulation of photosynthetic capacity to reduce energy costs. We also compared collections of pale and melanized thalli from three species of shade lichens with Symbiochloris as their photobiont. Interestingly, NPQ in melanized thalli from slightly more exposed microhabitats induced and relaxed in a way that resembled shade rather than sun forms of the trebouxioid lichens. This might suggest that in some locations melanization induced during a temporary period of high light may be excessive and could potentially reduce photosynthesis later in the growing season. Taken together, the results suggest that lichen photobionts can flexibly adjust the amount and type of NPQ, and their levels of rETR in response to light availability.
Non-photochemical quenching (NPQ) plays an important role in protecting photosynthetic organisms from photoinhibition by dissipating excess light energy as heat. However, excess NPQ can greatly reduce the quantum yield of photosynthesis at lower light levels. Recently, there has been considerable interest in understanding how plants balance NPQ to ensure optimal productivity in environments in which light levels are rapidly changing. In the present study, chlorophyll fluorescence was used to study the induction and relaxation of non-photochemical quenching (NPQ) in the dark and the induction of photosynthesis in ten species of lichens, five sampled from exposed and five sampled from shaded habitats. Here we show that the main difference between sun and shade lichens is the rate at which NPQ relaxes in the dark, rather than the speed that photosynthesis starts upon illumination. During the first two minutes in the dark, NPQ values in the five sun species declined only by an average of 2%, while by contrast, in shade species the average decline was 40%. For lichens growing in microhabitats where light levels are rapidly changing, rapid relaxation of NPQ may enable their photobionts to use the available light most efficiently.
In our earlier work, we demonstrated that the oxidases tyrosinase (TYR), laccase (LAC), and a heme peroxidase (POX) occur widely in lichens. Here we report on the occurrence of another oxidoreductase enzyme, quinone reductase (QR) (EC 22.214.171.124). While QR has been reported to occur widely in other organisms, there is currently no information on QR activities in lichens. Here we present a survey of QR activity in 14 species of lichens. Results demonstrate that QR activity is readily detectable in all lichen species tested. However, activities vary greatly, with ‘jelly’ lichens in the genera Collema and Leptogium having the highest activities. QR, LAC and POX are all believed to have a role in extracellular hydroxyl radical production. However, in this study no correlation was found between the activities of these enzymes and the rates at which hydroxyl radicals were produced. Possible roles for QR in lichen biology are discussed.
Lichens often grow in microhabitats where they are exposed to severe abiotic stresses such as desiccation and temperature extremes. They are also often exposed to levels of light that are greater than lichen photobionts can use in carbon fixation. Unless regulated, excess energy absorbed by the photobionts can convert ground state oxygen to reactive oxygen species (ROS). These ROS can attack the photosynthetic apparatus, causing photoinhibition and photo-oxidative stress, reducing the ability of the photobionts to fix carbon. Here, we outline our current understanding of the effects of high light on lichens and the mechanisms they use to mitigate or tolerate this stress in hydrated and desiccated states. Tolerance to high light can be achieved first by lowering ROS formation, via synthesizing light screening pigments or by thermally dissipating the excess light energy absorbed; second, by scavenging ROS once formed; or third, by repairing ROS-induced damage. While the primary focus of this review is tolerance to high light in lichen photobionts, our knowledge is rather fragmentary, and therefore we also include recent findings in free-living relatives to stimulate new lines of research in the study of high light tolerance in lichens.
Some lichenized ascomycetes synthesize melanic pigments in their upper cortices when exposed to ultraviolet light and high solar radiation. Our previous work showed that melanized chloro- and cyanolichens from both high light and more shaded habitats were less photoinhibited than pale ones during controlled exposure to high light. However, protection from high light might not necessarily be the consequence of just sun-screening by melanins in upper cortices. An inherent problem with earlier experiments was that the photobionts of melanized thalli might have received more light than those beneath pale cortices. The photobionts may therefore have possessed other light-induced tolerance mechanisms that gave protection from photoinhibition. Here, we aimed to test directly the inherent tolerance of lichen photobionts to photoinhibition. The method involved removing the lower cortices and medullas of three lichen species, Cetraria islandica, Crocodia aurata and Lobaria pulmonaria, and exposing the photobionts to light from below. Results confirmed that most of the improvement in tolerance to photoinhibition in melanized lichens derives from fungal melanization in the upper cortex. However, in C. islandica, the most heavily melanized species, algae from melanized thalli possessed a significantly higher tolerance to photoinhibition than those from pale thalli, suggesting that photobionts can also adapt themselves to high light.
Tyrosinases are a widespread family of multicopper oxidase enzymes. In our earlier work, we identified the presence of tyrosinases in lichenized Ascomycetes based on their substratum specificity, sensitivity to inhibitors and molecular mass. Here, we present a more detailed characterization of a tyrosinase from the lichen Lobaria pulmonaria. We also compare tyrosinase activity with the activities of laccases and peroxidases, the other redox enzymes present in this species. The importance of tyrosinases in lichen biology was studied by testing their role in melanin synthesis. Laboratory experiments clearly showed that tyrosinases from L. pulmonaria resemble those from other lichens and in free-living fungi. While the tyrosinases can metabolize the melanin precursor L-DOPA, L-DOPA can also be metabolized by peroxidases and laccases. A field experiment showed that exposing shade-adapted L. pulmonaria to normal solar radiation induces L-DOPA melanin synthesis. Synthesis occurred when lichens were exposed to either direct sunlight, or placed under a wavelength-neutral filter that slightly reduced overall light. In lichens receiving unfiltered sunlight, melanin synthesis was accompanied by increased laccase activity; by contrast, no changes in enzyme activity occurred in lichens placed under the wavelength-neutral filter. Melanization was reduced by placing lichens under filters that removed UV-B, and prevented by filters that removed both UV-A and UV-B. Removing UV-B had no effect on enzyme activity, whereas removing both UV-A and UV-B increased tyrosinase activity. Results from this study indicate that under some conditions laccases may be involved in melanin synthesis, but they provide no evidence for a role for tyrosinases in melanization. Although high tyrosinase activities are widespread in lichens, many questions on the role of this enzyme in lichen biology remain to be answered.
In our earlier work, we demonstrated that the oxidases tyrosinase and laccase occur widely in lichens from the Peltigerales. Recently, we discovered the occurrence of another oxidoreductase, a heme peroxidase, in the Peltigeralean ‘jelly lichens’ Leptogium and Collema. Here we present the results of a survey of peroxidase activity in a range of lichens. In addition to the jelly lichens, strong peroxidase activity also occurs within the Peltigeralean genera Lobaria, Pseudocyphellaria and Sticta. Significant activity occurs in the cell wall, and, unlike laccase activity, peroxidase activity increases considerably following the rehydration of dry thalli. However, activity is absent from Peltigera and from the non-Peltigeralean species tested here. Electrophoretic investigation showed that lichen peroxidases are oligomeric. Possible roles for peroxidases in lichen biology are discussed.
In our earlier work, we demonstrated the presence of the multicopper oxidases tyrosinase and laccase in the cell walls of lichens from the Peltigerales, while these enzymes appeared to be absent in lichens from other orders. Likely roles for tyrosinase in lichens include melanin synthesis, the generation of quinones needed for laccase-mediated redox cycling, and the removal of harmful reactive molecules formed by this cycling. Non-Peltigeralean lichens will not need tyrosinase to detoxify laccase-generated radicals. However, many non-Peltigeralean lichens are often heavily melanized. Apparent absence of tyrosinase activity in these species prompted us to suggest that, in these lichens, melanins are probably synthesized by the polyketide pathway, which does not involve tyrosinase. Here, we surveyed intracellular tyrosinase activity in thallus homogenates from a range of lichens. Results showed that Peltigeralean species generally have much higher activities than species from other orders. However, the non-Peltigeralean lichen Dermatocarpon miniatum displays significant tyrosinase activity. In D. miniatum, tyrosinase differs from the corresponding enzyme from Peltigeralean lichens with respect to cellular location, substratum specificity, stability and pH optimum. Furthermore, unlike Peltigeralean lichens, in D. miniatum tyrosinase activity increased strongly following the rehydration of dry thalli. These differences are possibly a consequence of the role of tyrosinase in melanin synthesis rather than laccase-mediated redox cycling.
This review discusses the production of reactive oxygen species (ROS) by lichens and their possible roles. All organisms produce ROS, and production is increased by many abiotic and biotic stresses. Intracellular ROS production is generally considered to be harmful, and a variety of enzymic and non-enzymic scavenging systems exist to detoxify them. However, extracellular ROS formation has been suggested to play ‘positive roles’, particularly in the response of organisms to stress. Given their high stress tolerance, it is rather surprising that studies on extracellular ROS production by lichens have just started. Surveys of a wide range of lichens have shown that constitutively high rates of extracellular superoxide production occur in the Suborder Peltigerineae, but production appears to be absent in other groups. In some members of the Peltigerineae ROS production is stimulated by desiccation and wounding. It seems probable that the enzymes that produce the superoxide are laccases, based on first the types of substrates that lichens can break down, and second the dependence of the breakdown of these substrates on pH, temperature and the presence of inhibitors. While much more work is needed, we suggest that physiological roles of extracellular ROS production will be found to include defence against pathogens, melanization, and lignin breakdown.