Photosynthesis Research 34: 339-340, 1992. © 1992 Kluwer Academic Publishers. Printed in the Netherlands.
An overlooked symbiosis D.J. Hill
Department for Continuing Education, University of Bristol, Bristol BS8 1HR, UK Received 23 March 1992; accepted in revised form 29 June 1992
My father never isolated his scientific work and interests from his private life. The benefits of this were that he never missed an opportunity to widen his knowledge and understanding of the natural world. As a tribute to this I am giving a very brief anecdotal account of a chance find of a plant (a lichen-like symbiosis) which I found on holiday in France. H e said to me more than once that I should have published it at the first possible opportunity. But I didn't. I hope this, however brief, is better late than never. One of the interesting things about lichens is their ability to carry out photosynthesis at very low water potentials (Lange and Matthes 1981, Hawksworth and Hill 1984). This feature allows them to be poikilohydric and to thrive in characteristically dry inhospitable places. The algal symbionts which are responsible can only themselves thrive in these habitats within the lichen thallus. Indeed, Brock (1975) has shown that some lichen algae can photosynthesise at lower water potentials when in a lichen than when separated from the fungus. Of the 37 genera (Hawksworth and Hill 1984) which have been found as lichen symbionts, there are two major groups which are notably absent: Phaeophycae (brown algae) and Rhodophycae (red algae). The Phaeophycae have to some extent colonised the poikilohydric habitat of the upper seashore although in Britain the familiar Channel Wrack (Pelvetia canaliculata) is also a type of lichen in that it always has growing in its tissues a minute fungus (Mycosphaerella ascophylli) (Hawksworth 1988). The association is constant and truly symbiotic and both partners reproduce sexually. The Rhodophycae however is a group of exclusively aquatic algae which have virtually no ability to colonise land, nor are they widely recognised as forming symbiotic associations
with fungi. Thus, it seems possible that, in nature, the ability for algae to thrive in habitats where water potentials can get very low ig somehow associated with lichenisation and that if lichenised members of the Rhodophycae would have a better chance of colonising the terrestrial habitat. While enjoying a particularly pleasant family picnic at the edge of an idyllic river in the Cevennes National Park, France in July 1986, I was struck by the finding of a lichenqike plant growing on a bare rock half submerged by the river. It was not a species I had seen before nor was it similar to any I had seen described. It occurred 15-30 cm above the water level in the full sun. The rivers there run much fuller in winter when it had been presumably submerged. I collected sufficient material to send to Prof D. Hawksworth for examination. It proved to be a lichen-like symbiosis (mycophycobiosis) between the fungus Phaeospora lemaneae and a species of red alga probably Lemanea sp. (Hawksworth 1987). This also seemed to be the first report of a symbiosis involving a member of the Rhodophycae appearing in the lichenological literature (Hawksworth 1988). Both symbionts were reproducing sexually. The structure of the fungus has been described in some detail by Brierley (1913) but little is known of its development or of its physiological and ecological characteristics. Further research would need to establish whether the lichenisation enabled the Lemanea to survive desication while exposed during the summer months. One of the characteristics of lichens is that they have extremely high soluble cellular concentrations of carbohydrates (usually polyols) (Farrar 1976, Hawksworth and Hill 1984) which are apparently able to offer hy-
340 droxyl groups to replace lost water molecules in maintaining integrity of structure and macromolecules in the cell. K r e m e r (1978) has shown that c a r b o n is accumulated in Lemanea in the f o r m of trehalose and the heteroside floridiside b o t h capable of acting to some extent in the s a m e way that polyols do in most other lichens. O n e a u t h o r even r e p o r t e d mannitol, which is a well k n o w n fungal c a r b o h y d r a t e , f r o m Lemanea. H o w the presence of a fungal symbiont in lichens allows the alga to photosynthesise and thrive in drier m o r e inhospitable habitats than free living algae has never been fully reviewed, u n d e r s t o o d or investigated although it is a complex p h e n o m e n o n involving m o r e than just tolerance of low water potentials. It would also be interesting to k n o w m o r e a b o u t the photosynthetic mechanisms at such very low water potentials in these poikilohydric eukaryotic algae. So I learnt that even on holiday one continues to think and, indeed, let that invaluable asset of the researcher, imagination, work.
References Brierley WB (1913) The structure and life-history of Leptosphaeria Lernaneae (Cohn). Memoires of the Manchester Literary and Philosophical Society 57:1-21 Brock TD (1975) The effect of water potential on photosynthesis in whole lichens and in their liberated algal componants. Planta (Heidelb.) 124:13-23 Farrar JF (1976) Ecological physiology of the lichen Hypogymnea physodes. III. The importance of the rewetting phase. New Phytol 77:115-125 Hawksworth DL (1987) Observations on three algicolous microfungi. Notes R Bot Gard, Edinb 44:549-560 Hawksworth DL (1988) The variety of fungal-algal symbioses, their evolutionary significance and the nature of lichens. Bot J Linn Soc 96:3-20 Hawksworth DL and Hill DJ (1984) The Lichen-Forming Fungi. Blackie, Glasgow Kremer BP (1978) Aspects of CO2-fixation in some freshwater Rhodophycae. Phycologia 17:430-434 Lange OL and Matthes U (1981) Moisture-dependent CO 2 exchange of lichens. Photosynthetica (Prague) 15:555-574
An overlooked symbiosis D.J. Hill
Department for Continuing Education, University of Bristol, Bristol BS8 1HR, UK Received 23 March 1992; accepted in revised form 29 June 1992
My father never isolated his scientific work and interests from his private life. The benefits of this were that he never missed an opportunity to widen his knowledge and understanding of the natural world. As a tribute to this I am giving a very brief anecdotal account of a chance find of a plant (a lichen-like symbiosis) which I found on holiday in France. H e said to me more than once that I should have published it at the first possible opportunity. But I didn't. I hope this, however brief, is better late than never. One of the interesting things about lichens is their ability to carry out photosynthesis at very low water potentials (Lange and Matthes 1981, Hawksworth and Hill 1984). This feature allows them to be poikilohydric and to thrive in characteristically dry inhospitable places. The algal symbionts which are responsible can only themselves thrive in these habitats within the lichen thallus. Indeed, Brock (1975) has shown that some lichen algae can photosynthesise at lower water potentials when in a lichen than when separated from the fungus. Of the 37 genera (Hawksworth and Hill 1984) which have been found as lichen symbionts, there are two major groups which are notably absent: Phaeophycae (brown algae) and Rhodophycae (red algae). The Phaeophycae have to some extent colonised the poikilohydric habitat of the upper seashore although in Britain the familiar Channel Wrack (Pelvetia canaliculata) is also a type of lichen in that it always has growing in its tissues a minute fungus (Mycosphaerella ascophylli) (Hawksworth 1988). The association is constant and truly symbiotic and both partners reproduce sexually. The Rhodophycae however is a group of exclusively aquatic algae which have virtually no ability to colonise land, nor are they widely recognised as forming symbiotic associations
with fungi. Thus, it seems possible that, in nature, the ability for algae to thrive in habitats where water potentials can get very low ig somehow associated with lichenisation and that if lichenised members of the Rhodophycae would have a better chance of colonising the terrestrial habitat. While enjoying a particularly pleasant family picnic at the edge of an idyllic river in the Cevennes National Park, France in July 1986, I was struck by the finding of a lichenqike plant growing on a bare rock half submerged by the river. It was not a species I had seen before nor was it similar to any I had seen described. It occurred 15-30 cm above the water level in the full sun. The rivers there run much fuller in winter when it had been presumably submerged. I collected sufficient material to send to Prof D. Hawksworth for examination. It proved to be a lichen-like symbiosis (mycophycobiosis) between the fungus Phaeospora lemaneae and a species of red alga probably Lemanea sp. (Hawksworth 1987). This also seemed to be the first report of a symbiosis involving a member of the Rhodophycae appearing in the lichenological literature (Hawksworth 1988). Both symbionts were reproducing sexually. The structure of the fungus has been described in some detail by Brierley (1913) but little is known of its development or of its physiological and ecological characteristics. Further research would need to establish whether the lichenisation enabled the Lemanea to survive desication while exposed during the summer months. One of the characteristics of lichens is that they have extremely high soluble cellular concentrations of carbohydrates (usually polyols) (Farrar 1976, Hawksworth and Hill 1984) which are apparently able to offer hy-
340 droxyl groups to replace lost water molecules in maintaining integrity of structure and macromolecules in the cell. K r e m e r (1978) has shown that c a r b o n is accumulated in Lemanea in the f o r m of trehalose and the heteroside floridiside b o t h capable of acting to some extent in the s a m e way that polyols do in most other lichens. O n e a u t h o r even r e p o r t e d mannitol, which is a well k n o w n fungal c a r b o h y d r a t e , f r o m Lemanea. H o w the presence of a fungal symbiont in lichens allows the alga to photosynthesise and thrive in drier m o r e inhospitable habitats than free living algae has never been fully reviewed, u n d e r s t o o d or investigated although it is a complex p h e n o m e n o n involving m o r e than just tolerance of low water potentials. It would also be interesting to k n o w m o r e a b o u t the photosynthetic mechanisms at such very low water potentials in these poikilohydric eukaryotic algae. So I learnt that even on holiday one continues to think and, indeed, let that invaluable asset of the researcher, imagination, work.
References Brierley WB (1913) The structure and life-history of Leptosphaeria Lernaneae (Cohn). Memoires of the Manchester Literary and Philosophical Society 57:1-21 Brock TD (1975) The effect of water potential on photosynthesis in whole lichens and in their liberated algal componants. Planta (Heidelb.) 124:13-23 Farrar JF (1976) Ecological physiology of the lichen Hypogymnea physodes. III. The importance of the rewetting phase. New Phytol 77:115-125 Hawksworth DL (1987) Observations on three algicolous microfungi. Notes R Bot Gard, Edinb 44:549-560 Hawksworth DL (1988) The variety of fungal-algal symbioses, their evolutionary significance and the nature of lichens. Bot J Linn Soc 96:3-20 Hawksworth DL and Hill DJ (1984) The Lichen-Forming Fungi. Blackie, Glasgow Kremer BP (1978) Aspects of CO2-fixation in some freshwater Rhodophycae. Phycologia 17:430-434 Lange OL and Matthes U (1981) Moisture-dependent CO 2 exchange of lichens. Photosynthetica (Prague) 15:555-574
