Acquisition of green algal photobionts enables both chlorolichens and chloro-cyanolichens to activate photosynthesis at low humidity without liquid water.

Abstract

Cyanobacteria require liquid water for photosynthesis, whereas green algae can photosynthesise with water vapour alone. We discovered that several Lobaria spp. which normally have cyanobacteria as the sole photobiont, in some regions of the trans-Himalayas also harboured green algae. We tested whether green algal acquisition was: limited to high elevations; obtained from neighbouring chloro-Lobaria species; enabled photosynthesis at low humidity. Lobaria spp. were collected from 2000 to 4000 m elevation. Spectrophotometry quantified green algal abundance by measuring chlorophyll b (absent in cyanobacteria). Thalli cross-sections visually confirmed green algal presence. We sequenced gene regions: Lobaria (ITS-EF-1α-RPB2), green algae (18S-RBC-L) and Nostoc (16S). Phylogenetic analysis determined myco-photobiont associations. We used a custom closed-circuit gas exchange system with an infrared gas analyser to measure CO2 exchange rates for desiccated specimens at 33%, 76%, 86% and 98% humidity. Cross-sections revealed that the photobiont layers in putative cyano-Lobaria contained both cyanobacteria and green algae, indicating that they should be considered chloro-cyanolichens. Chloro-Lobaria had no visible cephalodia nor cyanobacteria in the photobiont layer. Chloro-Lobaria and chloro-cyano-Lobaria had comparable levels of chlorophyll b. Chloro-Lobaria usually contained Symbiochloris. Chloro-cyano-Lobaria mainly associated with Parachloroidium and Nostoc; infrequently with Symbiochloris, Apatococcus, Chloroidium, Pseudochlorella, Trebouxia. Sequences from two green algal genera were obtained from within some thalli. Desiccated specimens of every Lobaria species could attain net photosynthesis with light exposure and 33% humidity. CO2 exchange dynamics over a five-day period differed between species. At all elevations, chloro-cyano-Lobaria spp. had abundant green algae in the photobiont layer, but green algal strains mostly differed to those of chloro-Lobaria spp. Both chloro-Lobaria and chloro-cyano-Lobaria were capable of conducting photosynthesis without liquid water. The data strongly suggest that they attained positive net photosynthesis.