Adaptation of Cyanobacteria to the Endolithic Light Spectrum in Hyper-Arid Deserts

Abstract

In hyper-arid deserts, endolithic microbial communities survive in the pore spaces and cracks of rocks, an environment that enhances water retention and filters UV radiation. The rock colonization zone is enriched in far-red light (FRL) and depleted in visible light. This poses a challenge to cyanobacteria, which are the primary producers of endolithic communities. Many species of cyanobacteria are capable of Far-Red-Light Photoacclimation (FaRLiP), a process in which FRL induces the synthesis of specialized chlorophylls and remodeling of the photosynthetic apparatus, providing the ability to grow in FRL. While FaRLiP has been reported in cyanobacteria from various low-light environments, our understanding of light adaptations for endolithic cyanobacteria remains limited. Here, we demonstrated that endolithic Chroococcidiopsis isolates from deserts around the world synthesize chlorophyll f, an FRL-specialized chlorophyll when FRL is the sole light source. The metagenome-assembled genomes of these isolates encoded chlorophyll f synthase and all the genes required to implement the FaRLiP response. We also present evidence of FRL-induced changes to the major light-harvesting complexes of a Chroococcidiopsis isolate. These findings indicate that endolithic cyanobacteria from hyper-arid deserts use FRL photoacclimation as an adaptation to the unique light transmission spectrum of their rocky habitat.

Identification of far-red light acclimation in an endolithic Chroococcidiopsis strain and associated genomic features: Implications for oxygenic photosynthesis on exoplanets

“…CCMEE 010 far-red cluster is distinct not only from the cluster in the related Chroococcidiopsis thermalis PCC 7203 but also from clusters in more distantly related strains such as the heterocyst-forming cyanobacteria ( Supplementary Figure 2 ). A Chroococcidiopsis -associated cluster recovered from an Atacama metagenome also did not show these changes ( Murray et al, 2022 ). Notably, psaF and psaJ were inserted between psbC and psbB , which has not been observed in any other FaRLiP clusters ( Gan et al, 2014 , 2015 ; Chen et al, 2019 ; Sheridan et al, 2020 ).…”

“…Such a low FaRLiP occurrence among desert strains of Chroococcidiopsis suggested that this photoacclimation mechanism might not be common among rock-inhabiting cyanobacteria. Enrichment cultures may nevertheless reveal it, for instance, in samples from Negev sandstone or the Atacama Desert ( Murray et al, 2022 ). It is possible that intense abiotic stress could result in reduced competition from other photosynthetic organisms ( Lacap-Bugler et al, 2017 ) and, consequently, a decreased evolutionary pressure to maintain a complex acclimation response.…”

“…The FaRLiP capacity of rock-inhabitant cyanobacteria in extreme environments has been poorly investigated. There has been one report focusing on the subject ( Murray et al, 2022 ), together with one report on the far-red apcE2 gene being present in the metagenome of endolithic communities from the Atacama Desert ( Antonaru et al, 2020 ). In fact, in hot and cold deserts, cyanobacteria take refuge in or under rocks, where the transmitted light is still sufficient for photosynthesis ( Cockell et al, 2009 ).…”

“…Depending on the mineralogical composition, cyanobacterial colonization can be endolithic, including beneath the rock surface within pores (cryptoendoliths) or in cracks or fissures (chasmoendoliths), but also hypolithic, at the rock–soil interface ( Wierzchos et al, 2011 ). Recently, chlorophylls d and f were reported for endolithic communities from gypsum, calcite, and sandstone from the Atacama and Namib deserts ( Murray et al, 2022 ), but these pigments were not detected in hypolithic communities from quartz pebbles in the latter desert ( Gwizdala et al, 2021 ). Red-shift carotenoids were also reported for endolithic communities (primarily composed of Chroococcidiopsis cyanobacteria) in ignimbrite rocks from the Atacama Desert ( Vítek et al, 2017 ).…”

Near infrared radiation-driven oxygenic photosynthesis contributes substantially to primary production in biofilms harboring chlorophyllf-containing cyanobacteria

“…In contrast, the ecological role of cyanobacteria with FaRLiP in natural habitats remains much less explored. Cyanobacteria with Chl f have been found in a variety of terrestrial (Behrendt et al, 2015(Behrendt et al, , 2010Zhang et al, 2019;Murray et al, 2022) and aquatic (e.g. Akutsu et al, 2011;Trampe and Kühl, 2016;Ohkubo and Miyashita, 2017) habitats.…”