Reading and surviving the harsh conditions in desert biological soil crust: the cyanobacterial viewpoint.

Biological soil crusts (BSCs) are found in drylands, cover ∼12% of the Earth's surface in arid and semi-arid lands and their destruction is considered an important promoter of desertification. These crusts are formed by the adhesion of soil particles to polysaccharides excreted mostly by filamentous cyanobacteria, which are the pioneers and main primary producers in BSCs. Desert BSCs survive in one of the harshest environments on Earth, and are exposed to daily fluctuations of extreme conditions. The cyanobacteria inhabiting these habitats must precisely read the changing conditions and predict, for example, the forthcoming desiccation. Moreover, they evolved a comprehensive regulation of multiple adaptation strategies to enhance their stress tolerance. Here, we focus on what distinguishes cyanobacteria able to revive after dehydration from those that cannot. While important progress has been made in our understanding of physiological, biochemical and omics aspects, clarification of the sensing, signal transduction and responses enabling desiccation tolerance are just emerging. We plot the trajectory of current research and open questions ranging from general strategies and regulatory adaptations in the hydration/desiccation cycle, to recent advances in our understanding of photosynthetic adaptation. The acquired knowledge provides new insights to mitigate desertification and improve plant productivity under drought conditions.

Cyanobacterial populations in biological soil crusts of the northwest Negev Desert, Israel-effects of local conditions and disturbance.

Biological soil crusts (BSCs) fulfil numerous ecological functions in arid and semiarid areas. Cyanobacteria are important BSC organisms, which are responsible for carbon fixation, N2 fixation and binding of soil via extracellular polysaccharides. The cyanobacterial populations were characterised in different sampling plots established in three experimental stations along a rainfall gradient within NW Negev Desert, Israel. Cyanobacterial crust thickness and osmolyte accumulation therein decreased in plots with lower moisture. The cyanobacterial population structure also changed in different plots. We observed an increase of subsection III cyanobacteria such as Microcoleus spp. and Leptolyngbya spp. and a decreasing proportion of strains belonging to subsections I and IV in drier areas on the rainfall gradient. This population shift was also observed in the sampling plots, which were situated at various relief positions within the sand dune experimental sites. We also characterised the cyanobacterial populations within mechanically disturbed plots. After 4 years, they reached between 80% and 50% of the control populations in the northernmost and southern stations, respectively. Our results suggest that the cyanobacterial population is sensitive not only to macroscale factors but may also be subject to local climate variations and that 4 years was insufficient for complete recovery of the cyanobacterial population.

The mechanisms whereby the green alga Chlorella ohadii, isolated from desert soil crust, exhibits unparalleled photodamage resistance.

Excess illumination damages the photosynthetic apparatus with severe implications with regard to plant productivity. Unlike model organisms, the growth of Chlorella ohadii, isolated from desert soil crust, remains unchanged and photosynthetic O2 evolution increases, even when exposed to irradiation twice that of maximal sunlight. Spectroscopic, biochemical and molecular approaches were applied to uncover the mechanisms involved. D1 protein in photosystem II (PSII) is barely degraded, even when exposed to antibiotics that prevent its replenishment. Measurements of various PSII parameters indicate that this complex functions differently from that in model organisms and suggest that C. ohadii activates a nonradiative electron recombination route which minimizes singlet oxygen formation and the resulting photoinhibition. The light-harvesting antenna is very small and carotene composition is hardly affected by excess illumination. Instead of succumbing to photodamage, C. ohadii activates additional means to dissipate excess light energy. It undergoes major structural, compositional and physiological changes, leading to a large rise in photosynthetic rate, lipids and carbohydrate content and inorganic carbon cycling. The ability of C. ohadii to avoid photodamage relies on a modified function of PSII and the dissipation of excess reductants downstream of the photosynthetic reaction centers. The biotechnological potential as a gene source for crop plant improvement is self-evident.

Towards clarifying what distinguishes cyanobacteria able to resurrect after desiccation from those that cannot: The photosynthetic aspect.

Organisms inhabiting biological soil crusts (BSCs) are able to cope with extreme environmental conditions including daily hydration/dehydration cycles, high irradiance and extreme temperatures. The photosynthetic machinery, potentially the main source of damaging reactive oxygen species during cessation of CO(2) fixation in desiccating cells, must be protected to avoid sustained photodamage. We compared certain photosynthetic parameters and the response to excess light of BCS-inhabiting, desiccation-tolerant cyanobacteria Leptolyngbya ohadii and Nostoc reinholdii with those observed in the "model" organisms Nostoc sp. PCC 7120, able to resurrect after mild desiccation, and Synechococcus elongatus PCC 7942 and Synechocystis sp. PCC 6803 that are unable to recover from dehydration. Desiccation-tolerant strains exhibited a transient decline in the photosynthetic rate at light intensities corresponding to the inflection point in the PI curve relating the O(2) evolution rate to light intensity. They also exhibited a faster and larger loss of variable fluorescence and profoundly faster Q(A)(-) re-oxidation rates after exposure to high illumination. Finally, a smaller difference was found in the temperature of maximal thermoluminescence signal in the absence or presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) than observed in "model" cyanobacteria. These parameters indicate specific functional differences of photosystem II (PSII) between desiccation tolerant and sensitive cyanobacteria. We propose that exposure to excess irradiation activates a non-radiative electron recombination route inside PSII that minimizes formation of damaging singlet oxygen in the desiccation-tolerant cyanobacteria and thereby reduces photodamage.

Three-dimensional structure and cyanobacterial activity within a desert biological soil crust.

Desert biological soil crusts (BSCs) are formed by adhesion of soil particles to polysaccharides excreted by filamentous cyanobacteria, the pioneers and main producers in this habitat. Biological soil crust destruction is a central factor leading to land degradation and desertification. We study the effect of BSC structure on cyanobacterial activity. Micro-scale structural analysis using X-ray microtomography revealed a vesiculated layer 1.5-2.5 mm beneath the surface in close proximity to the cyanobacterial location. Light profiles showed attenuation with depth of 1%-5% of surface light within 1 mm but also revealed the presence of 'light pockets', coinciding with the vesiculated layer, where the irradiance was 10-fold higher than adjacent crust parts at the same depth. Maximal photosynthetic activity, examined by O2 concentration profiles, was observed 1 mm beneath the surface and another peak in association with the 'light pockets'. Thus, photosynthetic activity may not be visible to currently used remote sensing techniques, suggesting that BSCs' contribution to terrestrial productivity is underestimated. Exposure to irradiance higher than 10% full sunlight diminished chlorophyll fluorescence, whereas O2 evolution and CO2 uptake rose, indicating that fluorescence did not reflect cyanobacterial photosynthetic activity. Our data also indicate that although resistant to high illumination, the BSC-inhabiting cyanobacteria function as 'low-light adapted' organisms.

Simulated soil crust conditions in a chamber system provide new insights on cyanobacterial acclimation to desiccation.

Environmental research often faces two major hurdles: (i) fluctuating spatial and temporal conditions and consequently large variability in the organisms' abundance and performance, and (ii) complex, costly logistics involved in field experiments. Measurements of physiological parameters or molecular analyses often represent single shot experiments. To study desiccation acclimation of filamentous cyanobacteria, the founders and main primary producers in desert biological soil crusts (BSC), we constructed an environmental chamber that can reproducibly and accurately simulate ambient conditions and measure microorganism performance. We show that recovery from desiccation of BSC cyanobacteria and Leptolyngbya ohadii isolated thereof are strongly affected by dehydration rate following morning dew. This effect is most pronounced in cells exposed to high light and temperature in the dry phase. Simultaneous measurements of water content, gas exchange and fluorescence were performed during dehydration. Photosynthetic performance measured by fluorescence begins declining when light intensity reaches values above 100 µmol photons m(-2) s(-1), even in fully hydrated cells. In contrast, photosynthetic rates measured using O2 evolution and CO2 uptake increased during rising irradiance to the point where the water content declined below ∼ 50%. Thus, fluorescence cannot serve as a reliable measure of photosynthesis in desert cyanobacteria. The effects of drying on gas exchange are discussed.

Cyanobacterial Diversity in Biological Soil Crusts along a Precipitation Gradient, Northwest Negev Desert, Israel.

Cyanobacteria occur worldwide but play an important role in the formation and primary activity of biological soil crusts (BSCs) in arid and semi-arid ecosystems. The cyanobacterial diversity in BSCs of the northwest Negev desert of Israel was surveyed at three fixed sampling stations situated along a precipitation gradient in the years 2010 to 2012. The three stations also are characterized by marked differences in soil features such as soil carbon, nitrogen, or electrical conductivity. The cyanobacterial biodiversity was analyzed by sequencing inserts of clone libraries harboring partial 16S rRNA gene sequences obtained with cyanobacteria-specific primers. Filamentous, non-diazotrophic strains (subsection III), particularly Microcoleus-like, dominated the cyanobacterial community (30% proportion) in all years. Specific cyanobacterial groups showed increased (e.g., Chroococcidiopsis, Leptolyngbya, and Nostoc strains) or decreased (e.g., unicellular strains belonging to the subsection I and Scytonema strains) abundances with declining water availability at the most arid, southern station, whereas many cyanobacterial strains were frequently found in the soils of all three stations. The cyanobacterial diversity at the three sampling stations appears dependent on the available precipitation, whereas the differences in soil chemistry were of lower importance.

A newly isolated Chlorella sp. from desert sand crusts exhibits a unique resistance to excess light intensity.

We recently isolated a small green alga from a biological sand crust (BSC) in the NW Negev, Israel. Based on its 18S rRNA and rbcL genes, it is a close relative of Chlorella sorokiniana and of certain strains of C. vulgaris and C. variabilis, but differs substantially in many aspects from C. sorokiniana. Because the classification of Chlorellales is still not resolved, we designated this species as C. ohadii (Trebouxiophyceae) in honor of Professor Itzhak Ohad. Under controlled laboratory conditions, C. ohadii showed marked structural and photosynthetic performance changes, depending on the carbon source used during growth, as well as remarkable resistance to photoinhibition. CO2 -dependent O2 evolution was not affected even when exposed to a light intensity of 3500 µmole photons m(-2)  s(-1) , over 1.5 times the maximal intensity reached at the BSC surface, whereas the variable fluorescence declined sharply. We briefly discuss the use of fluorescence to assess photosynthetic rate and the implications of this finding for the assessment of global BSCs activity.

Photoinactivation of photosystem II: is there more than one way to skin a cat?

We briefly review the main mechanisms proposed for photodamage to photosystem II (PSII), at the donor and acceptor sides, and then discuss the mechanism whereby filamentous cyanobacteria inhabiting biological sand crusts such as Microcoleus sp. are able to avoid serious damage to their photosynthetic machinery. We show that the decline in fluorescence following exposure to excess light does not reflect a reduction in PSII activity but rather the activation of a non-radiative charge recombination in PSII. Furthermore, we show that the difference in the thermoluminescent peak temperature intensities in these organisms, in the presence and absence of inhibitors such as dichlorophenyl-dimethylurea (DCMU), is smaller than observed in model organisms suggesting that the redox gap between Q(A)⁻ and P680+ is smaller. On the basis of these data, we propose that this could enable an alternative, pheophytin-independent recombination, thereby minimizing the damaging ¹O2 production associated with radiative recombination.