1. LITERATURE REVIEW
1.3 INTRODUCTION TO LICHENS
1.3.5 Nutrient acquisition in fungi/lichens
16 Sterecaulon grow as extensive carpets in the vegetation of oligotrophic tundra, sub-artic taiga and heath and ombrotrophic peabogs (RODWELL, 1991). They are important contributors to the functional ecology of these habitats, in terms of biomass and carbon storage (LANGE et al., 1998).
The need to study acid load in these fragile heathland ecosystems has prompted several studies. CRITTENDEN (1989) demonstrated the efficient uptake by Cladonia stellaris and Stereocaulon paschale of NH4+
and NO3-
delivered in rainfall (80%) and suggested that carpets of mat-forming lichens are significantly ombrotrophic in nature thus possess enormous potential as indicators of N deposition, particularly across large areas of remote northern terrain in which they are often abundant and for which measurement of N load are generally sparse. Mat- forming lichens occur typically in open situations where they intercept rainfall that is largely unmodified by overlapping plant canopies (HYVÄRINEN and CRITTENDEN, 1998). Recent studies by HOGAN et al. (2010a) revealed that mat- forming terricolous lichens provide coherent biomarkers for N enrichment. Interestingly, nitrogen enrichment also induces P-limitations in C. portentosa with attendant changes in chemical and physiological characteristics that could be used as a sensitive biomarker with which to detect low levels of N pollution (HOGAN et al., 2010a; 2010b).
17 Studies involving nutrient acquisition in lichens are still in its infancy. Other symbiotic organisms such as mycorrhizae and rhizospheric fungi have shed light on the ability of the symbiotic fungus to acquire nutrients. Vesicular-arbuscular mycorrhizal (VA) fungi colonize plant roots and transport water and mineral nutrients from the soil to the plant while the fungus is benefiting from carbon compounds provided by the host plant (TURK et al., 2006). VA-fungi are associated with improved growth of plant species due to increased nutrient uptake, production of growth promoting substances, tolerance to drought, salinity and transplant shock and synergistic interaction with other beneficial soil microorganism such as N-fixers and P-solubilizers (SREENIVASA and BAGYARAJ, 1989). The benefits of symbiotic association of plant roots with VA fungi are well-known.
Enhanced growth because of increased acquisition of phosphorus and other low mobile mineral nutrients have been reported (KWAPATA and HALL, 1985; TURK et al., 2006). Ectomycorrhizal (ECM) trees benefit from association with Basidiomycetes that possess several high-affinity P transporters that are expressed in extra-radical hyphae and whose expression is enhanced by P deficiency (PLASSARD and DELL, 2010).
To date no comparable flux of nutrients from the mycobiont to the photobiont has been demonstrated. Questions whether the fungus serves as the reservoir of inorganic nutrients for the photobionts through haustoria are being raised and need further investigation. In mycorrizal fungi, this seems to be the case. For instance, involvement of cytoplasmic streaming in the translocation of phosphate in arbuscular mycorrhizal fungi has been suggested based on calculations of the energy required for the high flux rates of phosphorus in hyphae (TINKER, 1975; HALEY and SMITH, 1983). The relationship between tubular-form vacuoles and cytoplasmic streaming implies the importance of this form in transport inside hyphae (UETAKE et al., 2002).
Nutrient acquisition in lichens can also be gleaned from field studies. The addition of nutrients often stimulates growth and various metabolic processes, thereby demonstrating nutrient requirements. For example, when lichens were fertilized, they exhibited a varying response. For instance Cladonia stellaris did not increase its growth whereas cyanobacteria species S. paschal and Peltigera aphthosa responded positively
18 (KYTÖVIITA, 1993; HYVÄRINEN et al., 2003). These results suggest that the impact of enhanced N on lichen growth may be biased towards the growth of the photobionts rather than the mycobionts. The consequence of increasing the photobiont‟s growth may inevitably lead to breakdown of the symbiosis.
SUN and FRIEDMANN (2005) found a positive relationship between alga to fungus ratio and habitat summer temperature in Cladina rangiferina. They suggested that regulation of the ratio of the producer (alga to fungus) directly contributes to adaptation to a wide range of thermal regimes and to the distribution of lichens. The differential responses of fungal and algal growth to N and P fertilization observed in their study suggested that the tissue nutrient contents, and particularly the nutrient balance, affect resource allocation in the lichen thallus (MAKKONEN et al., 2007).
The distribution and dominance of Cladonia portentosa in acidic and nutrients-poor soil, demonstrates the ability of this lichen to efficiently acquire nutrients. Several studies have demonstrated limiting effects of nitrogen (N) on lichen productivity but phosphorus (P) limitation deserves much more consideration. Unlike nitrogen, P has no gas phase, and frequently P may be lost from ecosystems by sedimentation and secondary mineral formation (NASH, 2008).
It is well known that the presence of an array of hydrolases such as PME helps these fungi to acquire nutrients. This is common in other symbiotic organisms like mycorrhizal fungi where phosphorus deficiency increase PME up-regulation. The importance of secreted acid phosphatase is better recognised in plant-fungus symbiotic (mycorrhizal) relationships, as their production by soil microorganisms increases the amount of phosphate available to plants (YADAV and TARAFDAR, 2003), contributing significantly to the nutrient dynamics of most ecological niches where phosphorus is deficient (MOLLA et al., 1984; JAYACHANDRAN et al., 1992; TURNER et al., 2001).
19 Phosphate (P) is one of the essential elements but least available nutrients in many natural ecosystems (HALSTEAD and MCKERCHER, 1975; SHIMOGAWARA et al., 1999;
ABEL et al., 2000; BOZZO et al., 2002; GEORGE et al., 2011). Paradoxically, soils usually contain a relatively large amount of P, in the form that is not directly available for use. Up to 80% occurs in organic forms (RICHARDSON et al., 2005) of which inositol phosphates constitute the largest (~50%) fraction (TURNER et al., 2002). Another contributing factor to low phosphate availability is mainly due to its insoluble precipitation with cations or its conversion into organic complexes (WYKOFF et al., 1999; CHEN et al., 2000; RAGHOTHAMA, 2000). To cope with low phosphate availability, many plants and microbes have evolved numerous physiological (inorganic phosphate (Pi) transporters), biochemical (secreted enzymes) and molecular (multi-genes) adaptations to scavenge traces of usable phosphorus from the environment (FURIHATA et al., 1992; SHIMOGAWARA and USUDA, 1995; JESCHKE et al., 1997;
SCHACHTMAN et al., 1998; RAGHOTHAMA, 1999; ABEL, 2002).
A central component in this situation is a class of enzymes, capable of acting on the ester bond (Enzyme Commission number, EC 3.1) and catalysing the cleavage of phosphate esters (EC 3.1.3), constituting the subclass of phosphohydrolases, i.e. phosphatases (phosphomonoesterases, PME).