NUCLEIC ACID IN ORGANIC MATTER IS A NITROGEN RESOURCE

Decomposition of plant residue in soil is achieved by biological activity and nutrient recycling. Nucleic acid is present in plant, animals and microorganisms. They are released into soil environment from dead plants and microbial cells which make up a portion of organic matter in soil. Nucleic acid (DNA & RNA) from dead organisms are a source of organically bound nitrogen and upon degradation release nitrogen as ammonia. Many soil microorganisms produce extra cellular nucleases, the enzyme that can break down nucleic acid. Nucleic acid can be cleaved and digested in soil by nucleases with release of inorganic phosphorus (Greaves and Wilson 1970). The extracellular ribonucleases (RNase) and deoxyribonucleases (DNase) produced by soil microorganisms attack RNA and DNA respectively. On decomposition nucleic acid produces nitrogenous bases (adenine, guanine, cytosine, thymine and uracil), sugar (pentose sugar) and phosphate. These nitrogenous base, sugar and phosphate are further degraded. Nucleic acid can be bound to clay and sand particle which protects them from rapid degradation by microbial nuclease (Lorenz and Wackernagel 1992).

There are two kind of nitrogen bases purines and pyrimidines. Purines such as adenine and guanine are present in both RNA and DNA, whereas, purines such as hypoxanthine and xanthine are not incorporated into nucleic acid but are synthesized as important intermediate in synthesis and degradation of purines nucleotide. Notable purines are hypoxanthine, xanthine, caffeine, theobromine and uric acid. Xanthine and hypoxanthine get into the soil on death and decay of plant containing them. Microorganisms uses purines under aerobic condition, converts uric acid to allantoin (Canellakis et al., 1955), whereas, pyrimidines are degraded by an oxidative or a reductive step (Vogels and Drift 1976). Allantoin can be degraded both under aerobic and anaerobic condition.

Nitrogen is a scarce resource limiting plant growth. Therefore plant remobilize nitrogen especially from the purine nucleobases. Adenine deaminase (adenine aminohydrolase EC 3.5.4.2) found in microorganisms converts adenine to hypoxanthine and ammonia. Hypoxanthine is then oxidized to form xanthine which is then converted to uric acid. Xanthine dehydrogenase converts xanthine to uric acid. Soil microorganisms have the ability to degrade uric acid by producing uricase. Large number of coryneform strain isolated from sandy soil, peaty soil and sewage decompose uric acid (Antheunisse 1972). Uric acid, allantoin and allantoic acid are present in a large number of plants (Bollard 1959; Reinbothe and Mothes 1962; Tracey 1956). Allantoin and its hydrolysis product, allantoic acid are nitrogen-rich compounds with a high nitrogen : carbon ratio (1:1) derived from the degradation of purines (Lamberto et al., 2010). In most plants allantoin and allantoic acid play an important role in the storage and translocation of nitrogen. In bleeding sap of maple, allantoin and allantoic acid account for 70 to 100% of the total soluble nitrogen. Allantoinase (allantoin amidohydrolase EC 3.5.2.5) occurs in many higher plants (Tracey 1956) and microorganisms.

Urea is a degradation product from organic matter and is taken up by roots from the soil. Urea formed during degradation of purines is degraded by urease (urea aminohydrolase, EC 3.5.1.5).

Enzyme xanthine dehydrogenase converts xanthine to uric acid
Uric acid is converted to allantoin by uricase
Allantoin is transformed into allantoic acid by allantoinase
Allantoic acid is converted to glyoxylic acid and urea by the enzyme allantoicase (Brunel 1939 )
Finally urea is converted to ammonia and carbon di oxide by enzyme urease

Xanthine dehydrogenase, uricase and allantoinase are constitutive enzyme but allantoicase is induced by xanthine or allantoin (Allam and Elzainy 1969). Purine is degraded by not just one single microorganisms but is utilized by large number of soil microorganisms for its growth and development. Examples are as follows:

Algae:

Chlorella pyrenoidosa and Chlorella vulgaris: Xanthine and uric acid serve as a nitrogen source.
Chlorella pyrenoidosa: Is able to utilize adenine and hypoxanthine.
Chlamydomonas reinhardi: Utilize xanthine and uric acid.

Fungi:

Aspergillus nidulans: Hypoxanthine, xanthine, uric acid, allantoin and allantoate serve as nitrogen source.
Penicillium chrysogenum: Utilizes guanosine, adenosine, adenine, hypoxanthine and xanthine as sole source of nitrogen for growth.
Penicillium roqueforti: Utilize methyl purines and xanthonine as sole sources of carbon or nitrogen for growth (Kurtzman and Schwimmer 1971).
Geotrichum candidum: Use xanthine, uric acid and allantoin as nitrogen sources (Barash 1972).
Neurospora crassa: Utilize adenine, hypoxanthine, uric acid, allantoin and allantoate (Reinert and Marzluf 1975) as nitrogen source.
Stemphylium species: Utilizes caffeine, theobromine and xanthine as either carbon or nitrogen source for growth (Kurtzman, Jr. and Schwimmer 1971).
Fusarium moniliformae: Can grow on hypoxanthine, xanthine, uric acid and allantoin which serves as nitrogen source.
Cladosporium herbarum and Paecilomyces farinosus: Uric acid serve as both carbon and nitrogen source.

Yeast

Candida utilis: Utilize purine base as nitrogen source.
Saccharomyces cerevisiae: Utilizes adenine and guanine moderately.

Bacteria:

Pseudomonas aeruginosa: Adenine, guanine, hypoxanthine and xanthine serve as nitrogen and carbon source (Rouf and Lomprey, Jr. 1968). Various member of genus Pseudomonas are able to grow on purines to use it as nitrogen or nitrogen and carbon source.

Number of microorganisms are able to degrade pyrimidines along a pathway involving the reduction of either uracil or thymine (Vogels and Drift 1976). Neurospora crassa utilizes uracil. Yeast strains have capability to utilize cytosine and uracil as nitrogen source. Di carlo et al., (1951) reported that Candida utilis grows well on cytosine and uracil which serves as nitrogen source but not on thymine, whereas, Saccharomyces cerevisiae grows moderately well on cytosine. Ammonia is formed from thymine by Nocardia rubra and by one strain of N. brasiliensis. Few yeasts can degrade thymine.

The specific physiological function of purine degradation lies in remobilization of nitrogen source and catabolic intermediates like ureides, allantoin and allantoate are involved in protecting plant against abiotic stress (Werner and Witte 2011). Plants secondary metabolites, bacteria, fungi and actinomycetes degrade uric acid into soluble ammonia. Soil microorganisms have the capacity to utilize numerous compounds, including nucleic acid as nitrogen and carbon sources.

References:

Allam, A. M. and Elzainy, T. A. 1969 Degradation of Xanthine by Penicillium chrysogenum J. Gen. Microbial. 56: 293-300

Antheunisse, J. 1972 Decomposition of Nucleic Acids and Some of their Degradation Products by Microorganisms. Antonie van Leeuwenhoek. J. Microbiol. Serol. 38: 311 – 327

Barash, I. 1972 Accumulation of Urea and Allantoin During Purine Utilization by Germinating Spores of Geotrichum candidum. J. Gen. Microbiol. 72: 539 – 542

Bollard, E. G. 1959 Urease, Urea and Ureides in Plants. Symp. Soc. Exp. Biol. 13: 304 – 329

Brunel, A. 1939 Formation of Allantoicase in the Mycelium of Aspergillus niger and Aspergillus phoenicis. Bull. Soc. Chim. Biol. 21: 380

Canellakis, E. S., Tuttle, A. L. and Cohen, P. P. 1955 A Comparative Study of the End Products of Uric Acid Oxidation by Peroxidases. J. Biol. Chem. 213: 397 – 404

Di Carlo, F. J., Schultz, A.S. and Mc-Manus, D. K. 1951 The Assimilation of Nucleic Acid Derivatives and Related Compounds by Yeasts. J. Biol. Chem. 189: 151-157

Greaves, M. P. and Wilson, M. J. 1970 The Degradation of Nucleic Acids and Montmorollinite-Nucleic-Acid Complexes by Soil Micro-Organisms. Soil Biol. and Biochem. 2: 257-268

Kurtzman, Jr., R. H. and Schwimmer 1971 Caffeine Removal from Growth Media by Microorganisms. Experientia 27: 481 – 482

Lamberto, I., Percudani, R., Gatti, R., Folli, C. and Petruccoa, S. 2010 Conserved Alternative Splicing of Arabidopsis Transthyretin-Like Determines Protein Localization and S-Allantoin Synthesis in Peroxisomes[C][W]. Plant Cell. 22(5): 1564–1574

doi: 10.1105/tpc.109.070102

Lorenz, M. G. and Wackernagel, W. 1992 DNA Binding to Various Clay Minerals and Retarded Enzymatic Degradation of DNA in a Sand/ Clay Matrix. In “Gene Transfers and Environment”. (ed. M.J. Gauthier), Springer Verlag, Berlin pp. 103-113

Reinbothe, H. and Mothes, K. 1962 Urea, Ureides and Guanidines in Plants. Annu. Rev. Plant Physiol. 13: 129 – 150

Reinert, W. R. and Marzluf, G. A. 1975 Genetic and Metabolic Control of the Purine Catabolic Enzymes of Neurospora crassa. Mol. Gen. Genet. 139: 39 – 55

Rouf, M. A. and Lomprey, Jr. R. F. 1968 Degradation of Uric Acid by Certain Aerobic Bacteria. J. Bacteriol. 96: 617 – 622

Tracey, M. V. 1956 Urea and ureides In “Moderne Methoden der Pflanzenanalyse (eds. Paech, K. and Tracey, M. V.) Springer-Verlag, Berlin. Vol. IV: 119 -141

Vogels, G. D. and Drift, C. Van der 1976 Degradation of Purines and Pyrimidines by Microorganisms. Bacteriol. Rev. 40(2): 403–468

Werner, A. K. and Witte, C. P. 2011 The Biochemistry of Nitrogen Mobilization: Purine Ring Catabolism. Trends Plant Sci. 16(7): 381-387