Soil biochemistry

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Soil biochemistry, as defined in this book, refers to the characteristics and dynamics of organic matter and the biochemical transformations brought about by enzymes and organisms in soil. Biochemical reactions appear to have proceeded without microorganisms. Later microorganisms were active without the presence of plants and animals for long periods of the earth's history. Biochemical reactions similar to those occurring in modern soils are thought to have occurred for an extended period before the occurrence of the first bacteria identified in rocks that have an age of approximately 3.8 billion years. Phototrophic bacteria and cyanobacteria have been identified in rocks that are 2.8 billion years old. Vascular plants and mammals are a product of only the past 500 million years.

Experiments with iron sulfides, at the elevated temperatures and pressures found in hydrothermal vents, have indicated the possibility of the formation of prebiotic, organic substrates. These are believed to involve organo-metal interactions often studied in today's soil biochemistry. Another theory involves an alkaline world in which the activity of negatively charged clay minerals, such as smectite, organized fatty acid micelles and lipids into vesicles that contained active clays. These are said to have concentrated and polymerized RNA and DNA. Once formed, vesicles such as these are postulated to have grown by extrusion through small pores. These reactions are all familiar to the soil biochemist, as are the concepts involving micropores, enzymatic activity, and habitat formation so important in early life studies (Bada and Laszano, 2003).

Waksman (1938), in his book entitled "Humus," states that from Theophrastus (373-328 BCE) to the time of Wallerius (1709-1778 CE), the concept of oleum untuosm, equating fertile soil with the fatness of the land, dominated the ideas of naturalists. The word "humus" was extensively used in Virgil's (79-19 BCE) poetry about farming, food production, and the joys of country life. His poetry is extensively quoted relative to soil fertility, decomposition, gardening, nature, the environment, and organic agriculture, with the 39 BCE quote from the second Georgics

"pinquis humus dulcique uliine laeta; Quique frequens hebis et fertilis ubre campus"

being the most familiar. The word humus, together with terra and solum, was used for earth. It is the root word for humans, homo, and even posthumous, after the earth or death. Virgil referred to dark soil as fertile, and the ancients knew that dark-colored soil was more productive, absorbed more water, and was easier to till than its lighter colored counterparts in the landscape. They had also observed that exposure to flames often lightened the soil. Feller (1997) quotes Pliny the Elder (23-79 CE) as saying

"the lupin penetrates the humus and wheat needs two feet of humus."

The period of alchemy and the phlogistic theory continued to use the original Latin definition of humus as soils or earth, as did Linnaeus (1707-1778), the great Swedish botanist. He classified soils as Humus daedalea (garden soil), Humus rualis (field soil), and Humus latum (muck soil). The concept that the application of dung to the soil replaced some substances that had been removed by plants was established in the 16th century. Van Helmont's (1577-1644) experiments that concluded that water was the source of plant nutrition were repeated by Robert Boyle with the same conclusion. However, Woodward in 1699 showed that impure water, such as that from the river Thames, increased the growth of mint. He also reported that dung that returns parts of either vegetables or animals was the best way of restoring soil. Boerhavein, in a 1727 textbook of chemistry, wrote that plants absorb the juices of the earth. Tull in 1730 stated that small, earth-like particles serve as nutrients for plants.

Wallerius in 1753 (see Feller, 1997) used the Latin word humus for loam or mold, which at that time referred to the organic surface horizon relative to decomposing organic matter, and is thus credited with the modern use of humus for organic matter. This was made easier by the fact that the later Roman and Latin texts then utilized the word terra rather than humus for earth. Wallerius went along with the thinking of that time in assuming humus was the essential nutritive element and that other soil constituents acted in mixing or dissolving it and, thus, assisted uptake by plants. Lime was considered to help dissolve the fat (humus) of the land and the function of clay was to fix or retain this fatness. The Russian scientist Komov, in his 1782 book on agriculture, associated the hydrophysical properties of soil and its richness in nutrients with the presence of humus and stated that the "nutritive juice" of soil was produced by rotting.

De Saussure, known for his chemical studies, also spent considerable time on humus. In 1804, he described humus as being of various complexes (oils and salts), capable of absorbing oxygen and producing CO2. He showed that it contained more C and less O and H than the plant residues that went into its formation. He also established that plants synthesize their organic matter from CO2 and give off O2. Thaer in 1808 differentiated between peat formed in limited O2 and mild humus formed under adequate O2. He ascribed to the humus theory of plant nutrition, which stated that humus was the direct source of plant nutrients. Thaer also has been called the father of sustainable agriculture (see Feller et al., 2003b). One of his books stated,

"Latterly the practice of sowing white clover with the last crop has become very general; only a few apathetic and indolent agriculturalists or men who are firmly wedded to old opinions and customs, neglect this practice."

It took the work of Sprengel in 1826, Liebeg in 1840, and Boussingault in 1841 (see Feller et al., 2003b) to found the concept of mineral nutrition of plants. However, modern organic agriculture still credits soil organic matter with properties other than nutrient supply, water and nutrient retention, complexation, and aggregation. Humic constituents in small quantities continue to be investigated for their effect on plant respiration as does the use of specific plant- and microbial-derived molecules as information signals for plant and microbial interactions (Vaughn, 1985; Bais et al., 2004).

Berzelius, first in 1806 and later in the 1830s, described the dark, black, and lighter yellow humic compounds and showed their interactions with metals. Field experiments carefully conducted in 1834 by Boussingault, considered the father of modern scientific agronomy, analyzed the C, H, O, N, and mineral inputs in manure relative to those in subsequent plant parts grown on manured soils. In 1826 and 1837, Sprengel found that the C content of humus is 58%, described the most important characteristics of humates (its salts), and studied their decomposition and solubility characteristics. The Russian scientist German, in 1837, still believed that humus was a direct source of plant nutrition, but found that cultivated soils contained less humus than virgin ones and attempted to obtain scientific confirmation of the value of rotations. This was a prelude to modern-day sustainable agriculture and the questions arising today regarding soil C and global change. He also was the first to question whether humic acids were chemically individual compounds. The large number of fractions he, and later others, identified as constituents of humus was not found to be reproducible and this led to a general questioning of the usefulness of soil organic matter fractionation. Danish scientist Müller (see Wilde, 1946) further defined the solubility and characteristics of humics in his book "Natural Forms of Humus" and developed the concepts of Mull and Mor in forest soils. Mull horizons had earthworms and fungi, whereas earthworms were absent from Mor soils.

Dokuchaiev, the founder of Western soil science, recognized the involvement of the five interacting factors of soil formation (parent material, vegetation, organisms, climate, and time) in the development of rich, high-organic-matter, chernozemic soils. Other scientists in this productive period include Kostychev, who in 1886 suggested that products synthesized by bacteria participated in the production of humic substances (see Kononova, 1961). Hebert in 1892 and Deherain in 1902 developed the concept of humus formation as the interaction of lignin and proteina-ceous substances. Büchner is credited for his pioneering work in enzymology by disrupting yeast cells to produce a cell-free system capable of alcoholic fermentation. This later led to the many investigations of enzyme reactions in soils.

During the period of 1908-1930, Shreiner, Shorrey, and their co-workers used large-scale extraction equipment to isolate 40 identifiable organics including hydrocarbons, sterols, fats, organic acids, aldehydes, carbohydrates, and organic P and N compounds. These studies gained a great deal of attention because of their precision, but may have detracted from the overall study of soil organic matter as a natural entity. They were a prelude to Waksman's detailed studies on the proximate analysis of organic matter in which he rejected the concepts of humic and fulvic acids. However, Tyurin in his 1937 book (see Kononova, 1961) on the organic matter of soils and Springer in 1934-1935 (see Kononova, 1961) regarded Waksman's denial of the existence of specific humic soil compounds as unfounded and incorrect, and claimed that proximate analysis, as suggested by Waksman, would not stand the test of time in that it characterized only a small fraction of humus. However, some mistrust of humic acid characterization, generated by Waksman's criticisms, continues today in Western soil science, although humic acid chemistry is well accepted in aquatic research in both marine and freshwater environments.

The translation of earlier Russian volumes entitled "Soil Organic Matter, Its Nature, Its Role in Soil Formation and Soil Fertility" (Kononova, 1961) described organic matter much as it is defined today and brought together literature on the role of physical, chemical, and biological factors of soil formation and its effect on cultivation. Stevenson's 1994 book entitled "Humus Chemistry" recognized the role of humic and fulvic acids and humic fractionation and delineated today's knowledge of organic C, N, P, and S transformations. Aiken et al. (1985) in "Humic Substances in Soil, Sediment and Water" recognize the similarity of humic substances in soils, sediments, and water. They describe methods, such as NMR and pyrolysis mass spectrometry, for studying this series of complex, and still difficult to study, soil organic matter constituents that form such an important component of present-day sustainable agriculture and global change investigations.

Nitrogen is important as a constituent of soil organic matter, as a nutrient in soil fertility, in water pollution, and in trace-gas, radiative forcing in global change. It thus continues to receive a great deal of attention. It took a great deal of research and many publications to delineate the processes of N2 fixation and N immobilization, mineralization, plant uptake, and denitrification. The reviews edited by Bartholomew and Clark (1965), Stevenson (1982), and Mosier et al. (2004) delineate the use of instrumentation, tracers, and inhibitors in determining the processes and rates in soils. In 1943, Norman and Werkman labeled soybeans with 15N. Addition of the labeled residue to soil showed that 26% of the tagged N was recovered by a subsequent crop. Work with both 15N and 13C by Broadbent and Norman in 1946, and Broadbent and Bartholomew in 1948 (see Jansson, 1958; Paul and Van Veen, 1978), established the principles for the use of soil tracers. The equations of Kirkham and Bartholomew (1955) for mineralization-immobilization and the epic work of Jannson (1958) on soil N dynamics should be required reading for anyone today contemplating tracer studies.

The advent of tracers in the 1940s came at a time when the principles affecting plant decomposition had been reasonably established. Harmsen and van Schreven (1955) summarized the early work on the effects of environmental factors and the possibility of soil biota turnover in subsequent releases of N as follows:

"The study of the general course of mineralization of organic N was practically completed before 1935. It is surprising that many of the modern publications still consider it worthwhile to consider parenthetical observations dealing with these entirely solved problems."

These authors then pointed out that the relationships between C and N and the effects of environmental factors had to be determined for each soil type, indicating that the underlying controls were not understood nor could the dynamics of resistant compounds be measured.

Libby developed the 14C dating technique in 1952. It was used for peats, buried soil profiles, and soil pedogenesis by Simonart and Mayaudon in 1958, Simonson in 1959, and Tamm and Ostlund in 1960 (see Paul and Van Veen, 1978). In 1964,

Paul and co-workers carbon dated soil organic matter fractions to calculate their mean residence times. The further interpretation of carbon dating by Scharpenseel, and Stout and Rafter (see Goh, 1991), did a great deal to establish pools and fluxes for modeling purposes. Decomposition experiments with plant residues with laboratory-enhanced 14C contents provided much information on the effects of soil type and climate management in studies by Sorensen in 1967, Jenkinson and Rayner in 1977, and Sauerbeck and Führ in 1968 (see Paul and Van Veen, 1978). Differences in naturally occurring 13C resulting from C3 ^ C4 plant vegetation switches and from enhanced CO2 experiments are now being effectively utilized to answer global change and soil and ecological sustainability questions involving soil organic matter (Coleman and Fry, 1991; Boutton and Yamasaki, 1996).

The use of tracers allows one to also measure nontracer soil C and N. There is continual turnover of organic matter during decomposition, and tracer experiments often show more soil C and N being released than can be determined in the absence of the tracer. Some of today's authors are mistakenly calling this priming. Fontaine et al. (2004) credit Löhnis as defining priming in 1926 as an increased availability of nutrients due to higher microbial activity resulting from the addition of substrate. With the use of tracers, Broadbent and Bartholomew (1948) also defined priming as the increased mineralization of unlabeled soil organic matter constituents in the presence of available fertilizer N or labeled plant residues. Replacement by the tracer of nontracer C or N during normal soil dynamics must be taken into consideration before priming is said to occur. It is hoped that today's authors will read the original literature and not erroneously redefine what was established many years ago. Priming does occur. We must, however, use a mass balance approach together with the tracers to determine that it is a net release of the nutrients from soil organic matter and not a normal exchange of the tracer for nontracer isotopes during microbial growth and product formation.

There are excellent reviews on soil N, such as Bartholomew and Clark (1965), Stevenson (1994), and Mosier et al. (2004). These contain discussions of the significance of fixed ammonia as part of total soil N, especially with regard to depth, in clay soils. Today's literature seems to have forgotten this constituent. It is hoped that in the next 10 years, we will not read a spate of papers that claim to have newly discovered this not necessarily active, but important, N component.

Fred et al. (1932), Stewart (1975), and Graham (2000) have reviewed N2 fixation. Prosser (1986) and Norton (2000) reviewed nitrification, whereas N losses, especially those leading to pollution and global warming, have been covered in Robertson (2000) and Groffman (2000). Publications such as "Biogeochemistry" (Schlesinger, 1997) and "Geomicrobiology" (Ehrlich, 1996) cover related areas of nutrient cycles and exchange in soils, freshwater sediments, and the vadose zone. The fact that the processes and process controls are similar in all environments is heartening for our level of knowledge. These controls lead to a rather similar composition for organic matter in most aerobic terrestrial soils. Modeling, such as that used by Jenkinson and Rayner (1977), is now an integral part of soil biochemistry used to test concepts and extrapolate information to different landscapes and for future predictions. Whether the ability to develop reasonably descriptive models based primarily on soil organic

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