Summer, 1990 (v2n4)
Sims, G.K.
Advances in Soil Science
11:289-330. 1990
This extensive review (197
references) concerns the role of soil microbiota in nutrient cycling,
waste and residue decomposition, and detoxification of environmental pollutants.
If these processes are disrupted, human health can ultimately be harmed.
Not all topics addressed pertain directly to agriculture, but the overall
treatment may help in understanding issues of soil health and regeneration.
The Cast of Characters
Soil microbial communities
are typically diverse. In addition, the roles of the various species are
inextricably interconnected, so that, in experiments, direct and indirect
treatment effects may be indistinguishable. This article considers mainly
the bacteria and fungi.
Soil bacteria are
mostly saprophytes or parasites. Their single-celled structure gives them
access to resources and refugia unavailable to larger organisms, but it
may be a disadvantage in accessing nutrients that are contained in relatively
large particles (e.g., plant residues) that may contain valuable carbon,
but be deficient in other nutrients. Even motile bacterial types, however,
can occur in colonies in the soil, and this habit may confer advantages
such as improved nutrient mobilization and absorption, and protection
from drying, toxins, or ultraviolet radiation.
Mycelial fungi and actinomycetes
have filamentous (threadlike and branching) growth habits that may make
them better suited as early exploiters of relatively large fragments of
lignified plant residue, because they can transport various nutrients
among zones of enrichment. The filamentous habit also enables exploration
of large soil volumes, provides protection against being washed through
the soil profile, and permits specialization of cells to fulfill various
functions more efficiently.
Microbial Metabolism and Soil Processes
Microbial energetics (and
all forms of metabolism) are driven by the Gibbs free-energy yield derived
from the chemical adenosine 5'-triphosphate (ATP). ATP can be generated
by fermentation or respiration. The latter requires terminal electron
acceptors (e.g., nitrate, sulfate, carbon dioxide, ferric iron, or molecular
hydrogen), and producs greater amounts of ATP per unit of substrate. Fermentation
is less feasible in the presence of either highly oxidized or highly reduced
substrates, and results in accumulation of toxic products (simple organic
acids) that can eventually impede the process.
Oxygenases are enzymes involved
in the breakdown of aromatic and aliphatic compounds (e.g., lignins, hydrocarbons,
various pesticides), and the dehalogenation of xenobiotic compounds. These
processes, important in nutrient cycling and in detoxification of soils,
can only occur in the presence of oxygen. (Reviewer's note: dehalogenation
by oxygenases can only occur in the presence of oxygen, but dehalogenation
per se may be more rapid under anaerobic conditions.) The pH of
the soil solution is another factor that governs enzymatic activity. Particular
enzymes (even if membrane bound) are only active over a narrow pH range.
Microbially-Mediated Soil Processes
Carbon entering the
soil from plant sources (e.g., as cellulose) usually leaves as carbon
dioxide or methane. At first glance, impairment of soil carbon cycling
would seem to require severe environmental insult, because many species
of soil fungi and bacteria can degrade cellulose. Nonetheless, such impairment
has been observed in the field.
Nitrogen cycling includes
mineralization, immobilization, nitrification, denitrification, and nitrogen
fixation. N-fixation and nitrification are most easily disrupted. Nitrifying
bacteria (e.g., Nitrosomonas and Nitrobacter) are sensitive
to acidity and require aerobic conditions. Waterlogged soils can become
anoxic and may not support nitrification. Symbiotic nitrogen fixation
is a delicate and complicated phenomenon. Nodulation of legumes could
be impeded by some kinds of pollutant molecules.
Phosphorus cycling
could conceivably be impeded by anything that interferes with mycorrhizal
fungi. Cycles involving sulfur, iron, manganese and other elements depend
to varying degrees on microorganisms. These processes are not discussed
in detail in the article.
Indicators of Biological Degradation
Sims identifies four general
approaches to measuring biological degradation.
Community diversity
can be used to assess perturbation of soil biology.
Bacteria and fungi can be evaluated by "viable count" methods,
most involve plating on nutrient-rich agar. These methods are controversial,
as are their alternatives. Biodiversity of soil microbial communities
can be measured by various mathematical indices that emphasize richness
(number of species), equitability (evenness of allocation of individuals
among the various species), or combinations of these two. There is no
clear indication that more diverse soil communities are more resistant
to pertrbation.
Nutrient cycling can
be indexed by measurement of soil enzymes, various components of the N
cycle, cellulose or wood degradation, and of respiration.
Accumulation of pollutants.
Toxins may accumulate if soil microbial life is degraded. The soil's ability
to dechlorinate organic compounds can be impaired, especially in sulfate-rich
anaerobic environments. Heavy application of animal wastes to low- pH
soils can lead to buildup of ammonium and a concomitant reduced functioning
of Nitrobacter. This effect can result in nitrite accumulation.
Redox status. Anaerobic
conditions can arise as a result of compaction or waterlogging. Oxygen
diffusion is only 1/10,000 as fast through water-filled soil pores as
it is through air-filled pores. Production of large amounts of methane
would indicate the strongly reducing conditions associated with anoxia.
Effects of Toxic Substances on Microorganisms
Generally speaking, organic
compounds are readily degraded in warm climates, and less so in cold.
Toxic metals, on the other hand, can remain in soils and cause long-term
damage to soil microbial communities regardless of temperature. Sims discusses
the effects of pesticides and organic and inorganic pollutants.
Pesticides. Pesticides
can influence soil microbial activity, at times paradoxically. Application
of paraquat led to buildup of fungi and bacteria, but reductions in CO2
production, cellulose degradation, and nitrogenase activity. Sometimes
selective destruction of predators and the resultant buildup of their
microbial prey can occur. For example, glyphosate or diquat + paraquat
application led to the buildup of Gaeumannomyces graminis var.
tritici, the causal agent of take-all disease of wheat. Inoculation
with untreated soil led to suppression of the pathogen in the treated
soil, suggesting the possible role of microbial antagonists.
Nitrification and symbiotic
nitrogen fixation are especially sensitive to disruption by pesticides,
probably in part due to the small numbers of species involved in these
processes. At normal application rates, Amitrole, 2,4-DB, and diallate
can inhibit nitrification for at least 8 weeks, whereas atrazine, bromacil,
picloram, and simazine can do so for shorter periods. Some degradation
products of these substances may also be inhibitory. There are also examples
of no effect and (paradoxically) even stimulation of nitrification for
some of the pesticides mentioned above. For symbiotic nitrogen fixation,
denitrification, and ammonification, there are also cases of inhibition,
no effect, and stimulation, but no specifics are recounted. Soil respiration
is relatively in-sensitive to pesticide application, but antimicrobials,
e.g., fungicides, can suppress it. (Reviewer's note: soil respiration
is frequently increased upon addition of pollutants because they kill
sensitive species which are then digested by survivors.)
Toxic organic and inorganic
pollutants. These compounds can result from chemical synthesis, coal
mining, and petroleum processing. Organic pesticides show less dramatic
effects on soil microbiology than do other classes of toxic organics,
probably because the former are screened to avoid such effects.
Oil spills in cold regions
cause long-term damage to soil microbiology, including adverse effects
on carbon (e.g., cellulose degradation) and nitrogen cycling (especially
nitrification and nitrogen fixation). Some alleviation and enhanced degradation
of n-alkanes occurred through fertilization with urea and phosphate. Addition
of oil-degrading bacteria showed little promise. Addition of retorted
oil shale (that from which oil has been extracted) can reduce soil fungal
growth and bacterial species diversity, which is also adversely affected
by pyridine contained in the retort water. Revegetation lessened the effect
of oil shale, apparently because bacteria are insulated in the rhizospheres
of the range plants employed.
Contamination by heavy metals
(e.g., Cd, Cu, Ni, Pb, Zn) can cause long-term suppression of carbon cycling,
microbial biomass, nitrogen fixation, nitrification, dehydrogenase activity,
and mycorrhizal incidence. Toxic metals can be abundant in some sewage
sludges. Microbes can mobilize and increase the toxicity of cadmium, perhaps
by producing water-soluble ligands or otherwise changing soil properties.
Effects of Mining Operations on Soil Biology
Acidification can occur when
excavation of ores containing iron sulfides leads to oxidative production
of sulfates. Discharge waters from mine spoils may have pH values of 1-2,
and can cause severe problems off site. Waters draining from coal mines
and associated spoils can be high in Zn, Cu, Ni, or Mn, all potentially
toxic. Reclamation of strip-mined sites does not arrest such discharges
immediately.
Effects of Land Management on Soil Biology
In addition to the effects
of pesticides and other toxic materials, soil biology may also be affected
through various land management practices, including forest management
and crop production.
Forest management.
Prescribed burning in forests can lead to increased pH and availability
of Ca and Mg. On the other hand, hot fires can lead to loss of S, P, and
B, and destruction of surface structure leading to lowered infiltration
and increased runoff and erosion. Cool fires can lead to formation of
hydrophobic surface layers that decrease infiltration and consequent soil
moisture. On the other hand, fires can also inhibit certain fungi whose
mycelia previously imparted a hydrophobic character to the soil surface.
Under these conditions, infiltration can be increased. If fire darkens
the soil surface and increases insolation by opening the forest canopy,
soil temperatures can be increased. Effects of fire on soil microbiology
are usually transitory, and mainly involve the surface strata. There can
be increased nitrogen fixation following burns and either long-term increase
or decrease in nitrification.
Clearcutting of hardwood
deciduous or conifer forests leads to a reduction of litter inputs, increased
microbial breakdown of litter, and a consequent reduction in forest-floor
biomass, decreased shading, and increased soil temperature and pH. The
latter two phenomena lead to increased nitrification, which can in turn
lead to nitrate-rich runoff and pollution of nearby streams. In-creased
release of nitrous oxide, a significant greenhouse gas, may also occur.
Cropping Practices.
Studies on farming practices, including the long-term studies at Broadbalk
Field, England, illustrate the constancy of some soil biological processes
under continuous cropping and fertilization regimes. One plot received
no nitrogen fertilizer, but P, K, Na, and Mg were added. Annual biological
nitrogen fixation was estimated to be 40-60 kg N/ha, and soil N content
remained between 0.107 percent and 0.105 percent. These values have remained
virtually the same for over 100 years. Several studies of rice culture
have yielded analogous results, and have also shown that the addition
of N fertilizer arrests fixation by cyanobacteria in sediment and water,
and by heterotrophic bacteria in the rhizosphere.
Microbial communities appear to be tolerant of normal farming practices, but are at best barely able to meet the nitrogen requirements of crops. Fallowing may lead to reduced microbial biomass, mainly through reduction of fungi. The addition of manures may raise carbon and nitrogen levels in soils without affecting numbers of bacteria, fungi, or protozoa. There is no clear evidence that
pesticides or fertilizers
cause long-term degeneration of soil microbial diversity or biochemical
potential.
Soil erosion is particularly
deleterious to organic matter, which is less dense than other soil solids
and at times less so than water itself. The clay fraction of soil, to
which organic matter is often adsorbed, is particularly vulnerable to
erosion. Vesicular-arbuscular mycorrhizae (VAM) can be adversely affected
even by mild soil erosion. Survival of rhizobia in eroded soils may depend
on their tolerances to pH of deeper soil horizons; soil pH, of course,
is amenable to correction. Soil resistance to erosion is itself dictated
in part by microbial activity, including the binding of water-stable aggregates
through polysaccharidic exudates or VAM hyphae. Under tillage, carbohydrates
associated with clay are relatively stable, but 27-43 percent of the total
polysaccharides are contained in the light fraction, and these are subject
to rapid loss. Carbohydrates as a class appear no more unstable than other
classes of soil carbon taken together. Cultivation can lead to decreases
in aggregate stability and increased susceptibility to soil erosion. In
one study, soil under virgin prairie showed greater aggregate stability
than soil cultivated for 14 years. Soil carbon associated with macroaggregates
declined under cultivation. On the other hand, a study concerning a waterlogged
meadow frequently fertilized with ammonium sulfate showed deteriorating
soil structure while organic matter increased. This may have been due
to acidification and the consequent adverse effects on bridges formed
by divalent cations, which are important (along with polysaccharides and
hyphae) in maintaining aggregate stability. The chronic waterlogging probably
also interfered with organic matter cycling and aggregate formation.
Tillage, particularly of
virgin lands, can lead to immediate and short-term increases in microbial
biomass and metabolism. On the other hand, soil mesofauna may decline.
Earthworms are often adversely affected, but not always. Incorporation
of crop residues disperses microbial activity to a greater depth than
is seen in reduced-tillage systems. The latter show aerobes, facultative
anaerobes, and nitrifiers concentrated in the surface strata. Tillage
also affects the composition of bacterial communities. Agricultural burning
leads to loss of organic matter and the liberation of P and other cations.
Soil pH increases, and there are often increases in soil microbes, N mineralization,
and nitrification, although nitrifiers and N availability can be reduced.
Burning is often accompanied by tillage, so effects are often compounded,
or confounded, in practice.
Tillage of virgin lands causes
slow decline in soil organic matter. In studies at Rothamsted Experiment
Station, England, tillage of "prairie" led to a decline in soil
C for 27 years, then a stabilization for the subsequent 100 years. The
scientists postulated the existence of a persistent and a labile fraction
of the total soil carbon. The former was believed to persist for 1,000
years or more, whereas the latter was believed to have a half-life of
about 10-15 years. Soil N and C are both contained in organic matter;
hence the close relationship observed between their concentrations. Tillage,
in prompting the accelerated breakdown of soil organic matter, can liberate
N in excess of that assimilable by the soil microbes. This excess is then
lost through plant uptake, leaching, or volatilization.
Reduced-tillage (RT) typically
supplies less N than does conventional tillage. Several explanatory hypotheses
have been advanced:
- Under RT, denitrification potential of the microbial community is greater (some results have contradicted this idea; also, greater water content may be responsible rather than tillage per se);
- Concentration of residues at the surface under RT may lead to a greater immobilization of N relative to nitrification;
- Possible higher leaching losses under RT;
- Impairment of root metabolism due to impaired oxygen availability in soils under RT; and
- RT systems may require several years to reach equilibrium (as organic matter accumulates), at which point nitrification may be much greater than that observed earlier. Such a trend has been shown in a study of a 16-year old RT system.
(Reviewer's note: Sims makes
no mention of increased volatilization of ammonia under RT, to which many
researchers now ascribe the reduced N availability.)
Long-term changes under tillage
appear related to gradual decline in soil organic matter, rather than
to cultural practices per se. Tillage of virgin soils results in accelerated
degradation of organic matter and consequent deterioration of soil structure
with the increased threat of erosion. Erosion can lead to decreased microbial
activity through further loss of organic matter and exposure of inhospitable
deeper horizons. Under a given farming system, stabilization may occur
with time, but reversal of the initial degradation is unlikely. Restoration
of soil microbial communities may occur after cultivation ceases, but
the recovery time is unknown.
Microorganisms as Pollutants
Microorganisms can themselves
become pollutants; particularly hazardous are pathogens associated with
livestock and waste-management operations. Dispersal of livestock (to
avoid excessive concentration), application to lands only of treated sewage
sludge, and the avoidance of below-ground septic systems in risky areas
have all proven to be useful strategies in avoiding these problems.
Conclusions
Strip mining and metal contamination
are much more serious perturbations to soil microbial communities than
are the applications of pesticides. Communities in colder regions are
much more prone to long-term disruption than those in warmer climates.
Remediation of damage may require long periods of time, and damaged sites
that return to relatively healthy status may not return to their pristine
states. Remediation usually begins with ceasing the perturbation. long-term
studies are required to test any proposed safe alternatives to current
practices.
Acknowledgment: We thank
Dr. Kate Scow, Land, Air & Water Resources Dept., UC Davis, for her
critique of this summary.
Contributed by Robert
Bugg
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