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OCR for page 233
MICROBIAL AND RHIZOSPHERE MARKERS
OF AIR POLLUTION INDUCED STRESS
R.K. Antibus A.E. Linkins III
Department of Biology
Clarkson University
Potsdam, N.Y. 13676
ABSTRACT
The rhizosphere is a soil region of intense biological activity
and differs significantly from bulk soil in terms of numbers and
types of microorganisms. The structural and functional diversity
of the rhizosphere is maintained by input of root derived carbon
sources. Rhizosphere activity has been shown to exert either
positive or negative effects on plant growth through effects on
nutrient availability, production of growth regulators or phytotoxic
substances, or by suppression of pathogens. Rhizosphere
structure and activity has been throughly studied in crop plants
grown in agricultural soils; much less is known about rhizospheres
of mature trees in forest soils. Research approaches tend to
emphasize either: l ~ the isolation, enumeration and identification
of rhizosphere species, or 2) the characterization of rhizosphere
activities or products. Advantages and disadvantages of the use of
such approaches as biomarkers are discussed. Rhizosphere studies
under natural conditions are greatly complicated by the high
spatial and temporal variability found in soil properties and root
development.
Air pollutants might influence rhizosphere organisms by: 1 )
affecting plant carbon fixation thus altering carbon availability in
the rhizosphere, or 2) through direct effects on soil chemical or
physical properties. Research results, obtained largely with potted
plants, are available to support both of the above mechanisms.
However, the paucity of information does not allow for
generalizations about potential rhizosphere biomarkers of pollution
induced stress. Long-term data on the occurrence of fruitbodies
of ectomycorrhizal fungi in Europe suggest that air pollution may
be involved in reducing the species diversity and abundance of
these endorhizosphere organisms. Data on acid phosphatase
production by field-collected ectomycorrhizae suggest that
different fungi may have different functional roles relative to host
nutrition. Air pollution induced changes in species composition of
tree ectomycorrhizae could potentially affect soil nutrient cycles
and tree growth.
INTRODUCTION
The rhizosphere is considered to be that zone of the soil environment influenced by
plant roots. It is widely believed that this zone will be variable in extent and be directly
influenced by root physiology and by soil environmental factors. Available evidence
suggests that plants and rhizosphere organisms function in an interdependent fashion.
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234
Rhizosphere organisms depend on plants for a continuous supply of reduced carbon and
are recognized to play a significant role in nutrient cycling, thus exerting an influence
on plant growth. Air pollutants or other stresses which affect carbon fixation may
influence rhizosphere populations through an effect on carbon supply; alternatively
rhizosphere populations may be influenced by direct effects of air pollutants on the soil
environment. Changes in rhizosphere structure or function would in turn affect nutrient
cycling and exert a feedback effect on plant growth. Much of what is presently known
about rhizosphere structure and function has been obtained by using crop plants grown in
agricultural soils and caution should be used in extrapolating these results to forest
ecosystems.
RHIZOSPHERE STRUCTURE AND MAINTENANCE
Numerous studies have shown that bacterial numbers are greatly increased in
rhizosphere soils. Dilution plate counts indicate that the ratio of bacterial numbers in
rhizosphere compared to nonrhizosphere soil varies from 10:1 - 50:1 (Richards 1987~.
Numbers of fungi are also increased in rhizosphere compared to nonrhizosphere soil;
however, the magnitude of this increase is often smaller than observed for bacteria.
Comparison of rhizosphere and nonrhizosphere soils indicate that significant qualitative
shifts occur in the bacterial and fungal species detected (Gerhardson and Clarholm 1986~.
Rhizosphere species composition is influenced by numerous factors, including plant
species and genotype, plant nutrient status, presence and type of mycorrhizae, soil type,
soil moisture, light supply and other factors.
The continued maintenance of a "normal" rhizosphere is mediated by the release of
a wide variety of organic carbon compounds. Available data, obtained from crops and tree
seedlings, suggest that 40-50 oh of the net carbon fixed may be exuded or rapidly
released to the rhizosphere (Perry et al. 1987), more complex carbon compounds may
enter the rhizosphere more slowly resulting from root aging. The rhizosphere contains a
diverse array of metabolic substrates such as exudates, secretions, plant mucilages,
mucigel, and lysates (Rovira et al. 1979~. The diversity and complexity of released
compounds is likely to be an important factor contributing to the high species diversity
of rhizosphere microorganisms.
Attempts to describe the rhizosphere have emphasized the spatial locations of
organisms within the root zone. Whipps and Lynch ( 1986) recognized three regions
supporting microbial growth: endorhizosphere organisms live within the root, rhizoplane
organisms live on the root surface, and ectorhizosphere organisms inhabit a zone around
the root. The terms mycorrhizosphere and mycosphere have also been applied to the
zones associated with mycorrhizae and fungal hyphae respectively. Although such
regions and their component species may be difficult to characterize operationally, such a
classification has heuristic value. Microorganisms can be envisioned as existing along a
gradient in terms of plant and soil influences. Endorhizosphere species are in contact
with the plant and have direct access to reduced carbon. Organisms in distal portions of
the ectorhizosphere will be more directly influenced by soil factors. We would expect
organisms to show metabolic adaptations to the resources available in their surroundings.
Our inability to grow vesicular-arbuscular (VA) fungi in pure culture and the limited
capacities for complex carbohydrate utilization demonstrated by ectomycorrhizal (ECM)
fungi suggest that endorhizosphere species are adapted to root supplied carbon (Harley
and Smith 1983~. Rhizosphere bacterial isolates demonstrate growth and amino acid
utilization patterns suggesting adaptation to root products. Air pollutants affecting tree
carbon fixation or allocation patterns have potential to influence rhizosphere organisms;
however, our knowledge of these effects in forest species is limited.
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235
RHIZOSPHERE FUNCTIONS
Rhizosphere organisms may exert either positive or negative effects on plant
growth. These effects are determined by the rhizosphere's capacity to: 1 ) influence
nutrient availability, 2) produce plant growth regulators or phytotoxic compounds, or 3)
suppress pathogenic organisms. A complex set of microbial interactions determines the
structure of the rhizosphere community, these include: antagonism, commensalism,
parasitism, and predation. Bacteria may exhibit inhibitory or stimulatory effects on the
formation of mycorrhizal associations, which in turn affect plant growth and mineral
nutrition (Bowen and Theodorou 1979~. Formation of various types of mycorrhizae can
subsequently produce quantitative and qualitative alterations in rhizosphere bacteria and
fungi (Katzoelson et al. 1962, Meyer and Linderman 1986~. These changes observed in
rhizosphere composition may be mediated by a diverse array of metabolites produced by
rhizosphere organisms (Lynch 1987~.
Nye and Tinker (1977) listed the mechanisms by which rhizosphere organisms might
influence plant nutrient availability, including alterations in root morphological and
physiological properties, effects on phase equilibria of soil nutrients, effects of soil
chemical composition and organic matter mineralization, direct transfer of nutrients, and
competition for soil nutrients. Potentially favorable effects on root morphology and
respiration have been obtained with several rhizosphere bacteria on crop plants (Hades
and Okon 1987~. Work with vesicular-arbuscular
suggests that the increased surface area provided
satisfactory explanation for observed increases in
phosphate. Under natural conditions, however, the
organisms such as nitrogen fixers and hyphal _
composition and nutrient cycling (Coleman 1985~.
species under controlled conditions
by extramatrical hyphae provides a
uptake of immobile nutrients like
situation becomes more complex and
Brazers will influence rhizo~nh~r~
Some workers have suggested that root and rhizosphere phosphatases and phosphate
solubilizing bacteria may contribute to P nutrition under field conditions. Recent studies
(Tarafdar and Jungk 1987, Kroehler and Linkins 1988) suggest that root surface and
rhizosphere phosphatase activities will hydrolyze organic phosphorus forms at rates
sufficient to meet plant needs. These studies do not imply a necessary role for
rhizosphere organisms, however. Ectomycorrhizae are the most common form of
mycorrhizae on many important temperate tree species and can increase the uptake of
macronutrients (Harley and Smith 1983~. Ectomycorrhizal fungi alter root morphology, and
control the movement of nutrients from rhizosphere to plant by surrounding plant roots
with a fungal sheath. Phosphatases produced by ECMs are active against a variety of
organic phosphate sources found in forest soils (Bartlett and Lewis 1973) and likely play
key roles in phosphorus cycling. We have shown that ECMs formed by different fungi
exhibit different levels of phosphatase activity (Antibus et al. 1981~. Activity appears to
vary seasonally for a given host-fungus combination (Antibus and Linkins, unpublished
data), and we feel that phosphatase activity reflects the general physiological activity of
ECMs at given times. Further research could determine the efficacy of using phosphatases
or other enzyme assays as general indicators of root and rhizosphere activity. It may
also be possible to use ratios of enzymes such as the ratio of acid alkaline phosphatases
to determine the relative contributions of bacteria to rhizosphere enzyme activity.
EXPERIMENTAL APPROACHES
Rhizosphere workers usually attempt either to dissect the rhizosphere and study the
workings of its components or to examine the physiology of the intact zone. Studies of
the former type emphasize isolation, quantification and identification of rhizosphere
organisms, whereas the latter type emphasize the measurement of specific rhizosphere
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236
activities or products. Both approaches are valid, but are subject to numerous limitations
and drawbacks.
Techniques employed in the dissection and study of the rhizosphere include
procedures such as plate counting, enrichment cultures, end-point dilutions, direct
visualization and many others. These have the advantage of allowing identification of
specific organisms or groups of organisms. However, the selective nature of isolation
techniques has led to severe criticisms (Brock 1987~. Direct visualization procedures
overcome some of these limitations but often do not allow identification. The use of
fluorescent antibodies may permit identification, but requires increased technical
expertise. Another technically complex but potentially useful method to study populations
of specific rhizosphere bacteria involves the use of specific DNA probes (Holben et al.
1988~. Biomass estimates suffer from difficulties in separating live and dead organisms,
or from an inability to separate various specific groups of organisms. The use of
biochemical markers specific to certain species or functional groups may allow the in situ
estimation of rhizosphere organisms (Pace et al. 1986~. One such study has been
conducted with rhizosphere bacteria under greenhouse conditions (Tumid et al. 1985~. The
application of specific biochemical markers requires a thorough knowledge of
biochemistry, technical expertise and elaborate equipment.
Workers attempting to understand the physiological aspects of the rhizosphere have
examined such processes as nitrogen fixation or enzyme activities in the root and
surrounding soil. A disadvantage of these studies is that the key organisms involved in
the process of interest are usually not identified. These techniques may thus fail to
detect perturbation-induced population shifts which buffer against physiological change.
Enzyme studies offer the advantage of studying processes, such as nutrient
mineralization, which are crucial to plant growth. The procedures are sensitive and assays
are easy to perform using commonly available equipment. Because enzyme assays are
integrated measures, they demonstrate less variability than microbial counts (Burns 1978~;
however, they may also demonstrate time delays in response to perturbations.
Rhizosphere characteristics change over extremely short distances making study of
this soil region difficult. In addition to methodological difficulties mentioned,
interpretation of results under natural conditions is complicated by a high amount of
spatial and temporal variability in root growth and soil properties.
AIR POLLUTION EFFECTS
Air pollutants might affect rhizosphere activity by plant mediated effects or through
direct effects on the soil environment. Using pine seedlings Luxmoore et al. (1986)
showed that carbon dioxide enrichment resulted in plant-induced decreases in rhizosphere
pH and increased solubility of certain cations. Firestone et al. (1984) found the effects of
simulated acid precipitation on rhizosphere composition resulted from an influence on
root characteristics rather than changes in soil properties. In this study solubilization of
cations by acid precipitation was an important factor affecting bulk soil microorganisms,
and various pollutants can, under controlled conditions, affect bulk soil microbiology, soil
processes and enzyme acitivities (Wilke 1987~. Dighton et al. (1986) found numbers of
root tips and types of ECMs formed on Pinus sylvestris were affected when seedlings
were grown in soils previously exposed to artificial acid rain for 5 years. Evidence based
on production of fruitbodies of known ECM fungi strongly suggests that the mycorrhizal
fungus flora of the Netherlands has changed in the last 80 years. It has been suggested
that fruitbody productivity has decreased because of air pollution-induced stress of the
host species Pinus sylvestris (Termorshuizen and Schaffers 1987), and that ECM species
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237
frequency and diversity have been reduced through air pollution induced changes in soil
chemistry (Arnolds 1988~. The latter study indicates that some species may have been lost
completely from the fungal flora. These data, and work by Haselwandter et al. ( 1988) on
radiocaesium accumulation in fruitbodies, suggest that the occurrence of ECM fungi may
provide a valuable and easily obtained record of the effects of air pollution on the
endorhizosphere of ECM tree species. Unfortunately, little data of a mycosociological
nature are available for North American forests. Our work (Fig. 1 ) shows that naturally
occurring ECM morpho-types formed by several species of ECM fungi produce
significantly different acid phosphatase activities and may exert differential influences on
organic phosphorus mineralization. Data on fruitbody occurrence suggest that ECM
populations in Europe have changed; a concomitant shift in mycorrhizal root tips would
likely influence enzyme production and rhizosphere composition. Shifts in the relative
abundance of these morpho-types, whether due to air pollution effects on trees or soils,
could affect phosphorus cycling and other soil processes. Alternatively, changes in soil
properties might result in ecotypic differentiation. Woolhouse ( 1969) showed that ecotypes
of plants growing on metal-contaminated soils produced acid phosphatases differing in
susceptibility to cation inhibition; the development of such changes in ECM fungi might
serve as a marker of air pollution-induced changes in forest soils.
130
A, 110
=~_ 90
o 3
70
50
30
10
~ oWR
- ~YB
- · C G
1
1 2 3 4 5 6 7 8
Time (hrs)
Figure 1. Acid phosphatase activity of field-collected Douglas fir ectomycorrhizal
morphotypes: WR - white rhizomorph producer, YB - yellow brown smooth type and CG-
Cenococcum geophilum. Assays were conducted at 25C in pH 5.0 citrate buffer. Values
are means with standard deviation bars (n=5~.
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238
A review of available literature indicates that air pollutants can affect structure and
function of tree rhizospheres. These effects may relate to changes in root supplied
carbon or changes in soil environment. Too few data are available to suggest that any
particular rhizosphere organisms or functions may serve as a simple biomarker of
pollution induced stress. We suggest that the measure of root and rhizosphere enzyme
activities can provide a simple and useful approach to the study of air pollution effects
on rhizosphere physiology.
be interpreted in terms of tree growth. However, such information on the function of
rhizosphere organisms is crucial if we are to understand the significance of air pollution
effects on the occurrence of rhizosphere organisms.
More data will be needed before rhizosphere physiology can
SUMMARY
- The rhizosphere is an area of intense biological activity driven by root-derived
carbon.
- Rhizosphere activity may exert positive or negative influences on plant growth
through effects on nutrient availability, production of growth regulators or phytotoxic
substances, or by suppression of pathogens. Most of what is known about rhizosphere
effects comes from studies of crop plants in agricultural soils.
- Air pollutants might influence rhizosphere structure or function by effects on plant
carbon fixation or allocation, or by direct effects on the soil environment. Evidence to
support both mechanisms is available.
- Rhizosphere studies usually emphasize either: 1 ) isolation, enumeration and
identification of component species, or 2) the characterization of activities or products.
The former approach would allow detection of air pollution-induced shifts in key
rhizosphere organisms, whereas the latter would detect shifts in important rhizosphere
processes. Advantages and limitations of these approaches are discussed.
-Potentially useful approaches to rhizosphere study using techniques from molecular
biology are appearing; however, these often require technical expertise and sophisticated
equipment.
- The study of the response of the rhizosphere under natural conditions is complicated
by great spatial and temporal variability in soil properties and root development.
- Occurrence and composition of ectomycorrhizal fruitbodies could potentially serve as a
biomarker in forests of ECM trees. Studies of ECM fruitbody occurrence in the
Netherlands suggest that air pollution has reduced the frequency and diversity of these
endorhizosphere organisms.
-ECMs formed by different fungi on a single tree species can demonstrate significantly
different acid phosphatase activities. Shifts in ECM species composition in relation to air
pollution could potentially affect forest soil nutrient cycles.
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239
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Katznelson, H.,
mycorrhizal
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phosphorus. Plant Soil 105:3-10.
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Termorshuizen, A.~., and A.P. Schaffers. 1987. Occurrence of carpophores of
ectomycorrhizal fungi in selected stands of Pinus sylvestris in the Netherlands in
relation to stand vitality and air pollution. Plant Soil 104:209-217.
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hydroxybutyrate for estimation of bacterial biomass and activity in the rhizosphere
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Whipps, J.M., and J.M. Lynch. 1986. The influence of the rhizosphere on crop
productivity. Pp. 187-244 in Advances in microbial ecology, Vol. 9, K.C. Marshall
(ed.~. Plenum Press, New York.
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OCR for page 242
240
Katznelson, H.,
mycorrhizal
40:377-382.
J.W. Rouatt, and E.A. Peterson. 1962. The rhizosphere effect of
and non-mycorrhizal roots of yellow birch seedlings. Can. I. Bot.
Kroehler, C.J., and A.E. Linkins. 1988. The root surface phosphatases of Eriophorum
vaginatum: Effects of temperature, pH, substrate concentration and inorganic
phosphorus. Plant Soil 105:3-10.
Luxmoore, R.J., E.G. O'Neill, J.M. Ellis, and H.H. Rogers. 1986. Nutrient uptake and
growth responses of Virginia pine to elevated atmospheric carbon dioxide. J.
Environ. Qual. 15:244-251.
Lynch, J.M. 1987. Biological control within microbial communities of the rhizosphere. Pp.
55-82 in Ecology of microbial communities, M. Fletcher, T.R.G. Gray and J.G. Jones
(easy. Cambridge University Press, Cambridge.
Meyer, J.L., and R.G. Linderman. 1986. Selective influence on populations of rhizosphere
or rhizoplane bacteria and actinomycetes by mycorrhizas formed by GIomus
fasiculatum. Soil Biol. Biochem. 18:191-196.
Nye, P.H., and P.B. Tinker. 1977. Solute movement in the soil-plant system. Blackwell,
Oxford.
Pace, N.R., D.A. Stahl, D.~. Lane, and G.J. Olsen. 1986. The analysis of natural microbial
populations by ribosomal RNA sequences. Pp 1-55 in Advances in microbial ecology.
Vol. 9, K.C. Marshall (ed.~. Plenum Press, New York.
Perry, D.A., R. Molina, and M.P. Amaranthus. 1987. Mycorrhizae, mycorrhizospheres, and
reforestation: current knowledge and research needs. Can. J. For. Res. 17:929-940.
Richards, B.N. 1987. The microbiology of terrestrial ecosystems. Longman, Essex.
Rovira, A.D., R.C. Foster, and J.K. Martin. 1979. Origin, nature and nomenclature of the
organic materials in the rhizosphere. Pp. 1-4 in The soil-root interface, I.L. Harley
anc! R.S. Russell (eds.~. Academic Press, New York.
Tarafdar, J.C., and ~ A. Jungk. 1987. Phosphatase activity in the rhizosphere and its
relation to the clepletion of soil organic phosphorus. Biol. Fertil. Soils 3:199-204.
Termorshuizen, A.~., and A.P. Schaffers. 1987. Occurrence of carpophores of
ectomycorrhizal fungi in selected stands of Pinus sylvestris in the Netherlands in
relation to stand vitality and air pollution. Plant Soil 104:209-217.
Tunlid, A., B.H. Baird, M.B. Trexler, S. Olsen, R.H. Findlay, and D.C. White. 1985.
Determination of phospholipid ester-linked fatty acids and poly beta-
hydroxybutyrate for estimation of bacterial biomass and activity in the rhizosphere
of the rape plant Brassica napus L. Can J. Microbiol. 31:1113-1119.
Whipps, J.M., and J.M. Lynch. 1986. The influence of the rhizosphere on crop
productivity. Pp. 187-244 in Advances in microbial ecology, Vol. 9, K.C. Marshall
(ed.~. Plenum Press, New York.
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The Workshop Papers
Biochemical/Cell-Tissue Session
OCR for page 244
Representative terms from entire chapter:
plant growth
