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III. Enzymatic Activities in Soil under Conditions Unfavorable for the Proliferation of Microorganisms

III. Enzymatic Activities in Soil under Conditions Unfavorable for the Proliferation of Microorganisms

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ENZYMES ACCUMULATED IN SOIL



65



other hydrolases? remain active even at low soil humidities that are incompatible with microbial proliferation and the life of higher plants.

SkujiqS and McLaren ( 1 969) have studied the same problem in the

case of urease. They used labeled substrate (14C-labeled urea). For the

determination of soil urease activity at various atmospheric humidities, the

soil samples were equilibrated at each humidity in a closed container. Upon

equilibration, dry IT-labeled urea was added to the soil, and the mixture

was placed in a radioactive gas detection chamber. The atmosphere in the

chamber was equilibrated at the desired humidity before the soil-urea mixture was introduced. Humidity was kept constant during incubation. The

results show a decrease of urease activity with decreasing relative humidity.

A measurable urea hydrolysis may still be evident at 80% relative humidity. Since proliferation of most soil microorganisms ceases between 85 and

95% relative humidity, the urease activity in soil below this relative humidity level can be attributed to the accumulated urease.

Ahrens and von Klopotek (1970) stored samples of three soils under

field and laboratory conditions for 1.5 years. The samples kept in laboratory had a constant water content or were air-dried. Plate counting of bacterial and fungal populations and determination of dehydrogenase activity

performed every 4 weeks on air-dried samples showed that bacterial and

fungal counts decreased to a larger extent than the dehydrogenase activity.

This observation would suggest that dehydrogenases in soil are more persistent than the viability of soil micropopulation.

It is known that in the climatic zones with well-defined successive wet

and dry seasons, the start of the rainy season after a dry period leads to

a pronounced reactivation of life in soil. Mineralization of the soil organic

matter is intensified. In order to better understand the mineralization of

organic phosphorus compounds in the soils of these climatic zones, Birch

( 1964) conducted laboratory experiments simulating natural soil conditions. Dry soil samples were moistened and incubated at 25OC for 17 days.

Periodically, subsamples were removed and halved. Inorganic phosphate

was immediately extracted from one half; the second half was submitted

to the extraction after exposure to chloroform vapor for 24 hours. After

chloroform treatment, the amount of extractable phosphate increased. The

analytical data suggest that the increase resulted from dephosphorylation

of the organic P compounds of the microorganisms killed by the chloroform. Dephosphorylation was catalyzed by accumulated soil phosphatases.

Similarly, the organic phosphorus compounds of microorganisms which



’ Enikeeva’s work (1948) is an unpublished dissertation. Some results were, however, published in 1952. Unfortunately, neither the 1952 publication nor Mishustin’s

reports contain any information concerning the nature of these hydrolases and the

methods used for their study. This is why we could not refer to these studies in

the preceding sections of this report.



66



s.



KISS, M.



DRAGAN-BULARDA,



AND D.



RXDULESCU



died during the dry season may serve, at the beginning of the wet season,

as substrates for the accumulated soil phosphatases.

Alternation of rainy and dry seasons exerts a strong effect on soil arylsulfatase activity. Cooper (1972) found that during the rainy season, when

soils were continually moist, the enzyme activity increased, but at the end

of the rainy season, as soils dried out, arylsulfatase activity was again

reduced.

Drying and rewetting can also influence soil enzyme activity in other

climatic zones. Koepf (1954b) worked with soil samples from which the

root residues were thoroughly removed. Drying and rewetting caused little

changes in invertase activity of these samples. When the samples contained

fresh rye roots, invertase activity diminished considerably not only in dried

and rewetted samples, but also in those kept continuously wet. This phenomenon follows from the rapid inactivation of root invertase. Ambrol:

(1970, 1973a) found that drying of rendzinas resulted in a marked drop

of their enzyme activities. Rewetting and the subsequent incubation led

to slight increases in invertase and phosphatase activities and to higher

increases in amylase, gelatinase, and caseinase activities. Repeated dryings

and remoistenings reduced the enzyme activities to a degree that the soils

no longer responded to moistening.

2. Temperature



It is known that after thawing of frozen soils microorganisms become

very active and mineralization of soil organic matter intensifies. According

to Antoniani et al. (1955), the intensification is due to cryoactivation of

enzymes rather than to the numerical growth of soil micropopulation.

Tagliabue (1958) explained the increase of urease activity in samples of

a soil previously stored at temperatures between O°C and -33OC as the

dispersing action of freezing and thawing on soil colloids. In three other

soils, urease activity decreased but did not disappear after freezing.

When the soil was stored at --15OC, uricase activity remained reasonably stable over the period of 1 month but the soil extracts in 0.1 M phosphate buffer stored under the same conditions lost some 50% of their uricase activity (Martin-Smith, 1963).

Ross (1965b) studied the influence of freezing on the soil enzymes hydrolyzing sucrose and starch. Freezing did not lead to disappearance of

their activity; more precisely, saccharolytic activity decreased on storage

at -2OoC, but the changes were slight over long periods. Inactivation of

the amylolytic enzymes was greater and tended to increase with prolonged

storage. At the same time, storage at -2OOC for 77 days and the subsequent thawing enhanced dehydrogenase activity in samples of five of the

eight grassland topsoils examined (Ross, 1970) . Increase of dehydrogenase



ENZYMES ACCUMULATED IN SOIL



67



activity following 3 weeks of storage at -14OC took place in two of the

three soils studied by Ivarson and Sowden (1970). Even freezing at

-2OOC for 18 hours followed by thawing led to increased dehydrogenase

activity in some grassland topsoils (Ross, 1972), but storage at -2OOC

for 1-63 days and the subsequent thawing resulted in decreased dehydrogenase activity in all litter and soil samples from a hard beech forest (Ross

and McNeilly, 1972).

Storage at -10°C did not significantly affect the soil arylsulfatase activity (Tabatabai and Bremner, 1970b), nor did gelatinase and caseinase activities of soil suffer any considerable changes on storage at -8OC for

7-360 days (Ambrof, 1972). Phosphatase was only partially inactivated

in solonetz soils frozen for 45 days (Ponomareva et al., 1972). Ross and

McNeilly (1973) showed that storage of hard beech-forest litter and soil

at -2OOC for 24 hours had little influence on catechol-oxidizing activity.

Enzymes in soil are more resistant to high temperatures than enzymes

in pure preparations and solutions. Nevertheless, enzymes in soil could

also be completely destroyed by repeated steam heating, by dry heating

at high temperatures, and by autoclaving. The relative heat resistance of

enzymes in soil was observed by several investigators.

Studying invertase activity, Hofmann and Seegerer (1951b) found that

15-25% of the activity in a soil persisted following one and three heat

treatments by steaming. In Koepf's (1954a) experiment, an 80-minute

steaming did not destroy completely the soil invertase (the residual activity

was -15% 1. After dry heating at 1OSo, 120°, and 150° for 80 minutes,

the residual invertase activity in the samples of a chernozem was 78.4,

73.2, and 47.4%, respectively (Kiss, 1 9 5 8 ~ )No

. changes occurred in the

invertase activity of dry soil samples heated at 50°C for 25 days (Galstyan,

1965b, 1974). Autoclaving ( 2 atm for 2 hours) left unchanged 4-6% of

the invertase activity in peaty marsh soils (Kuprevich and Shcherbakova,

1966). About 17% of soil invertase activity persisted after a dry heat treatment (140OC for 3 hours) (Galstyan and Markosyan, 1967). AmbroB

(1973a,b) heated samples of rendzinas at 8OoC for 1 hour or at 14OOC

for 45 minutes and found that the residual invertase activity was nearly

60 and 30%, respectively.

Low residual p-glucosidase activity ( 1-4% ) was found in soil samples

submitted to dry heating at 16OOC (Hofmann and Hoffmann, 1953b) or

to autoclaving at 13OoC for 15 minutes (Hayano, 1973).

Amylase activity in samples of three soils dry-heated at 150°C for 30

hours decreased to - 5 % in a sandy and in a gravelly soil and to -25%

in a clay soil (Hofmann and Hoffmann, 1955). About 70% of amylase

activity in samples of a rendzina survived a 1-hour heating at 8OoC

( Ambrof, 1973a).



-



68



s.



KISS, M.



DRAGAN-BULARDA,



AND D.



RXDULESCU



The rendzina studied by AmbroZ (1973b) retained -50% of its cellulase activity following a 45-minute heat treatment at 14OOC. DrgganBularda ( 1974) found that dry-heating at 12OOC for 80 minutes left unchanged 34.3% of cellulase, 22.2% of levansucrase, 4% of levanase, and

20.5 % of dextranase activities in samples of a chernozem.

Peroxidase activity in soils resisted to a 3-hour dry heating at 18OOC

(Shatsman and Kalikina, 1972).

Residual urease activity in soil samples dry-heated at 78O, 8 8 O , and

98OC for 15 hours was 59.0, 49.3, and 32.6%, respectively (Rotini,

193%). Approximately 7% of the urease activity of a soil resisted two

heat treatments by steaming (Hofmann and Schmidt, 1953). Similarly,

about 7% of the urease activity was retained in a soil submitted to an

80-minute steaming by Koepf (1954b). Oven-drying at 160°C for 6 hours

and then adding urea to soil reduced NH, losses; i.e., the urease was only

partially destroyed during heat treatment (Musa, 1967). About 3% of

the urease activity persisted in soils autoclaved at 120°C for 15 minutes

(Said, 1972).

Dry heating of the samples of a rendzina and a chernozem at 130°C

for 1 hour led only to partial inactivation of the proteolytic enzymes. The

samples retained -50% of the gelatinase and -25% of the caseinase

activities ( Ambroi, 1966b). Nearly the same residual activity values were

found in samples of another rendzina heated for 1 hour at 8OoC (Ambrof,

1973a).

Chalvignac’s (1968) observation concerning heat resistance of the tryptophan-metabolizing enzyme system in soil has already been mentioned

in Section 11, B, 11.

Soil samples preheated to 8OoCfor 15 minutes retained -12% (mineral

soil) or 20% (organic soil) of their phosphatase activity (Halstead, 1964).

Residual phosphatase activity in samples of a rendzina heated for 1 hour

at 8OoC was 50-60% (Ambrot, 1973a). According to Khaziev (1969),

about one-third of the nuclease activity in chernozems of Bashkiria resists

dry heating at 100°C for 3 hours.

In samples of 13 soils dried at 105OC for 24 hours, the medium persistence of arylsulfatase activity was equal to 46% (Tabatabai and Bremner,

1970b).

Complete inactivation of catalase in different soils requires dry heating

at 145OC for 12-36 hours (Beck, 1971 ), Of course, only the residual H,O,splitting activity should be attributed to nonenzymatic catalysts.

3. Radiations



A series of experimental data already mentioned in preceding sections

of this paper show that activity of many soil enzymes persists after steriliza-



ENZYMES ACCUMULATED IN SOIL



69



tion with electron beam or 7-radiation, a fact emphasized also by Cawse

( 1969). Radiation-sterilized soil respires at a rate approaching that of the

nonsterile soil, which is attributed to persistence of the respiratory enzyme

activities in the dead microbial cells (Peterson, 1962). Roberge (1971 )

also concluded that respiratory enzymes were responsible for most of the

0,uptake in y-sterilized samples of a black spruce humus. But any enzyme

activity which persists after microorganisms have been killed can be destroyed by additional irradiation (SkujipS et af., 1962; Roberge and

Knowles, 1968b). At the same time, Cawse and Mableson’s (1971) investigations suggest that heavy 7-irradiations sufficient to destroy both cells

and enzymes in soil cannot stop production of CO,. This indicates that

CO, can also be formed by radiolytic decarboxylation of soil organic

matter.

It should be added that the influence of ultraviolet, infrared, and microwave radiations on soil enzymes has also been studied. After UV irradiation, catalytic activity of soil diminished (Scharrer, 1928). In a tropical

clay soil submitted to continuous infrared irradiation for 7 days, the count

of bacteria and actionomycetes was reduced to -50% while invertase activity remained unchanged. In four other soils, decreases of 13-29% in

the invertase activity occurred (Dommergues, 1960). Voets and Dedeken

(1965) submitted samples of a sandy loam to 40 and 90 MHz microwave

radiation, which resulted in a considerable diminution of both microbial

counts and activities of invertase and protease.

Effects of irradiation of soil on enzymes have been reviewed by McLaren

(1969).



FACTORS

B. CHEMICAL

The antibiotic preparation “BIN No, 7” exerted no influence on invertase activity in soil (Kuprevich, 1951) . Activity of the accumulated invertase remained unchanged in 50-g soil samples treated with benzylpenicillin

(200,000 IU), streptomycin sulfate (350 mg), sulfanilamide ( 150 mg),

2,4-dinitrophenol ( 150 mg), and NaN, (150 mg). After addition of HgC1,

(150 mg) and CHzO (10 ml of 40% solution), the residual activity values

of the accumulated invertase were -70 and 20%, respectively. However,

each of these compounds strongly inhibited the microbial synthesis of invertase when soil samples not treated with toluene were composted with

the substrate (sucrose) and incubated for 3 weeks (Kiss, 1958a). Methylene blue did not affect the activity of soil invertase. The invertase inhibitors, aniline and p-toluidine, brought about only 2341.5% inhibition of

soil invertase activity. The same concentrations of these inhibitors caused

70-90% reduction in the invertase activity of yeast cell suspensions and



70



s.



KISS, M. DRAGAN-BULARDA, AND D.



RXDULESCU



autolyzates, although the initial invertase activity was 10-20 times lower

in the soil than in the yeast suspensions and autolyzates examined. It is

deduced that the soil exerts a protective action against inhibition of soil

invertase activity. Comparison of the inhibitory effect of HgCI, on soil and

yeast invertase activities also revealed the protective action of soil (Kiss,

1958b).

In order to study the influence of partial sterilization with CS, on invertase activity, 85 ml of CS, were added to 100 g of air-dried soil. The mixture was kept at room temperature for 5 days and then filtered. The soil

was again kept at room temperature to permit a complete volatilization

of the residual CS,.The soil thus treated was submitted to invertase activity

determination. It was found that CS, did not bring about any changes in

invertase activity (Kiss, 1964).

For studying the influence of ethanol on soil invertase activity, reaction

mixtures were prepared in which the final ethanol concentration was

50-60% (v/v). It should be emphasized that even though the presence

of ethanol decreased invertase activity, the depression was never complete

(Kiss, 1964; Kiss and Drigan-Bularda, 1968b, 1970b; Kiss et al., 1972).

Kuprevich and Shcherbakova (1966) found that a 24-hour treatment of

2-g soil samples with 5 ml of 80% ethanol did not cause complete inactivation of the invertase, and 25% of the activity remained.

Chloromycetin used in a saturated aqueous solution did not stop hydrolysis of sucrose in soil. In soil samples treated with I-10% solutions of

chloromycetin in ethanol (final ethanol concentration in the reaction mixtures was 50% ), invertase activity decreased owing to ethanol but not to

chloromycetin (Kiss ad Driigan-Bularda, 1968b, 1970b; Kiss et al.,

1972).

The protective action of soil against enzyme inhibition and inactivation

is not absolute. Heavy doses of lead acetate (2.5-5 g per 10 g of soil)

completely inactivate the invertase in soil (Kiss, 1 9 5 8 ~ ) .

Dihydrostreptomycin exerted practically no effect on maltase activity in

soil. This activity was slightly reduced by HgCI, and more strongly by

AgNO, (Kiss and PCterfi, 1960). Chloromycetin used in a saturated

aqueous solution did not influence maltase and cellobiase activities in soil.

Lactase activity was slightly reduced. Ethanol at 50% concentration in

reaction mixtures decreased the activities of each oligase (Kiss et al.,

1972).

Mercuric chloride inhibited soil amylase activity only partially. In two

soils examined, 36% of amylase activity persisted although the HgCl, concentration in the reaction mixtures was 6 X lo-' N (Hofmann and Hoffmann, 1955).



ENZYMES ACCUMULATED IN SOIL



71



Benefield ( 1 97 1 ) measured soil cellulase activity in reaction mixtures

containing penicillin G in 2 x lo-' M concentration. Drggan-Bularda

( 1974) found that mercuric chloride, silver nitrate, copper sulfate, and

lead acetate used in lo-' M concentration were not able completely to

inhibit cellulase activity of a chernozem.

Levansucrase activity is detectable in reaction mixtures containing soil,

toluene, sucrose, and 3 M acetate buffer, 25% NaCI, saturated aqueous

2,4-dinitrophenol, or 2.5% streptomycin sulfate solutions (Kiss, 1961;

Kiss and Drigan-Bularda, 1968b). Of the seven phenol derivatives examined, only rn-nitrophenol inhibited completely the levansucrase activity

in soil. Partial but significant inhibitions occurred with 2,4-dinitrophenol,

2,5-dinitrophenol, catechol, resorcinol, and hydroquinone. Tyrosine caused

a slight inhibition (Kiss et al., 1963). Partial sterilization with CS2 did

not lead to any significant changes in soil levansucrase activity (Kiss,

1964). Ethanol at 50-60% concentrations in the reaction mixtures decreased levansucrase activity (Kiss, 1964; Kiss and DrBgan-Bularda,

1968b, 1970b; Kiss et al., 1972). Chloromycetin used in a saturated

aqueous solution did not prevent enzymatic formation of levan. When

]-lo% solutions of chloromycetin in ethanol were added to soil samples

(final ethanol concentration in reaction mixtures was 50% ), a strong depression in levansucrase activity occurred. The inhibition was caused by

the ethanol, not by the chloromycetin (Kiss and Drigan-Bularda, 1968b,

1970b; Kiss et al., 1972). Samples of a chernozem to which mercuric chloride was added in lo-? M concentration lost their levansucrase activity,

but the inhibition was incomplete when HgCI, was replaced with AgNO,,

CuSO,, or (CH:,COO),Pb (Dragan-Bularda, 1974).

Levanase and dextranase activities in soil persisted in the presence of

chloromycetin used in a saturated aqueous solution. Ethanol and 1-10%

chloromycetin solutions in ethanol reduced both levanase and dextranase

activities. Ethanol concentration in reaction mixtures was also 50%

(Driigan-Bularda and Kiss, 1972b). None of the four heavy metal salts

used in lo-: M concentration by Drigan-Bularda (1974) brought about

a complete inhibition of soil levanase and dextranase activities.

Sterilization of soil with ethylene oxide led to complete loss of the ethylbutyrate-hydrolyzing capacity but decreased the esterase activity toward

phenyl acetate only by half (Haig, 1955). Lipase-active extracts of a loamy

sand were treated with ethylenediaminetetraacetate (EDTA) , cupric acetate (Cu"), sodium sulfide ( S 2 - ) and ferric chloride (Fe") at 0.1 M levels.

Highly significant competitive inhibition of lipase activity was induced with

Cu'+, S'-, and EDTA at substrate (4-methylumbelliferone butyrate) levels

of 12.5 to 75.0 x lo-' M. Thus, each inhibitor blocked completely the



72



S.



KISS, M. DUGAN-BULARDA, AND D. R h U L E S C U



enzyme activity at 12.5 x lo-*M substrate concentration, but caused only

a -12% (Cuz+), -15%

(S2-), and -25% (EDTA) inhibition at

M substrate concentration. The Fe3+-inducedinhibition was

75.0 X

noncompetitive and nearly constant (-50% ) at all substrate levels

(Pancholy and Lynd, 1973). Getzin and Rosefield (1971) and Satyanarayana and Getzin (1973) found that phosphonate and phenyl thiophosphate derivatives were potent competitive inhibitors of the activity of malathion esterase extracted from soil. Inhibition was also observed with monoand dithiols, but not with diisopropyl fluorophosphate or SH group reagents.

The enzyme was not easily inactivated by heavy metal ions.

Oxidative decarboxylation of DL-DOPAthrough the action of a purified

soil-enzyme preparation containing o- and p-diphenol oxidases was inhibited by H,O, ( 5 X lo-, M) , KCN (0.6 X 1 O-, M ),diethyldithiocarbamate

M ) and 2,3-dimercapto-l-propanol(0.4X

M ) at rates of 74,

75,90,and 97%, respectively (Mayaudon et al., 1973b).

Soil urease activity as influenced by inhibitors has already been dealt

with in Section 11, B, 1.

Soil gelatinase activity decreased considerably in reaction mixtures

treated with 0.5% KMnO, or 1% Kclo, (Ambrot, 1963). In 0.05%

concentration, KNO, and KNO, led to some reduction of gelatinase activity

(AmbroZ, 1971 ) . Colloidal silver inhibited proteolytic activity of sandy

soils but did not affect proteolysis in loamy soils (Smol'yaninov, 1969).

Freezing followed by incubation increased the NH,-N in soil samples previously sterilized with ethylene oxide. It is possible that some of the NH,

released during incubation was the additive result of residual activities of

proteases and other soil enzymes (Campbell et al., 1971 ). o-Phenanthroline and HgCI, used in 2 x lo-, M concentration caused nearly complete inhibition of the protease activity of soil extracts toward N-benzyloxycarbonylL-phenylalanyl-L-leucine.Inhibitions by 2 X 1O-,M concentration of EDTA

and p-phenyl propionate was 82 and 88% , respectively (Ladd, 1972).

Sodium azide used in 1.66 and 3.3% concentrations diminished asparaginase activity in soil (Mouraret, 1965).

Peroxidase activity of a soil extract toward o-dianisidine was inhibited

M concentration of either KCN or Na,S

strongly but incompletely by

(Burge, 1973).

Martin-Smith (1963) has found that uricase activity in soil extracts obtained at pH 7 and pH 8.4 responds differently to inhibitors. NaCN and

NaN, inhibited completely (extract at pH 7) or partially (extract at pH

8.4) the uricase activity. Other compounds, such as diethyldithiocarbamate, EDTA, cysteine, 2,3-dimercapto-l-propanol, monoiodoacetate,

p-hydroxymercuribenzoate, and HgC12, exhibited partial inhibition of uricase activity of both soil extracts.



ENZYMES ACCUMULATED IN SOIL



73



Halstead ( 1 964) moistened 5-g samples of air-dried soil with 10 ml

of H,O plus 5 ml of 0.1 or 0.4 M NaF solution and determined the phosphatase activity of the mixtures. Maximum inhibition was 60% in a mineral soil and -9% in an organic soil. Stronger but incomplete inhibitory

effect of NaF on soil phosphatase activity was observed by Yaroshevich

( 1966). Addition of KF, HgCl,, CH,O, and tannin led to slight decreases

in soil phosphatase activity (Goian, 1972).

No arylsulfatase activity was detected after treatment of soil samples

with HgCl,, but phosphate, sulfite, and cyanide caused only partial reductions of the activity (Tabatabai and Bremner, 1970a).

Catalase activity in soil is strongly inhibited by HCN and slightly by

HgCI, (Konig et al., 1906). CuSO, and AICI, also caused slight decreases

in the catalytic activity (Scharrer, 1928). KCN and NaNO, strongly inhibited catalase activity in soil (Rotini, 1931, 1932; Vhly, 1937). According to Kuprevich (1951 ), catalase activity was not inhibited by the antibiotic preparation “BIN No. 7.” The mineral salts studied by Galstyan

( 1957, 1974) reduced to some extent catalase and peroxidase activities

in soil. Inhibition was due to the anions SO,”, C1-, POa3-,and NO,-. KC10,

caused a partial inhibition of catalase activity (AmbroZ, 1963).

The influence of pesticides on enzyme activities in soil has been studied

by many investigators (Table V ) . Most of these studies are devoted to

the herbicides. Effects of the pesticides on soil enzymes depend on many

factors including the chemical nature and dose of the pesticide, type of

the enzyme, type of the soil, conditions of the experiment (laboratory or

field), etc. The results show either unchanged, increased, or decreased soil

enzyme activities following pesticide application, In many cases, the following situation can be pictured: “un sol biologiquement tuC par addition massive d’un herbicide toxique peut garder (ou m&me acqukir) un pouvoir

enzymatique t d s tlevt” (Vojinovic er al., 1961) .

In the studies referred to in Table V, the determination of soil enzyme

activities as influenced by pesticides was carried out usually in association

with counting of bacteria, actinomycetes, fungi, and microorganisms belonging to different physiological groups. The enzymatic methods did not

serve as substitutes for the microbiological methods. A special case was

reported, however (Rodriguez-Kabana et al., 1970), in which the simple

method of determining invertase activity replaced the more laborious

method of counting fungi. The effect of the herbicide eptam (EPTC) on

the growth of a soil-borne phytopathogenic fungus, Sclerotium rolfsii, was

studied. A sandy loam soil was sterilized by autoclaving and inoculated

with the fungus. After a 24-hour incubation, the soil culture was treated

with eptam in a nutrient solution. Fungal growth was measured in terms

of soil invertase activity, as mycelial dry weight was found to give signifi-



74



S. KISS, M. DRAGAN-BULARDA, AND D. RXDULESCU



TABLE V

Studies Concerning the Influence of Pesticides on Enzyme Activities in Soil

Pesticides

Herbicides



Enzymes

Invertase



References



Balasubramanian et al., 1973; Bliev, 1973a,b; Chulakov and Zharasov, 1973; Chunderova and Zubets,

1969, 1971; Chunderova et al., 1971; Gamzikova,

1968; Gamzikova and Svyatskaya, 1968, 1970;

Geshtovt ef al., 1974; Ghinea, 1964; Gruzdev et al.,

1973; Keller, 1961; Kiss, 1958~;Krezel and Musial,

1969; Krokhalev e f al., 1973; Kruglov and BeiBienko, 1971; Kruglov e f al., 1973; Kulinska, 1967;

Livens et al., 1973; Mereshko, 1969; Nikitin and

Svechkov, 1973; Soreanu, 1972; Svyatskaya, 1972;

Voets et al., 1974; Walter and Bastgen, 1971; Zinchenko and Osinskaya, 1969; Zinchenko e f al., 1969;

Zubets, 1967, 1968a,b, 1973a,b

8-Glucosidase

Keller, 1961;Voets et al., 1974; Walter and Bastgen,

1971

Amylase

Balasubramanian et al., 1973; Beck, 1973; Bliev,

1973a,b; Chunderova and Zubets, 1969; Mereshko,

1969; Zubets, 1967, 1968b

Cellulase

Giardina et al., 1970; Mereshko, 1969

Peroxidase

Mereshko, 1969; Spiridonov and Spiridonova, 1973 ;

Spiridonov et al., 1973

Polyphenol oxidase Mereshko, 1969

Urease

Chunderova and Zubets, 1969, 1971; Chunderova

etal., 1971;Gamzikova and Svyatskaya, 1968,1970;

Giardina ef al., 1970; Gruzdev et al., 1973; lshizawa

et al., 1961; Krezel and Musial, 1969; Krokhalev

et al., 1973; Kruglov and Bei-Bienko, 1971;Kruglov

et al., 1973; Kulinska, 1967; Livens et al., 1973;

Manorik and Malichenko, 1969; Markert, 1974;

Mereshko, 1969; Namdeo and Dube, 1973a,b; Nikitin and Svechkov, 1973; Pel’tser, 1972; Svyatskaya,

1972; Voets et al., 1974; Walter, 1970; Walter and

Bastgen, 1971;Zinchenko and Osinskaya, 1969; Zinchenko et al., 1969; Zubets, 1967, 1968a,b, 1973a,b

Asparaginase

Krezel and Musial, 1969

Protease

Beck, 1973; Chulakov and Zharasov, 1973; Chunderova and Zubets, 1969, 1971; Chunderova et al.,

1971; hinea, 1964; Giardina ef al., 1970; Krezel

and Musial, 1969; Kruglov and Bei-Bienko, 1971;

Kruglov et al., 1973; Mereshko, 1969; Namdeo and

Dube, 1973a,b; Spiridonov and Spiridonova, 1973;

Zubets, 1967, 1968a,b, 1973a,b

Nitrate reductase Spiridonov and Spiridonova, 1973

Phosp hatase

Chulakov and Zharasov, 1973; Chunderova and Zubets, 1969, 1971; Chunderova ef al., 1971; Goian,

1969; Gruzdev et al., 1973; Livens et al., 1973;

Manorik and Malichenko, 1969; Voets et al., 1974;

Walter and Bastgen, 1971; Zubets, 1967, 1968a,b,

1973a,b



ENZYMES ACCUMULATED IN SOIL



75



TABLE V (Continued)

Pesticides

Herbicides



Enzymes

Catalase



Dehydrogenase



Fungicides



lnvertase

p-Glucosidase

Amylase

Urease

Phosphatase

Catalase

Dehydrogenase



Insecticides



Invertase

0-Glucosidase

Amylase

Urease

Protease

Phosp hatase

Catalase

Dehydrogenase



Nematicides



lnvertase

Urease

Catalase

Dehydrogenase



References

Beck, 1973; Bliev, 1973a,b; Gruzdev el al., 1973;

Krokhalev et al., 1973; Kruglov and Bei-Bienko,

1971; Kruglov et al., 1973; Kulinska, 1967; Latypova e f al., 1968; Leusheva and Mel'nik, 1969;

Mereshko, 1969; Nikitin and Svechkov, 1973; Protasov, 1968, 1970; Putintseva, 1970; Soldatov, 1968;

Soldatov et al., 1971; Spiridonov and Spiridonova,

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Voets and Vandamme, 1970

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Naumann, 1970a, 1972



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III. Enzymatic Activities in Soil under Conditions Unfavorable for the Proliferation of Microorganisms

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