Sulfur transformations i n soil, involving t h e metabolism of inorganic sulfur compounds, such as sulfate, sulfide, a n d polythionates, a n d of organic sulfur compounds, a r e of profound i m p o r t a n c e i n t h e n u t r i t i o n of plants. N o t o n l y does t h e p l a n t n e e d for its development t h e sulfur compounds w h i c h a r e obtained o n l y from t h e soil, b u t t h e processes of germination a n d p l a n t g r o w t h a r e m a r k e d l y influenced b y t h e presence of sulfur compounds such as h y d r o g e n sulfide or thiosulfate.
A . F O R M S O F S U L F U R I N S O I L
T h e sulfur of soil exists i n various forms, including inorganic sulfates a n d sulfides a n d e l e m e n t a r y sulfur a n d also organic compounds w h i c h are mostly of biological origin. I t h a s b e e n calculated t h a t from 80 to 9 0 % of t h e sulfur i n soil is present i n organic combination a n d t h a t o n l y about 1 0 - 2 0 % is present as sulfate. P l a n t residues contain organic sulfur compounds; alfalfa {Medicago sativa), for example, contains 0 . 2 9 % sulfur, t u r n i p {Brassica rapa) tops 0 . 9 % ; a n d w h e a t {Triticum aestivum) s t r a w 0 . 1 2 % ; this sulfur is e v e n t u a l l y transformed into sul-fate i n t h e soil.
M u c h is n o w becoming k n o w n of t h e biological transformations of sulfur i n soil [see reviews b y S t a r k e y ( 2 3 1 ) , B u n k e r ( 2 9 ) , a n d Butlin ( 3 1 ) ] . G u i t t o n e a u (81) a n d Roach (206) h a v e shown t h a t sulfur m a y u n d e r g o biological attack w i t h t h e formation of thiosulfate, a n d Guit-toneau a n d Keilling (82) h a v e found t h a t heterotrophic organisms can t r a n s f o r m sulfur into thiosulfate a n d tetrathionate. T h e autotrophs Thiobacillus thiooxidans a n d Thiobacillus thioparus accomplish t h e oxidation of thiosulfate to sulfate a n d sulfur, a n d a v a r i e t y of hetero-trophs oxidize thiosulfate to tetrathionate ( 2 2 7 ) . M a n y y e a r s ago Lockett (145) demonstrated t h a t w h e n thiosulfates a n d other poly-thionates (except dithionate) a r e passed t h r o u g h sewage sludge t h e y a r e oxidized, microbiologically, to sulfate. T h e polythionates u n d e r g o both biological a n d nonbiological transformations into sulfur a n d sul-fate. Vishniac (251) has s h o w n t h a t t h e oxidation of thiosulfate b y Thiobacillus thioparus is accompanied b y t h e formation of tetrathionate a n d trithionate. Moreover, elemental sulfur m a y arise i n cultures of T. thioparus b y a nonbiological m e c h a n i s m , excess thiosulfate catalyz-ing t h e dismutation of tetrathionate to trithionate a n d pentathionate, t h e latter breaking d o w n to tetrathionate a n d sulfur ( 2 5 1 ) . It h a d been suggested earlier b y T a m i y a et al. (241) t h a t spontaneous decomposi-tion of tetrathionate gives rise to sulfur a n d trithionate. Vishniac a n d
718 J. H . Q U A S T E L
S a n i e r (252) h a v e proposed a comprehensive scheme to cover t h e oxida-tion of thiosulfate, tetrathionate, a n d sulfur. T h i s scheme envisages t h a t sulfur enters t h e cell b y reversible combination w i t h protein thiol groups, a n d t h e n it condenses w i t h i n t r a c e l l u l a r sulfite to form thio-sulfate, w h i c h becomes oxidized b y w a y of tetrathionate to sulfate.
Sulfate reduction is effected largely b y a specific group of. anaerobic organisms generally referred to as m e m b e r s of t h e genus Desulfovibrio.
T h e culture first described b y Beijerinck ( 1 9 a ) , a n d t h e one to w h i c h reference is u s u a l l y m a d e , is Desulfovibrio desulfuricans. T h e sulfate-r e d u c i n g bactesulfate-ria a sulfate-r e w i d e l y distsulfate-ributed as t h e y asulfate-re able to gsulfate-row on various organic substances a n d also i n t h e presence of e l e m e n t a r y h y d r o g e n a n d t h e y c a n also tolerate w i d e r a n g e s of t e m p e r a t u r e a n d salt content a n d h i g h concentrations of sulfide ( 1 6 5 ) . T h e y a r e readily obtained from soil, m u d , fresh a n d salt w a t e r sediments, a n d sewages.
T h e y a r e responsible for most of t h e sulfide occurring as ferrous sulfide i n m a r i n e sediments a n d i n waterlogged soils. It should be recalled in this connection t h a t sulfate is one of t h e most a b u n d a n t ions in sea water. Redfield (205) has pointed out t h a t t h e quantities of oxygen in t h e sea m a y h a v e been regulated b y t h e activities of sulfate-reducing organisms, w h i c h h a v e t h e ability to u s e sulfate as a n oxidizing source.
T h e over-all reaction
S 04— — S— + 2 02
is m a d e u p of two m a i n reactions w h i c h occur in different locations:
SO4-" + 2 C (carbon compound) -> 2 C 02 + S ~ 2 C 02 -> 2 C + 2 02 (photosynthesis)
T h u s microbiological sulfate reduction is a n indirect, b u t i m p o r t a n t , source of atmospheric oxygen. P r e s u m a b l y m u c h of the sulfide so formed h a s been laid d o w n in s e d i m e n t a r y rocks.
A p a r t from t h e necessity of t h e presence of inorganic sulfur in t h e form of sulfate for p l a n t nutrition, t h e r e is reason to believe t h a t or-ganic sulfur compounds a r e also necessary, e.g., for optimal root development a n d growth. T h i a m i n e is a l r e a d y k n o w n to be of impor-t a n c e i n impor-this connecimpor-tion. Possibly oimpor-ther sulfur-conimpor-taining subsimpor-tances, such as biotin, thioethanolamine, lipoic acid, m e t h i o n i n e , t a u r i n e , m a y also be implicated.
B. O X I D A T I O N O F S U L F U R I N S O I L
Sulfur oxidation i n soil takes place u s u a l l y b y t h e operations of t h e thiobacilli, b u t it is also b r o u g h t about b y t h e photosynthetic p u r p l e a n d green sulfur bacteria. A brief description of t h e physiology of thiobacilli is given b y Baalsrud ( 1 3 ) .
6 . M I C R O B I A L A C T I V I T I E S O F S O I L A N D P L A N T N U T R I T I O N 7 1 9
Thiobacillus thiooxidans, described b y W a k s m a n a n d Joffe in 1 9 2 2 , converts sulfur into sulfuric acid a n d is able to w i t h s t a n d considerable acidity, e.g., p H values between 0 a n d 1 , a n d it m a y survive for long periods i n this acid condition. T h i s group of organisms is economically i m p o r t a n t because it can cause r a p i d corrosion of concrete ( 3 3 ) . It is of obvious i m p o r t a n c e i n soils as it brings about a lowered p H , w i t h consequent increased availability to t h e p l a n t of phosphates a n d certain metallic ions, a n d possibly also a m o r e favorable p H a n d i m p r o v e d soil structure for p l a n t growth. Sulfur has been used, i n this m a n n e r , to combat m a n g a n e s e deficiency, a condition often encountered i n soils subjected to excessive liming, or w i t h increased p H , or w i t h a h i g h content of organic m a t t e r . H o w e v e r , some of t h e r e m e d i a l effects of sulfur i n counteracting m a n g a n e s e deficiency m a y be due to t h e libera-tion of thiosulfate ( 1 9 3 ) as well as to t h a t of acid. Thiobacillus thio-oxidans is a strict a u t o t r o p h w h i c h oxidizes sulfur, thiosulfate, or tetra-thionate to sulfate. Its o p t i m u m p H for these oxidations is 2 . 0 to 3 . 0 , a n d it fails to grow appreciably above p H 6 . 0 . I t is encountered i n all soil e n v i r o n m e n t s t h a t h a v e become acid b y oxidations of sulfur or its compounds.
Thiobacillus thioparus, t h e first of this group to be described ( b y N a t h a n s o n i n 1 9 0 2 a n d n a m e d b y Beijerinck) is a strict autotroph, oxidizes sulfur slowly a n d polythionates such as thiosulfate w i t h greater rapidity. T h e reactions involved a r e as follows:
5 N a2S203 + 4 02 + H20 5 N a2S 04 + H2S04 + 4 S 2S + 3 02 + 2 H20 -> 2 H2S04
T h e organism, w h i c h is widely distributed i n soils a n d w a t e r s , grows well n e a r n e u t r a l i t y , causing s o m e w h a t acid conditions (between p H 4 a n d 5 ) w h i c h w h e n m a i n t a i n e d cause t h e death of t h e organism.
Thiobacillus denitrificons, w h i c h m a y be a v a r i a n t of T. thioparus, w a s described b y Beijerinck as a n autotrophic organism w h i c h oxidizes thiosulfate w i t h reduction of nitrate. It has been established ( 1 4 ) t h a t although n i t r a t e is utilized b y the organism, it cannot supply t h e nitro-gen for assimilation; a m m o n i a c a l nitronitro-gen suffices for this purpose.
T h e organism can g r o w aerobically w i t h o u t n i t r a t e , b u t it needs both n i t r a t e a n d a m m o n i a for anaerobic growth. I t develops best n e a r n e u t r a l i t y a n d oxidizes sulfur, a n d thiosulfate m o r e rapidly, in ac-cordance w i t h t h e following reactions:
Na2S203 + 2 02 + H20 Na2S04 + H2S04
2 S + 3 02 + 2 H20 -> 2 H2S04
5 Na2S203 + 8 ΚΝΟ3 + H20 5 Na2S04 + 4 K2S04 + H2S04 + 4 N2 5 S + 6 ΚΝΟ3 + 2 H20 3 K2S04 + 2 H2S04 + 3 N2
Some sulfur is u s u a l l y formed d u r i n g t h e thiosulfate oxidation.
720 J. H . Q U A S T E L
O t h e r organisms placed, for t h e t i m e being, i n t h e Thiobacillus family are Thiobacillus novellus ( 2 2 8 ) , a facultative anaerobe t h a t oxidizes thiosulfate to sulfate; Thiobacillus ferrooxidans ( 4 3 , 243) a n autotroph t h a t oxidizes not o n l y thiosulfate, b u t also ferrous ions u n d e r acid conditions; a n d Thiobacillus thiocyanoxidans ( 8 5 , 86, 279) a strict autotroph t h a t oxidizes thiocyanate, thiosulfate, a n d sulfur. M a n y of t h e thiobacilli oxidize sulfides at low concentrations, b u t t h e r e exists a group of sulfur bacteria t h a t a r e a p p a r e n t l y adapted to t h e aerobic oxidation of sulfide or h y d r o g e n sulfide i n solution. T h e s e a r e t h e fila-m e n t o u s bacteria Beggiatoa a n d Thiothrix ( 2 1 ) . T h e y a r e able to deposit sulfur i n granules w i t h i n their cells, oxidizing it to sulfate w h e n t h e supply of sulfide is depleted. W i n o g r a d s k y (272, 273) reported t h a t t h e y can oxidize two to four times their weight of h y d r o g e n sulfide daily.
A group of sulfur bacteria resembles green plants i n t h a t its m e m b e r s r e q u i r e light for g r o w t h (119) a n d contain p i g m e n t s of t h e carotene a n d chlorophyll class. T h e s e organisms m a y be r e d (Chromatium, Thio-pedia), owing to h i g h carotene content, or green (Chlorobium), owing to t h e chlorophyll present. T h e colored sulfur bacteria c a r r y out a reac-tion, analogous to t h a t i n plants, n a m e l y :
light
CO2 -f H2S > carbon complexes + H20 + S
T h e y can oxidize t h e sulfur further to sulfuric acid. T h e y a r e strict anaerobes a n d a r e plentiful (e.g., i n certain lakes in C y r e n a i c a ) w h e r e sulfur is being produced n a t u r a l l y , a n d t h e y m a y t h e r e contribute to t h e sulfur formation. T h e green b a c t e r i u m Chlorobium thiosulfato-philum oxidizes sulfur, sulfide, thiosulfate, a n d tetrathionate to sulfate, b u t C. limicola oxidizes o n l y sulfur a n d sulfide. All the p u r p l e a n d green bacteria a r e able to develop i n t h e absence of organic m a t t e r , using carbon dioxide as their source of carbon a n d reduced sulfur com-pounds, t h e oxidation of w h i c h provides e n e r g y for growth. T h e y are capable also of nitrogen fixation (134, 135, 2 6 6 ) .
Oxidation of Polythionates in Soil
Gleen a n d Quastel (75) used a soil perfusion technique w h i c h m a d e it possible to s t u d y t h e transformations of sulfur compounds in soil u n d e r conditions w h i c h a p p r o x i m a t e d to those in t h e field; t h e y found that, u n d e r aerobic conditions, thiosulfate is transformed i n soil to sulfate a n d tetrathionate, or to sulfate a n d sulfur, the former products being t h e m o r e c o m m o n l y occurring. T h e presence of relatively high concentrations of phosphate, or of thiosulfate, tends to favor t h e
produc-6 . M I C R O B I A L A C T I V I T I E S O F S O I L A N D P L A N T N U T R I T I O N 7 2 1
tion of sulfur a n d sulfate. Soils, exposed to thiosulfate, become enriched w i t h thiosulfate-oxidizing organisms, a n d such soils will r e t a i n their oxidizing activities for several m o n t h s if t h e y a r e dried a n d stored at 0°C. T e t r a t h i o n a t e is oxidized i n t h e soil to sulfate d u r i n g perfusion at room t e m p e r a t u r e , t h e organisms responsible being also capable of oxidizing thiosulfate. T e t r a t h i o n a t e is a n o r m a l intermediate in t h e conversion of thiosulfate to sulfate i n soil. T h e kinetics of thiosulfate a n d tetrathionate oxidation i n soil point to the presence of adaptive enzymes, w h i c h oxidize these sulfur compounds, in t h e organisms in-volved. T r i t h i o n a t e is oxidized to sulfate in soils, but dithionate is v e r y resistant to breakdown.
2. Effects of Biological Inhibitors on Thiosulfate Oxidation in Soil Sodium azide ( 0 . 0 1 % ) a n d sulfanilamide ( 0 . 1 % ) inhibit thiosulfate oxidation i n soil, b u t t h e latter acts o n l y b y r e t a r d i n g the proliferation of t h e organisms responsible ( 7 5 ) . Chloretone, a narcotic t h a t inhibits nitrification, also inhibits thiosulfate oxidation i n soil. T h e presence of 2,4-dinitro-o-cresol a n d 2,4-dinitro-o-phenol at low concentrations sup-presses thiosulfate oxidation i n soil. T h i s indicates t h a t phosphorylation m e c h a n i s m s m a y be involved in microbiological thiosulfate oxidations, a fact to be correlated w i t h t h e observations of Vogler a n d U m b r e i t ( 2 5 3 ) on t h e esterification of inorganic phosphate d u r i n g t h e oxida-tion of sulfur b y Thiobacillus thiooxidans. Arsenites, selenites, a n d tel-lurites inhibit thiosulfate oxidation i n soil, b u t arsenates, selenates, a n d tellurates a r e w i t h o u t effect. Sodium p y r u v a t e is also h i g h l y inhibitory, b u t glucose is w i t h o u t effect ( 7 5 ) .
3 . Effects of the Presence of Sugars and Amino Acids
I n view of t h e fact t h a t soil, at a n y time, m a y contain transient quantities of sugars a n d a m i n o acids, it is of interest to k n o w t h e effect of such substances on sulfur metabolism in soil.
Perfusion studies ( 7 5 ) show t h a t t h e presence of a m i n o acids in-creases t h e r a t e of oxidation of thiosulfate to tetrathionate, possibly b y favoring t h e g r o w t h of heterotrophs w h i c h are capable of this oxida-tion (e.g., Pseudomonas fluorescens). T h e presence of glucose, sucrose, or m a n n i t o l favors t h e reduction of tetrathionate to thiosulfate i n soil.
It is evident t h a t tetrathionate can u n d e r g o both oxidation to sulfate a n d reduction to thiosulfate according to the conditions in soil, t h e presence of sugars favoring t h e reductive process. T h e reduction of tetrathionate to thiosulfate b y intestinal organisms is a well-known p h e n o m e n o n sometimes used for diagnostic purposes ( 1 1 7 , 1 8 3 ) .
722 J. H . Q U A S T E L
C. M E T A B O L I S M O F S U L F U R A M I N O A C I D S I N S O I L
M u c h of t h e sulfur in agricultural soils in h u m i d or semiarid regions is organic in character (50, 2 6 4 ) . Relatively little is k n o w n of t h e m a n -n e r i-n w h i c h this sulfur is co-nverted to sulfate i-n soil.
Using the soil perfusion technique, F r e n e y (62) has shown t h a t cysteine is oxidized to sulfate in soil, the steps i n t h e process being as follows: cysteine -» cystine -> cystine disulfoxide -> cysteine-sulfinic acid -» sulfate. T h e first step is nonbiological, the r e m a i n d e r are bio-logical a n d i n t h e soil perfusion a p p a r a t u s exhibit t h e kinetics charac-teristic of effects attributable to proliferating organisms. Cystine disulf-oxide w a s observed, as a n intermediate, b y c h r o m a t o g r a p h y of the soil perfusate. T a u r i n e w a s n o t detected; n o r is it a n intermediate i n cysteine oxidation.
Although these steps represent t h e over-all m o d e of breakdown of cysteine in soil, it m u s t be b o r n e i n m i n d t h a t a variety of soil or-ganisms, w h e n examined separately, will oxidize cysteine to different products. T h u s cystine is broken d o w n b y Achromobacter cystinovorum to sulfur as a final product ( 1 5 ) ; b y Microsporum gypseum to sulfite a n d sulfate ( 2 2 3 ) ; b y other soil organisms to sulfur, polythionates, and sulfate ( 2 3 3 ) .
M e t h i o n i n e is k n o w n to be broken down to m e r c a p t a n s b y the an-aerobe Clostridium tetanomorphum (278) a n d to m e t h y l m e r c a p t a n a n d d i m e t h y l sulfide b y Scopulariopsis brevicaulis (151) a n d b y M . gypseum a n d Aspergillus niger ( 3 5 ) . It will form m e r c a p t a n s a n d sul-fides i n soil ( 1 9 2 ) . M e t h i o n i n e decomposition, however, takes place very slowly, in soils, compared w i t h t h a t of other a m i n o acids, a n d n o n i t r a t e appears u n t i l t h e m e t h i o n i n e h a s been fully decomposed. M e t h i o n i n e doubtless produces a variety of substances, besides t h e m e r c a p t a n s , that can exercise a suppressing effect on soil nitrification. T h e presence of other forms of organic m a t t e r stimulates b r e a k d o w n of methionine in soil ( 2 3 3 ) .
Using t h e soil perfusion technique, Frederick, Starkey, a n d Segal (61) h a v e found t h a t cystine, t a u r i n e , a n d taurocholate readily form sulfate in soils, t h i a m i n e is less easily broken down, a n d such sub-stances as methionine, thiourea, phenylthiourea, e t h y l x a n t h a t e , sul-fathiazole, or sulfonemethane show almost no breakdown d u r i n g a period of 6 weeks' perfusion. M e t h i o n i n e forms, to some extent, m e t h y l -m e r c a p t a n a n d its oxidized for-m d i -m e t h y l disulfide. T h i o u r e a , w h i c h is h i g h l y inhibitory to soil nitrification a n d w h i c h is broken d o w n v e r y slowly i n a n agricultural soil, can be attacked b y Aspergillus a n d Pénicillium w i t h sulfate formation ( 1 0 0 ) .
6. M I C R O B I A L A C T I V I T I E S O F S O I L A N D P L A N T N U T R I T I O N 7 2 3
D . S U L F A T E R E D U C T I O N I N S O I L
T h e sulfate-reducing bacteria, of w h i c h Desulfovibrio desulfuricans is a typical example, a r e strictly anaerobic a n d use sulfate as the h y d r o g e n acceptor. Sulfite, thiosulfate, a n d tetrathionate m a y , however, be used instead of sulfate. H y d r o g e n donors m a y be formate, lactate, a m i n o acids, carbohydrates, a n d h y d r o g e n itself. W h e n it utilizes h y d r o -gen, t h e organism behaves as a n autotroph ( 3 2 ) , t h e e n e r g y for growth being derived from t h e reaction:
4 H2 + C a S 04- > H2S + Ca(OH)2 + 2 H20
Microbiological sulfate reduction m a y occur a t m o d e r a t e a n d h i g h temperatures ( 5 5 - 6 0 ° C ) , t h e cultures showing t h e characteristics of mesophils or thermophils, t h e latter of w h i c h produce spores. T h e spor-ing a n d nonsporspor-ing forms are a p p a r e n t l y different groups of bacteria.
T h e y are w i d e l y distributed a n d are of great importance in modifying plant fertility in waterlogged or semianaerobic soils. T h e y a r e also of economic i m p o r t a n c e as bacterial reduction of sulfate is concerned in the disintegration of concrete, in t h e corrosion of metals, a n d in lethal effects on fish in t h e oceans a n d in lakes. Oxygen is a strong inhibitor of the metabolism of Desulfovibrio desulfuricans ( 6 4 a ) .
T h e process of sulfate reduction involves t h e participation of cyto-chrome c3 ( 1 8 6 ) . T h i s w a s a n unexpected observation, as the cyto-chromes w e r e not believed to exist i n anaerobic bacteria. All the mesophilic ( 3 0 ° ) strains of Desulfovibrio desulfuricans contain cyto-chrome c3 a n d desulfoviridin, b u t these pigments are not detectable in the strains of t h e thermophilic D. thermodesulfuricans g r o w n at 5 0 -55°. T h e s e organisms do n o t reduce selenate, but selenate acts as a competitive inhibitor to sulfate ( 1 8 4 ) . Monofluorphosphate, w h i c h has a structural analogy to sulfate, is also a competitive inhibitor, b u t sub-stituted sulfates do not affect the reaction ( 1 8 5 ) . A study b y Butlin, Selwyn, a n d W a k e r l e y (34) of the microbiological reduction of sulfate in sewage sludge has shown t h a t sterilized sludge, fortified w i t h sulfate a n d inoculated w i t h D . desulfuricans yields b u t little sulfide. T h e u n -sterilized sludge, supplemented w i t h sulfate, a n d inoculated w i t h crude cultures of sulfate-reducing bacteria obtained from sewage, produces appreciable quantities of sulfide. T h u s , o n l y w h e n m i x e d populations of sulfate-reducing bacteria a n d other microorganisms derived from sewage a r e used is considerable sulfate reduction obtained. Doubtless increased rates of formation of the organisms w h i c h metabolize sewage sludge components a r e necessary for t h e production of t h e h y d r o g e n donors t h a t a r e required for the reduction of sulfate b y t h e proliferating
724 J . H . Q U A S T E L
sulfate reducers. P r e s u m a b l y , similar conditions exist in soils w h e r e r a p i d sulfide formation takes place. Studies of t h e microbial metabolism in p a d d y soils (240) h a v e shown t h a t after the initial stages of iron reduction a n d n i t r a t e disappearance, t h e r e is active sulfide formation.
Moreover, i n t h e final stage, following initial carbon dioxide produc-tion, h y d r o g e n a n d t h e n m e t h a n e a r e evolved. Such soils are rich in sulfate-reducing organisms ( 6 5 ) .
E . T H E C Y C L E O F S U L F U R T R A N S F O R M A T I O N S I N S O I L
As a l r e a d y mentioned, the interconversions of thiosulfate a n d tetra-thionate i n soils involves the activities of both autotrophic a n d hetero-trophic organisms. I n fact t h e conversion of thiosulfate to sulfate m a y be suppressed if sufficient organic m a t t e r (e.g., carbohydrate) is present to stimulate t h e reduction of tetrathionate to thiosulfate. A n o t h e r product of thiosulfate b r e a k d o w n is sulfur itself, w h i c h undergoes oxida-tion b y appropriate organisms to thiosulfate a n d t h e n c e to tetrathionate a n d sulfate. So a cycle of operations takes place in soil, this cycle being extended u n d e r anaerobic or semianaerobic conditions, as sulfate, t h e n , undergoes biological reduction to h y d r o g e n sulfide w h i c h in t u r n is oxidized to sulfur [see Butlin (31) or Butlin a n d Postgate (33) for a description of t h e sulfur cycle i n soils].
T h e study of sulfur metabolism i n soil shows h o w varied species of organisms m a y arise t h a t are capable of attacking both the initial sub-strate a n d t h e products derived from it. These dependent organisms develop almost simultaneously, forming a biological complex that ac-complishes a cycle of events. I n this cycle t h e sulfur m a y act in a catalytic role because, b y its varied transformations, it secures the g r o w t h of t h e groups of organisms w h i c h obtain e n e r g y for develop-m e n t frodevelop-m oxidations a n d reductions of specific sulfur-containing sub-stances. If t h e cycle is blocked at a n y point, accumulation of a sulfur product at t h e blocked point will progress u n t i l n o further change occurs. Proliferation of the responsible organisms will t h e n cease, for the sulfur is no longer available for energy-yielding purposes a n d the majority of organisms involved in t h e cycle will t h e n cease to m u l t i p l y a n d will disintegrate, leaving only a few h a r d y m e m b e r s to c a r r y on operations again w h e n favorable conditions r e t u r n ( 1 9 2 ) .
F . I N F L U E N C E O F M A N G A N E S E D I O X I D E
It is well established t h a t u n d e r optimal aerobic conditions the trans-formations of sulfur compounds i n soil lead to m a x i m u m yields of sulfate. It is n o t e w o r t h y t h a t t h e properties of m a n g a n e s e dioxide, w h i c h can accomplish the oxidation of sulfides a n d thiol compounds,
6 . M I C R O B I A L A C T I V I T I E S O F S O I L A N D P L A N T N U T R I T I O N 7 2 5
Concentrations (mM) producing 50 % inhibition
Plant Of root growth Of germination
Garden pea 4.0 31.0
Cress 4.7 26.0
Cabbage 6.0 20.0
Rape 10.0 25.0
Maize 11.0 31.0
Flax 20.0 33.0
Radish 25.0 80.0
Mustard 27.0 15.0
Carrot 41.0 38.0
"From Audus and Quastel (11).
cates the concentrations of thiosulfate required to b r i n g about 5 0 % inhibition of t h e n o r m a l rates of germination a n d of root growth of various plants in w a t e r culture ( 1 1 ) . It is obvious t h a t t h e r e a r e selec-tive herbicidal effects, t h e root g r o w t h of t h e g a r d e n pea (Pisum sativum) being far m o r e sensitive to thiosulfate t h a n t h a t of carrot
ferrous ions, polyphenols, etc. ( 9 5 ) , h a v e i m p o r t a n t consequences in soil chemistry. It is well k n o w n t h a t thiol compounds act in a h a r m f u l m a n n e r i n soil either b y depriving soil microflora of oxygen or b y en-couraging t h e development of anaerobes or b y accomplishing specific toxic effects on the plant. T h e presence of m a n g a n e s e dioxide in a soil, will, so long as it is in excess, r e n d e r the soil relatively free from thiol compounds. W h e n the anaerobic conditions a r e replaced b y aerobic, the m a n g a n e s e ions are reconverted to m a n g a n e s e dioxide a n d t h e soil store of this substance is replenished. T h u s t h e m a n g a n e s e dioxide-man-ganese cycle acts as a n oxidation buffer system protecting t h e soil or-ganisms, including t h e h i g h e r plants, against deleterious agents such as a variety of sulfur compounds a n d a variety of other reducing bodies.
It m a y well be t h a t a n indispensable constituent of a fertile soil is t h e presence i n it of such a substance as m a n g a n e s e dioxide t h a t will ac-complish t h e oxidation of toxic compounds formed w h e n the oxygen supply becomes limited or w h e n it disappears altogether.
G . H E R B I C I D A L E F F E C T S O F T H I O S U L F A T E S
T h e herbicidal effects of thiosulfates are relevant to t h e subject of sulfur metabolism i n soil in relation to p l a n t nutrition. T a b l e I X
indi-T A B L E I X
EFFECTS OF SODIUM THIOSULFATE ON PLANT GROWTH"
726 J. H . Q U A S T E L
{Daucus carota var. sativa). T h e reason for t h e toxicity of thiosulfate to root g r o w t h of certain plants is u n k n o w n . D i t h i o n a t e a n d trithionate a r e t e n times less effective t h a n thiosulfate u n d e r t h e identical experi-m e n t a l conditions.