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SOIL MICROBIOLOGYl
By H. G. THORNTON AND JANE MEIKLEJOHN
Rothamsted Experimental Station, Harpenden, Hertfordshire, England

The field of Soil Microbiology was last reviewed in this journal by Loch­
head in 1952. The present review is thus intended to deal with the period from
1952 to 1956 inclusive, although a few papers published before this period
have been included for various reasons. A complete coverage of the literature
is not possible in a review of this length, and where a subject has been re­
cently reviewed the authors have only mentioned the subject briefly and have
Annu. Rev. Microbiol. 1957.11:123-148. Downloaded from www.annualreviews.org

quoted the review as a source of references.

TECHNIQUE
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Soil microbiologists have been concerned for a long time with the prob­
lem of studying the soil micropopulation in the natural solid soil as little
affected by manipulation as possible. A method for demonstrating microor­
ganisms in sections of soil has been developed by Alexander and Jackson.
A core sample stained in bulk with cotton blue is vacuum-impregnated with
a polyester resin and sectioned by a method similar to that used for rock
specimens. This method is very promising, particularly for the observation
of fungal hyphae (1).
The method initiated by Rossi and Cholodny, in which the growth of
microorganisms is observed on slides buried in soil, is used in its original
form as well as in various modifications (60, 182). It has always given results
difficult to interpret in terms of microbial habit in the soil mass itself; but
useful information has been obtained on antibiosis by modified Rossi­
Cholodny methods. Dobbs & Hinson have used one to study fungistasis (47);
Chinn, and also Stevenson, have placed fungal spores on slides and inserted
them in soil. By subsequent examination of the preparations the percentage
germination can be estimated, while by pregerminating the spores, deformed
growth of the hyphae, or lysis, can be observed (35, 199). Methods of isolat­
ing Acrasieae from soil, by using a suspension of edible bacteria, either sprin­
kled on soil, or in agar, have been developed by Kitzke (105) and by Borg
(19).
Most methods used for the study of soil microorganisms, however, still
depend on making a suspension of the soil. In the most direct application of
this method, films are made from the suspensions, and the organisms in
them examined microscopically. Tchan has used fluorescence microscopy
for observing and counting algae, and Tchan & Bunt have developed a
method in which protozoa, fixed in the wet film with osmic acid or formalin
vapour, are then stained with erythrosin and methyl green (208, 213).

1 The survey of the literature pertaining to this review was concluded in December,
1956.

123
 124 THORNTON AND MEIKLEJOHN
Experiments made to test the agreement between estimates of the num­
bers of microorganisms in replicate samples of soil, usually based on plate
counts, have given very different results in different localities and soil condi­
tions. In contrast with the good agreement obtained in past work on the very
long term arable experiments of Rothamsted, Rose & Miller found very
great variation in plate counts of fungi from replicate soil cores taken from
virgin land and pasture in New Zealand, and have proposed a method for
reducing error by bulking numerous cores (176).
In some cases plate counts of bacteria made at a range of dilutions give
estimates of numbers per gram that rise with the degree of dilution. Lavergne
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& Augier attribute this to the retention of bacteria by the internal surfaces
of the pipettes used in making and distributing the dilutions, and also to
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the break-up of clumps of bacteria (112). The same effect would, of course,
be observed if the soil contained some factor inhibiting bacterial grDwth on
agar, which was progressively removed by increasing dilution of the soil
suspension (138). Miller and his colleagues recommend the use of oxgall as a
bacterial inhibitor in agar media for isolating fungi and yeasts, as it can be
sterilized in the medium (11, 143), and de Barjac proposes the use of soil
humic acid to acidify media used to grow organisms from acid soils (41).
Several methods based on fractionation of soil suspensions have been
used for the isolation of fungi (4, 113, 234); Chesters & Thornton ha.ve com­
pared six different techniques for isolating soil fungi, and find that two of
them, dilution plates and Warcup's soil plates, favour species which sporu­
late abundantly. The greatest variety of species was obtained by the screened
immersion plate method of Thornton (34, 235).
Among techniques for estimating the total microbial activity in a soil,
the macrorespirometer of Swaby & Passey may be mentioned (205). Pochon
and his colleagues measure various types of microbial activity by comparing
the rates at which a reaction takes place in media inoculated with a series of
dilutions from a soil suspension (43). Tchan has proposed that nutrients
should be assessed by measuring the growth of the indigenous algal flora of
a soil with and without added test compounds (211).
EFFECTS OF SOIL CONDITIONS ON THE MICROFLORA
LOCALITY AND TYPE

Bacteria.-It is usually supposed that all species of soil bacteria have a

world-wide distribution; Prevot & Moureau have shown that this is probably
true of the common anaerobic bacteria, which they have isolated from a
variety of soils, including some from the Antarctic (169). Curiously enough,
thermophilic bacteria have been found by McBee & McBee, in an Arctic
soil which is frozen for most of the year (128).
A relation between the quality of the bacterial flora of a soil and its fer­
tility was found by Po chon & Coppier, who compared neighbouring fertile
and infertile soils from two localities in France. The fertile soils contained
more microorganisms in general, but fewer cellulose decomposers than in-
 SOIL MICROBIOLOGY 125
fertile soils; and non-symbiotic nitrogen fixers were found in the fertile, but
not in the infertile soils (164). On the Broadbalk wheat field at Rothamsted,
on the other hand, Skinner, Jones, & Mollison found larger numbers of
bacteria, actinomycetes, and fungi in plot 2B, given farmyard manure, than
in plot 7, given artificials, or plot 3, unmanured; but there was little differ­
ence in numbers between these last two plots, which differ greatly in their
yield of wheat (190). Pochon and his colleagues have shown that a compost
may contain a high total number of bacteria developing on agar plates, and
yet be very poor in nitrifiers, nitrogen fixers, and other important groups
(166).
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The most striking effects of soil amelioration on the microflora are shown
by reclaimed peaty soils which, like acid forest soils, are very poor in micro­
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organisms in their natural state. De Barjac has made a detailed study of the
microflora of several types of peat before and after improvement (42).
Boquel, Kauffmann, & Toussaint, in a study of the tropical forest soils of the
Ivory Coast, found increased numbers of nitrogen-fixing clostridia, and of
cellulose-decomposers, during the rainy season. Clearing the forest decreased
the numbers of the latter (18).
Fungi.-Peyronel represents the character of thefungus flora of a particular
soil by dividing the species into 8 groups, and showing the frequency of each
group on a compass diagram. He has compared the flora of different tem­
perate and tropical soils by this method (163). Stenton has reported on the
fungus flora of the soil of Wicken Fen (195), and Gordon on the occurrence
of Fusarium species on cereal plots in Canada (62). Zeidberg & Ajello report
on the presence of two pathogenic fungi in Tennessee soils (248). Forest and
agricultural soils were compared by Welvaert & Veldeman, who found a
greater variety of fungi in polder soil (pH 7.S) than in a sandy loam forest
soil (pH 4.3). They suggested that, in the latter, the antagonistic action of
Trichoderma and Penicillium might be an important factor (239). The short
time needed for trees to affect the micro flora is illustrated by work reported
by Meyer, who found differences in the fungal population under pasture
and under tree saplings (141). An influence of the type of tree growing on
forest soils is suggested by the results obtained by Chase & Baker, who
showed that the ratio of fungi to bacteria and actinomycetes was higher
under conifers than under maples (33).
The soil yeasts are a little-known group that has been studied recently
by Capriotti (32) in Holland and by Di Menna (46) in New Zealand. Those
found in New Zealand soil included the pathogen Candida albicans.

VERTICAL DISTRIBUTION OF MICROORGANISMS

The distribution of microorganisms down a sandy soil profile is reported

in a paper by Blue, Eno, & Westgate. Highest numbers occurred in the top
six inches. Very few microorganisms were found in the A2 horizon, nine to
twelve in. down, which was deficient in nutrients. More were found between
12 and 30 inches below the surface; numbers at this level were increased by
 126 THORNTON AND MEIKLE]OHN
dressings of potassium and of nitrate (15). Tchan & Whitehouse have shown
that algae are confined to the top few mm. in wet soil, and that there is no
evidence that they can live under the soil surface as heterotrophs (214).
Garbosky reports that Azotobacter is found at depths down to two metres in
Argentine soils, and that it may be more abundant between 50 and 100 cm.
down than at the surface (58). The distribution of fungal species at different
levels in sandy podsol profiles was studied by Jeffreys and co-workers, who
found that plate counts decreased generally with depth but showed a
secondary maximum in the B horizon, noticeable for the preponderance of
Mucor at this level (92). Guillemat & Montegut observed, in plots from the
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long-term field experiments at Grignon (69), that different species of fungi

occurred at different depths. Burges & Fenton conclude that the ability of
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fungi to live deep in the SOli is a consequence, not, as is commonly supposed,

of their ability to do without oxygen, but of their ability to withstand high
concentrations of carbon dioxide (25).

NUTRIENTS

Starkey has reviewed the whole subject of the need of different micro­
organisms for inorganic nutrients (193). Jensen has shown that Azotobacter
needs much more magnesium than the related genus Beijerinckia, which,
unlike Azotobacter, cannot partly replace its need for molybdenum by using
vanadium (95, 96). Shug et al. have thrown more light on the reason why
some microorganisms need molybdenum, by showing that it is a cofactor
for the hydrogenase of Clostridium pasteurianum (186).
Lochhead & Thexton found that an important group of soil bacteria re­
quired vitamin Bl2, replaceable by an aqueous extract of soil (125). More
than a quarter of the 500 isolates from soil studied by Lochhead & Burton
were found to require one or more of the following growth factors: thiamin,
biotin, Bl2, pantothenic acid, folic acid, nicotinic acid, and riboflavin (122).
In soil, the growth factor requirements of such bacteria can, no doubt, be
supplied by other organisms; for example, Burton & Lochhead found that
several species, especially of Rhizobium, can synthesise vitamin B12
(27). Soil extract has also been found by Lochhead & Burton to contain at
least one growth factor other than B12, and not supplied by yeast extract.
Culture filtrates from a number of soil bacteria having simple nutrient re­
quirements were able to supply a growth factor having the same effect. One
of them, named Arthrobacter pascens, synthesises such a factor, to which a
related species, Arthrobacter terregens, is exacting. Soil extract is therefore
useful in the study of soil bacteria, not only as a source of minerals, but also
of some organic nutrients (123).

PARTIAL STERILISATION

In their early work on partial sterilisation, Russell & Hutchinson sug­

gested that increased bacterial activity following partial sterilisation was
due to the destruction of soil protozoa. Singh & Crump used the improved
 SOIL MICROBIOLOGY 127
dilution technique, developed by the former (Singh), to estimate numbers of
amoebae in soils from forest nursery beds, untreated and partially sterilised
with steam and formalin. Bacterial counts were also made by plating. In
the formalin-treated soil, bacterial numbers rose above those in the untreated,
and numbers of amoebae were reduced. But in steamed soil, numbers of both
bacteria and amoebae increased over those in the untreated soil. These
effects were found to persist over a period of six months (187). It is thus un­
safe to generalise as to the effects of different types of partial sterilisation on
relative numbers of amoebae and bacteria. Stout's qualitative observations
of steamed glasshouse soil also showed that a number of species of protozoa
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survived the treatment (202). The fungal population seems to be more dras­
tically affected by partial sterilisation of soil. Mollison followed the changes
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in fungi in the same forest nursery plots that were examined by Singh and
Crump. Both steam. and formalin treatments almost completely eliminated
the fungi and, even after later recolonisation, the plate "counts" of fungi
were much reduced, an effect which lasted for the 25 months during which
counts were made. The fungal population was still varied after steam treat­
ment, but after formalin, Trichoderma viride appeared to be the principal
species that recolonised the soil (146). This fungus is exceptionally tolerant
of formalin. Wensley, in a paper giving useful data on the immediate micro­
biological effects of soil treatment with several fumigants, reports that after
treatment with methyl bromide, soil was recolonised in 4 weeks, mainly by
Aspergillus (240). Evans also followed the recolonisation of soil by fungi
after partial sterilisation, in this case with formalin and chlorpicrin (53). War­
cup showed that Pythium in forest nursery soils is killed by steam or formalin
(233). There is also a change in the relative proportions of different groups
of bacteria in soil following partial sterilisation. Thus Davies & Owen found
that ammonia accumulates in steamed glasshouse soils, because the nitrify­
ing bacteria are killed (39); and Holding found an increase in the percentage
of Gram-negative bacteria after steaming. This group also increased after
the addition of fresh organic matter or the growth of oat seedlings, suggest­
ing that the effect of steaming may be partly due to release of nutrients which
favour these bacteria (84).
An interesting specific effect was noted by Bromfield in some experi­
ments with soil treated with carbon tetrachloride. After treatment these
soils evolved hydrogen sulphide from ammonium sulphate added to them,
apparently owing to the activity of Bacillus megaterium, which, when iso­
lated from the soil, would carry out this reduction in pure culture. The action
of carbon tetrachloride was to eliminate certain bacteria which prevent this
reducing activity of B. megaterium from taking place in untreated soil (21).
The practical aspects of disinfestation of soil by heat, flooding and fumiga­
tion have recently been reviewed by Newhall (151).
Weedkillers and other poisons.-More and more very poisonous sub­
stances are being added to soils all over the world to kill weeds or insects,
and it is fortunate that most of them have been found, on investigation,
 128 THOR�TON AND MEIKLEJOHN
to have no lasting harmful effect on useful soil microorganisms. Magee &
Colmer (129), for instance, found that Azotobacter was poisoned in culture
only by much larger doses of herbicides than would ever be used in practice,
and the same was found to be true of four commonly-used insecticides by
Callao & Montoya (31), who worked with soil as well as liquid cultures.
Gray has carried out a series of studies on the effects of hexachlorocyclo­
hexane and its gamma isomer (Gammexane), and finds that the etfect of
both isomers is very much less in soil than in culture media; but it did reduce
the count on soil-extract agar plates (66). Stanek (191) reports that Gam­
mexane actually stimulates Azotobacter, however, and Koike & Gainey (108)
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and Jones (101) find that the total plate count of bacteria is increased by
large doses of 2-4-D, CADE and DDT; and none of these three compounds
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affected nitrification in any dose likely to be used in practice. Surface·-active

agents are regularly added as spreaders to agricultural sprays; Ivarson &
Pramer have found that Tween 80, a non-ionic compound, was rapidly de­
composed in soil, and had little or no undesirable biological effect. The cati­
onic spreader Ceepryn was more slowly decomposed, and in large doses it
reduced the total plate count and hindered nitrification. An anionic com­
pound, Nacconol NRSF, on the other hand, was not decomposed at all, and
had serious and lasting toxic effects (89). The same may be true of radioac­
tive phosphorus, and Goring & Clark recommend that it should not be used
for experiments on plants if the soil in which the plant is growing is meant
to be in its natural state (63).
ACTIVITIES OF SOIL MICROORGANISMS
SOIL STRUCTURE

There is evidence that some fungi may hold the soil together by the net­
work of their mycelium; Downs, McCalla, & Haskins found that one out of
twelve cellulose-decomposing fungi improved the structure of a soil poor
in organic matter (50). The gum produced by Agrobacterium radiobacter im­
proved aggregation (173); Rorem suggests that bacterial gums, besides in­
creasing aggregation, may be important to the species which produce them
as a mechanism whereby they can concentrate ions that they need out of the
surrounding soil (175). Hely & Bonnier found that synthetic soil condi­
tioners increased the numbers of bacteria which produced natural gums,
and so had a double effect on soil structure; the synthetic compounds were
not toxic (76). Mortensen & Martin found that two synthetic soil condition­
ers were not toxic to microorganisms, but were very resistant to decomposi­
tion (147). In certain soils be addition of synthetic aggregating substances
has been found to improve nodulation of soy beans and of lucerne (18S, 78).
BREAKDOWN OF NATURAL CARBON COMPOUNDS

Not much interest is being taken at present in this aspect of Soil Micro­
biology. Reese & Levinson have compared the breakdown of cellulose by dif­
ferent species; Kox found that aerobic bacteria, as well as fungi, are responsi-
 SOIL M ICROBIOLOGY 129
ble for the breakdown of cellulose and pectin in Sphagnum peat, and McBee
describes a thermophilic anaerobe which can decompose cellulose (110, 127,
172).
Until recently, fungi were thought to be the only organisms capable of
decomposing lignin; but Fischer, Bizzini, Raynaud, & Prevot have found
that bacteria which can break down lignin are very widespread, and espe­
cially numerous in forest soils. All their strains were species of Pseudomonas,
and most of them could attack benzoate and other aromatic carbon com­
pounds as well as lignin (55). Henderson & Farmer found that some soil
fungi could utilize aromatic compounds such as syringaldehyde, which might
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be breakdown products of lignin (79). Veldkamp found that a number of

soil microorganisms can decompose chitin; actinomycetes seem to be the
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most numerous. Twenty-three different actinomycete species were found to

be chitin-decomposers, and likewise 50 species of bacteria, including the
myxobacterium Cytophaga johnsonae. Ammonia and acetic acid are the final
breakdown products in cultures of this species and of a new species, Pseu­
domonas chitinovorans (220). The breakdown of pectin in fallen leaves has
been studied by Wieringa; he finds that the first agent of breakdown is al­
ways the fungus Pullularia pullulans, which is present on the surface of
leaves while they are still on the tree. Pectin-decomposers in acid soils are
mostly fungi, but in well-limed soils, actinomycetes predominate (242).

THE NITROGEN CYCLE

Soil microbiologists have written over a hundred papers on this sub­

ject since 1951, but their interest is very unevenly distributed; over three­
quarters are concerned with the fashionable subjects of Azotobacter and
nitrification. There is practically no work on the formation of ammonia,
which is overdue for investigation by modern methods. It is usually sup­
posed that the breakdown of proteins is the source of soil ammonia; but
Veldkamp has recently shown that chitin, which is abundant in soil in fungus
hyphal walls and arthropod integuments, is an important ammonia source
(220). He incubated chitin in soil, and found that up to 60 per cent of the
nitrogen in it was recovered as nitrate, presumably formed by the oxida­
tion of ammonia. It is also possible that nitrogen fixers supply ammonia
directly to the soil (as Winogradsky thought), for Delwiche & Wijler found
that most of the nitrogen fixed in their experiments could be accounted for
as nitrate (44).
Nitrification.-There have been recent reviews on this subject by Lees
(116, 117) and Meiklejohn (132, 134). It is becoming increasingly apparent
that the agents of nitrification are the classical autotrophic nitrifiers of
Warington and Winogradsky, which are ubiquitous, and which convert
ammonia quantitatively to nitrite and then to nitrate. There are several
recent reports of heterotrophic microorganisms which form nitrite or nitrate
by oxidation; but, if the amounts are stated, they are always very small
(54, 56, 85, 88). The very laborious dilution method is still the only satis-
 130 THOR�'l'TON AND MEIKLEJOHN
factory way of counting nitrifiers in soil (37). Many of the colonies which
develop on Winogradsky's silica-gel plates are not nitrifiers, and Millbank
found that a method with agar disks, similar to Singh's method for protozoa,
would not work because agar and soil together were toxic to Nitrosomonas
(59, 86, 142). It is possible to compare the nitrifying activity of different
soils by measuring the rate of nitrification in enrichment cultures, or by the
Lees & Quastel percolation method, if the soil structure is good enough (133,
200). This method was used by Stevenson & Chase, who found that nitrifica­
tion was less under a grass cover than under bare fallow (200). Mills (144)
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has also found that different African grass species depress the forma.tion of
nitrate to different degrees. In the Uganda soil that he studied, there was an
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accumulation of nitrate in the top 6 inches in the dry season, though the soil
was acid. Meiklejohn found that this soil contained autotrophic nitrifying
bacteria (133). Jacquemin & Berlier found that there were very few nitrifiers
in a forest soil from the Ivory Coast, and many more in cleared land (90).
Burning the vegetation over a Kenya soil was found by Meiklejohn to kill
the nitrifiers (136).
There has not been much work on the physiology of the nitrifying bac­
teria, mainly because of the enormous difficulty of getting them to grow in
pure culture. This may be partly due to their need for some growth factor
which they can obtain readily in soil, and which is lacking in culture media;
but Gundersen (70) tried various vitamins of the B group on pure cultures
of Nitrosomonas, and Meiklejohn (131) tried several other possible stimu­
lants in enrichment cultures, in both cases with entirely negative results.
Though Gundersen (70) found that several amino-acids are very toxic to
Nitrosomonas, and though Jensen & S¢rensen (100) found that the same
was true of some organic sulphur compounds, there does not seem to be any
truth in the belief that organic matter as such has a mysterious toxic effect
on nitrification.
Goldberg & Gainey (61) have studied the effect of clay minerals on am­
monia oxidation, and find that ammonium ions are more readily oxidized
by enrichment cultures if free in solution than if adsorbed on the clay. This
is quite contrary to earlier results of Lees & Quastel with soil (see Lees, 116).
Lees (115) has found, by using very dilute solutions, that hydroxylamine
is an intermediate product in the oxidation of ammonia by Nitrosomonas
cells, and ImshenetskiI & Ruban (87) have shown that it is oxidized by cell­
free autolysates. Hydroxylamine is also formed in the oxidation of pyruvic
acid oxime by heterotrophs; further oxidation to nitrite, in these species as
well as in Nitrosomonas, is blocked by hydrazine (120). It would be interest­
ing to know if chelating agents such as allylthiourea, which Lees (114), and
Hofman & Lees (83), found to stop ammonia oxidation at a very low con­
centration in suspensions, have the same effect in soil. Lees & Simpson find
that the oxidation of nitrite by Nitrobacter is interrupted at different stages
by chlorate and by cyanate. Nitrobacter contains more than one cytochrome,
 SOI L MICROBIOLOGY 131
and they are reduced as nitrite is oxidized (118,119). In view of these results
it is most puzzling that Engel, Krech, & Friederichsen conclude that neither
iron nor zinc-containing enzymes are involved in the oxidation of nitrite,
though Nitrobaeter needs iron for growth (52). These workers also investi­
gated the amino acids in Nitrobaeter, and found the same 18 that Hofman
had found in Nitrosomonas, and that they themselves had found in Hypho­
mierobium. The list does not include aIpha-epsiIon-diaminopimelic acid. Hof­
man found four sugars, galactose, ribose, rhamnose and xylose, but oddly
enough, no glucose, in his Nitrosomonas preparations (81).
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Several workers find that the ratio of nitrogen oxidized to carbon assim­
ilated is higher in old than in young cultures of nitrifiers, Hofman & Lees
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(82), looking at this from a thermodynamic point of view, think that the
ratio increases because Nitrosomonas needs more energy to keep increaing
concentrations of toxic nitrite out of its cells. But, as Engel et al. point out,
this can hardly be true of Nitrobaeter, which forms a less toxic compound,
nitrate, from the more toxic nitrite (52). A more probable explanation is
given by Bomeke, who thinks that there is a progressive loss of carbon from
old cultures, as the cells break down some organic storage material to keep
themselves alive (16).
Enrichment cultures have been studied by Klein, who found a way to
get rid of Nitrobaeter, which can be a very troublesome contaminant of
Nitrosomonas, by supplying ammonia in the form of ammonium borate (106).
Imshenetskii (86) and also Bisset & Grace (12) claim that there are no
genera of autotrophic nitrifying bacteria other than Nitrosomonas and Nitro­
baeter, and that the genera Nitrosoeystis, Nitrosogloea, Nitrosospira, and
Nitroeystis, described by Winogradsky and his colleagues, are not nitrifiers
(86, 12). They base this criticism on the observation that nitrifying cultures
may be contaminated with Myxobaeteria, whose fruiting bodies could have
been mistaken for zoogloeal organisms responsible for the nitrification. More
definite evidence is needed to substantiate so comprehensive a criticism.
Indeed, Palleroni has claimed to have isolated Nitrosospira sp. from Ant­
arctic and Argentine desert soils and found that it was a nitrifier (155, 156).
Denitrification. Wij le r & Delwiche, using isotopic nitrogen and soil,
-

showed that denitrification is probably entirely due to microbial action, as

all the nitrogen in the reduction products was derived from nitrate, which ex­
cludes the formation of nitrogen by a non-biological reaction between nitrite
and amino groups. They also found that nitrous oxide, as well as nitrogen
gas, was released when soil and nitrate were incubated together (243). The
soil they used therefore presumably contained organisms such as the
Denitrobaeillus species studied by Verhoeven, that produce nitrous oxide as
well as nitrogen in the reduction of nitrate (221). The effect of aeration on
denitrification may vary with the species of bacteria present in a soil, as
Marshall et al. found that different Pseudomonas strains are differently af­
fected by aeration. One strain may only reduce nitrate under conditions of
 132 THORNTON AND MEIKLEJOHN

almost complete anaerobiosis, while another may be so little affected by oxy­

gen that it is almost impossible to stop it reducing nitrate in culture by in­
creasing the air supply (130).
Nitrogen fixation.-There has been a recent experiment with iE,otopic
nitrogen by Delwiche & Wijler, the results of which were almost entirely
negative. In the soil that they studied they found negligible fixation in bare
fallow, and very little under grass (44). In consequence of this, some micro­
biologists may conclude that non-symbiotic nitrogen fixation never adds
any nitrogen to any soil in any circumstances. But, if one leaves the labora­
tory and turns to the field, it is obvious that the nitrogen supply is main­
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tained in soils in which legumes are not growing, and in which leaching cer­
tainly, and denitrification probably, takes place. The evidence as to non­
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biological fixation is most contradictory, but recently BjaHve has shown

that light is not an agent of nitrogen fixation (13). Biological fixation has been
reviewed by Wilson & Burris (245), by Fogg (57), and again by Wilson (244),
who deals especially with the mechanism of fixation.
Azotobacter.-There is a certain irony in the fact that so much is being
written about Azotobacter, as it is becoming more and more doubtful if this
genus is of real practical importance in adding to the soil's nitrogen supply,
for there seem to be many soils, in various parts of the world, where it is
never found (20, 102, 135). Where it does occur, it is usually found in very
small numbers, and not only in poor soils, like the Arno Atoll soils examined
by Stevenson (197), for Meiklejohn (137) found less than 2000 Azotobacter
cells per gram throughout a series of counts on Rothamsted soil. But Pochon
and his colleagues record a count on the very fertile Nile silt, in which about
8000 Azotobacter per gram of dry matter, as well as nitrogen-fixing clostridia,
were present (167). Counting Azotobacter in soil is difficult, however; neither
Hely & Bonnier (76) nor Meiklejohn (137) were able to obtain consistent
results with Winogradsky's method of "plaques moulees"; and when they
tried his other method, of crumbs of soil sprinkled on silica gel, they found
that a colony of Azotobacter developed from every crumb. Eventually they
used surface inoculation on r:itrogen-poor agar, as did Tehan (207), who also
used a dilution method with liquid cultures. Absence or scarcity of Azoto­
bacter may be due to lack of moisture, to lack of calcium or phosphate, and
perhaps of other nutrients (135, 206). It might even be due to excess of oxy­
gen, as Parker (158) has found that Azotobacter fixes nitrogen more efficiently
under reduced oxygen tension; but lack of water is an equally probable ex­
planation for the scarcity of Azotobacter near the surface of soils in Argentina,
described by Garbosky (58).
Inoculation with Azotobacter to increase the yield of various crops is regu­
larly practised in Russia, but it does not seem to be uniformly successful
(180, 226, 228, 241). Petrenko suggests that many of the negative results
may be due to the use of unsuitable cultures; it is well known to all micro­
biologists who have worked with Azotobacter that long-continued mainte­
nance in artificial culture alters its properties, and use of an old stock culture
 SOIL MICROBIOLOGY 133
from a type collection may well lead to confusing results (162). On the other
hand, it is possible that some positive results of inoculation are due to fertiliz­
ers added with the bacterial culture (9). Bukatsch & Heitzer claim that
strains of Azotobacter isolated from the rhizospheres of different plant species
differ in nitrogen-fixing power; it is unfortunate that they examined one
strain only from each species of plant, and still more unfortunate that their
experiment on Azotobacter-inoculated peas was carried out in open pots, so
that infection with Rhizobium cannot be excluded as the cause of the fixation
observed (24).
Parker has produced evidence that Azotobacter fixes nitrogen more
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efficiently in the presence of other bacteria than in pure culture. His freshly­
isolated cultures fixed 18 mg. N per gram sugar decomposed when the
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Azotobacter was still contaminated with a small motile rod; but when this
last contaminant was removed, fixation in the pure culture went down to
three mg. N per gram sugar, and only gradually improved after several trans­
fers in a nitrogen-poor medium (160).
It is generaJly supposed that Azotobacter does not grow or fix nitrogen at
any pH more acid than 6.0, but recently several acid-tolerant Azotobacter
strains have been found. Jensen (97) has described a new species, Azotobacter
macrocytogenes, and acid-tolerant varieties of known species have been found
by Tchan (209), Dobereiner (48), and Metcalfe (139). A new species, Azoto­
bacter halophilum, which will only develop in saline media, has been found
in saline soils in Siberia by Blinkov (14).
Beijerinckia.-Jensen has shown that there are good reasons for separat­
ing the aerobic acid-resistant nitrogen fixers of tropical soils from Azotobacter
and placing them in the genus Beijerinckia. They differ from Azotobacter in
morphology (the cells are much smaller), and also in being able to fix nitrogen
at pH 3.5, in needing no calcium, and in being unable to use vanadium in
place of molybdenum. Azotobacters occur in the tropics in calcareous soils,
but tropical soils are commonly acid, and here Beijerinckias, which are effi­
cient but slow nitrogen fixers, replace them (96). Many attempts have been
made without success to isolate Beijerinckia from temperate-zone and sub­
tropical soils (210). Derx (45) attributed the tropical distribution of this
genus to a possible association with some special genera of plants, perhaps
legumes which do not form nodules (e.g. Cassia spp.), and suggested that
Beijerinckia is a facultative symbiont which, unlike Rhizobium, has not lost
the power to fix nitrogen outside the plant. On the other hand, Kluyver &
Becking (107) think that Beijerinckia may be confined to lateritic soils.
There is a recent report of the occurrence of Beijerinckia outside the tropics,
as Suto has isolated a nitrogen-fixer, which seems from his description to be­
long to this genus, from an acid volcanic soil at Sendai, Japan (lat. 38°N)
(204). Ruinen has found a new habitat; she has discovered large numbers of
Beijerinckia cells on the leaves of trees and epiphytes in the tropical forests
of Indonesia, a fact which may explain the lavish vegetation of the forest on
a soil which gives very poor yields of crops when cleared and planted (179).
 134 THORNTON AND MEIKLEJOHN

Clostridium.-Though very little has been written about Clostridium

pasteurianum (and related species) in recent years, it is quite possible that
these anaerobes account for much more nitrogen fixation than does. Azoto­
bacter. In the first place, they are much more widely distributed than
Azotobacter; Rybalkina (181) in Russia, Kaila (102) in Finland, Boswell (20)
in England, Meiklejohn (135) in East Africa, and Tchan & Beadle (212) in
Australia, found them always, or nearly always present in every soil ex­
amined. They are also far more numerous; in contrast to the thousand
Azotobacter cells per gram, Clostridium cells number hundreds of thousands
(74, 137). Hart found from a hundred thousand to a million per gram of
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garden soil, nine-tenths of them vegetative cells and one-tenth spores.. Num­
bers in an oakwood soil were somewhat smaller (74).
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It has generally been supposed that clostridia were poor fixers of nitro­
gen, adding only about two to four mg. per gram of sugar decomposed. But
Parker (159) has recently shown that, given suitable cultural conditions, a
strain of Clostridium butyricum can do as well as the best Azotobacter, fixing
27 mgm. N per gram sugar. To obtain this level of fixation it is necessary to
grow the bacteria in presence of carbon dioxide as well as nitrogen, in ab­
sence of carbon monoxide, and to supply them with growth factors. Parker's
strain required biotin and para-aminobenzoic acid, and a strain studied by
Virtanen & Lundbom (227) required folic acid.
It might be objected that strict anaerobes could not multiply fast enough
to be able to fix much nitrogen in the topsoil; but Hart found that his nitro­
gen-fixing clostridia were able to grow under aerobic conditions if supplied
with combined nitrogen. They did not fix nitrogen aerobically; but it is quite
possible that clostridia could grow in topsoil if combined nitrogen were pres­
ent, and then, in local pockets of anaerobiosis, or at times of temporary
waterlogging, proceed to fix nitrogen when the original supply was exhausted
(74).
Other Nitrogen-fixers.-The blue-green algae are probably the most
efficient of all non-symbiotic nitrogen fixers. De & Mandai estimate that,
given sufficient phosphate and molybdenum, algae in flooded rice soils can
fix as much as 70 lb. nitrogen per acre in six weeks (40). Blue-green algae are
also able to fix nitrogen in some symbiotic systems, for Bond & Scott showed
that lichens and liverworts can fix nitrogen if Nostoc is present as a partner
in them (17). Douin showed that the nodules on the roots of Cycads con­
tained a species of Anabaena (49). There is also an increasing list of organ­
iims which can only fix very small quantities of nitrogen, in many cases so
small that fixation can only be detected by the use of isotopic nitrogen. Met­
calfe et at. (140) used this method to find that two yeasts, isolated by the
percolation method from acid health soils, were able to fix nitrogen. Ander­
son (3) describes another poor nitrogen fixer which is apparently a Pseudo­
monas, and Brown (23) has found two nitrogen-fixing Nocardia, one of which
could decompose cellulose. Newton & Wilson (152) report that the purple
sulphur bacterium Chromatium can fix small quantities of nitrogen, and
 SOIL MICROBIOLOGY 135
Hamilton & Wilson (71) have been able to show, by using isotopic nitrogen,
that Aerobacter aerogenes, which has long been suspected of being a nitrogen­
fixer, can fix small amounts anaerobically in a well-buffered medium.

MICROORGANISMS AND INORGANIC SOIL CONSTITUENTS

Evidence continues to grow that microorganisms can make various in­

organic nutrients available to plants by bringing them into solution. Brom­
field found that several common species of soil bacteria, Bacillus circulans,
Bacillus megaterium, and Aerobacter aerogenes, could reduce ferric compounds
in the presence of a suitable hydrogen donor and so increase the available
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iron (and manganese) in soils (22). Aristovskaya points out that the acid
produced by some microorganisms may be an important agent of soil
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formation, especially in podzols. She found that the microflora from podzols
was mostly composed of species which grew best in media poor in nutrients,
and that several fungus species produce more acid in poor than in rich media
(5). Uarova found bacteria in the rhizosphere of wheat plants, which could
decompose calcium phosphate, and which increased the water-soluble phos­
phorus in a compost (219).
Budin & Postgate have reviewed the sulphur cycle in nature, and have
pointed out the economic importance of organisms which produce actual
sulphur (28, 29). Quispel, Harmsen, & Otzen report on the oxidation of
pyrite in newly-reclaimed marine soils; only the second stage of the process,
the oxidation of sulphur to sulphate, is carried out by bacteria, but this
reaction stimulates the primary chemical oxidation of the sulphide to sulphur
(170). Oxidation of sulphur in Kansas soils has been studied by Moser &
Olsen (149).

THE BREAKDOWN OF INTRODUCED ORGANIC COMPOUNDS

There are few substances which are so insoluble, or so toxic, that soil
microorganisms cannot dispose of them. As is well known, even such un­
promising carbon sources as the straight-chain hydrocarbons can be broken
down by bacteria. Ladd (111) describes a Corynebacterium which oxidizes
such compounds, and Konovaltschikoff-Mazoyer & Senez (109) obtained
several hydrocarbon-decomposing pseudomonads from the oil-soaked earth
near the Marseilles refineries (111, 109). Levine & Krampitz found a Coryne­
bacterium which could oxidize acetone (121).
Arnaudi, Canonica, & Treccani have reviewed the whole subject of the
breakdown of hydrocarbons, and also of aromatic compounds (6). Treccani
et al. (218) and Murphy & Stone (150) studied the breakdown of naphthalene,
and Walker & Wiltshire (230) that of chloro and bromo-naphthalene, by
soil bacteria. Webley et al. found that Nocardia opaca breaks down the side
chain of phenyl-substituted fatty acids by beta-oxidation (237).
Many studies deal with the decomposition of the hormone herbicides
and related compounds. Audus (7) has published a series of papers on the
breakdown of 2,4-dichloro-phenoxyacetic and 4-chloro-2-methyl-phenoxya-
 136 THORNTON AND MEIKLEJOHN

cetic acids (better known as the weedkillers 2,4-D and MCPA). Jensen &
Petersen (99) describe two species that can break down 2,4-D, and Stapp &
Spicher isolated a new 2,4-D decomposer, Flavobacterium peregrinum (192).
Audus & Symonds (8) studied the kinetics of breakdown of 2,4-D by their
previously-isolated strain of Bacterium globiforme, and Walker & Newman
found that the same compound was attacked by a species which they tenta­
tively identify as a Mycoplana (231).
Steenson & Walker have isolated, from soil, a Flavobacterium t:Jat can
break down 2,4-D, an Achromobacter which attacks both 2,4-D and the re­
lated compound MCPA, and another Achromobacter which attacks para­
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chloro-phenoxyacetic acid (194). Rogoff & Reid (174) find that a Coryne­
bacterium can break down 2,4-D, and Jensen & Gundersen (98) describe an­
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other that decomposes aromatic nitro-compounds. Walker has measured the

breakdown of chlorophenols in soil by the percolation method (229).

INTERRELATIONS OF THE SOIL POPULATION

Thornton in his Leeuwenhoek lecture (216) has discussed the various
possible effects which the different groups of soil microorganisms may have
among and between themselves. It is of course clear that the relations be­
tween microorganisms in soil may be either mutually beneficial or harmful,
but comparatively little attention has been paid to the former aspect. The
process of dissimilation of a compound in soil is usually by stages so that an
organism that carries out :he initial stage may provide nourishment to dif­
ferent groups, but these food chains are usually complex, and their analysis
awaits knowledge of the chemical pathways along which the compounds
concerned are broken down (79, 194, 230). Some organisms bene.fit their
neighbours by synthesising growth substances such as vitamin Bl2 (27).
Most attention has been paid to the competition between microorganisms
in soil and this aspect has received increasing attention lately because of its
importance to the control of root pathogens. Most of these are fungi, hence
soil microbiologists have been concerned with the isolation and study of soil
organisms antagonistic to fungi. These include other fungi, actinomycetes
and bacteria. Morton & Stroube found that 3.5 per cent of the fungi, 1.7
per cent of the actinomycetes and 0.2 per cent of the bacteria isolated by
them from soil were antagonistic in agar cultures to Sclerotium rolfsii (148).
Luke & Connell found that 16 per cent of the fungi and 3.6 per cent of the
bacteria isolated by them from sugar cane soils were antagonistic to Pythium
(126). Soil bacteria producing antibiotics are relatively uncommon but are
of interest as being possibly easier to use as inoculants for biological con­
trol. Chinn described a pseudomonad, found to predominate on a sample of
wheat grain, that was strongly antibiotic to Helminthosporium and showed
considerable antibiotic antagonism to Fusarium and to a wide variety of
bacteria (36). Antibiotic fungi are more abundant in soil. Jeffreys et al. found
that of 65 fungal species isolated from sandy soils, about half produced an­
tibiotics, usually active against both bacteria and other fungi. About 45 per
 SOIL MICROBIOLOGY 137

cent of the species that were widespread or locally abundant antagonised

other fungi, but only 15 per cent of the rare fungi did so, suggesting some
selective advantage in antibiotic production. None of the ten species of
Phycomycetes showed such antagonism (92).
On platings of soil suspensions, antagonism of actinomycete colonies
towards nearby colonies of fungi is often noticeable so that the former group
has attracted particular attention as an tagonists to fungi (217). Thus StesseI,
Leben & Keitt sprayed platings of soil dilutions with suspensions of the
fungi Glomerula, Colletotrichum, Helminthosporium and Verticillum. Out of
some 70,000 colonies developing on the plates, 170 were antagonistic and, of
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these, 80 per cent were of actinomycetes (196). Fungi vary greatly in suscep­
tibility to actinomycete antibiotics and this specificity is found even amongst
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closely related strains. Buxton & Richards tested sixteen soil actinomycetes
for activity in vitro against eight pathogenic strains of Fusarium oxysporum.
Three of the former were inactive, nine inhibited all the Fusarium strains
equally, but four of the actinomycetes showed specific differences in degree
of inhibition according to strain of Fusarium, which they could be used to
distinguish (30). One of the actinomycetes that showed specific activity was
identified as Streptomyces albidoflavus, shown by Skinner also to be strongly
antagonistic to Fusarium culmorum (188). Antibiotics produced by actino­
mycetes are also active against some other actinomycetes. Peterson studied
the cross antagonisms amongst a collection of 46 actinomycetes, all of which
were active against Streptomyces scabies. They varied greatly both in the
number of the other strains that they would antagonise, and in the number
to which each was susceptible. These results show the need for careful selec­
tion of antagonistic actinomycetes resistant to the attack of other species,
if it is desired to establish them in soil to control a pathogen (161).
The potential usefulness of antibiotic-producing organisms for biological
control in soil depends not only on the feasibility of establishing them in
fresh soil, but also on their ability to produce antibiotics in effective con­
centration in field soil and on the activity and persistence of these antibiotics
in the soil. Even in sterilised and partially sterilised soil Grossbard (68) found
that Penicillium patulum, Aspergillus clavatus and Aspergillus terrens only
produced antibiotic in detectable amounts where available carbon sources
were added, while Gregory et al. found only traces of activity in soil cultures
of P. patulum (67). Clear evidence for the production of a specific antibiotic
in unamended soil was obtained by Gottlieb & Siminoff (65) in the case of
chloromycetin and by Wright for gliotoxin (247). But attempts to show this
with other antibiotics have generally been negative. Even if an antibiotic
is formed in soil a variety of environmental factors may limit its activity or
result in its rapid destruction. These factors have been studied in the case
of several antibiotics by Gottlieb et at. (64) and Hessayon (80), while Jeffreys
investigated the behaviour of 10 antibiotics in soil (91). The principal factors
causing inactivation appear to be (a) the adsorption of basic antibiotics by
the soil, (b) instability at the pH of the soil, (c) chemical reaction with some
 138 THORNTON AND MEILKE]OHN

soil component and (d) microbial decomposition. Such results have caused
the view to be expressed that antibiotic action is unlikely to be important
in soil. On the other hand failure to detect antibiotics in soil cultures of or­
ganisms known to be capable of their production may be due to a lack of
selectivity in the methods used for their detection, most of which have in­
volved extraction from the soil. Stevenson (198, 199) has developed a sensi­
tive method for detecting the production of antibiotics by cultures of actino­
mycetes in sterilised soil. Agar-coated microscope slides seeded with spores
of Helminthosporium were buried in the soil culture, which inhibited their
germination to varying degrees as compared with a sterile soil control. Evi­
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dence that this effect was in fact due to the actinomycete antibiotic was ob­
tained by studying the effect with pregerminated spores. Some of the actino­
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mycetes employed produced quite characteristic types of deformation of the

fungal hyphae in vitro, and these specific effects were also shown on the
hyphae from pregerminated spores buried in soil culture. Moreover the same
specific effects were produced by Streptomyces antibioticus and by the anti­
biotic actinomycin, which it produces, both in vitro and in soil.
Another important cause of antagonism between microorganisms in soil
is competition for some limiting nutrient which may be exerted whether or
not a competing organism produces an antibiotic. Skinner studied the growth
of Fusarium culmorum in the presence of Streptomyces albidoflavus which
produces an antibiotic very active against this fungus but one that is strongly
adsorbed by bentonite. In sand culture, the actinomycete could strongly in­
hibit the fungus, even preventing the germination of its spores. When ben­
tonite was added to the sand in excess, normal germination of the fungal
spores took place but growth of the fungal mycelium was still much reduced
by the actinomycete, and this Skinner attributed to nutrient competition.
He found that competition increased with the concentration of glucose sup­
plied (188, 189).
Antibiotic organisms may merely arrest growth of a susceptible organism
but some, such as the Myxobacteria (Noren) actually lyse and can thus feed
on the organisms attacked (153). Such lysis of fungal mycelium by actino­
mycetes has also been observed by Skinner (188). A dramatic example of
direct attack of one organism on another is that of fungi that catch and
destroy eelworms. In a survey of these fungi from 49 English soil samples,
Duddington found that the most abundant were Arthrobotrys dactycoides
and an unidentified species that would not form spores (51). Equally remark­
able is the amoeboid organism found by Weber, Zwillenberg & van der Laan
that attacks and digests nematodes (236).
Evidence is accumulating that fresh soil contains a fungistatic factor,
destroyed by heating, that inhibits the germination of spores of a number
of fungi. This has been found by Dobbs & Hinson (47), Chinn (35) and Jef­
freys & Hemming (93) while extracts of fresh peat have been found to be
strongly inhibitory to bacterial growth by Pochon & de Barjac (165).
Stover (203) and Sanford (184) have reported on the survival of differ-
 SOIL MICROBI OLOGY 139
ent plant-pathogenic fungi in soil, and Park (157) has found that alien species
of fungi introduced into soil do not withstand competition from the indige­
nous microflora as well as do species native to the soil. Cuthbert et al. report
on the survival of bacteria which are indicators of faecal pollution (38).
Vilas, Tejerina & Rubio put forward the interesting hypothesis that some
bacteria may be present in soil as filterable forms, perhaps less vulnerable
to antibiotic attack (222).
When the difficulties of establishing an antibiotic organism in soil, of
ensuring conditions therein for adequate antibiotic production, and of choos­
ing an organism whose antibiotic is active and persistent in soil are con­
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sidered, it is small wonder that attempts at biological control of root disease

have so far met with very limited success, though the number of positive
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results has been by no means negligible. This field has been well reviewed re­
cently by Wood & Tveit (246).
Since the root surroundings are the site at which biological control might
most likely be effective, more search for antagonistic organisms in the rhizo­
sphere would seem worth while. This is the more so since several antibiotics
are known to be taken up by the roots wherein they remain active and may
be protected from the hazards to which they are exposed in the soil (168,
201).
INTERACTIONS OF PLANTS WITH THE MICROFLORA
THE RHIZOSPHERE

The micropopulation of the rhizosphere has continued to attract well­

deserved attention. The rhizosphere effect can be particularly well studied
in soils poor in organic matter, where the population of the control soil is
sparse. Sand dunes in course of reclamation, for instance, show a gradual
increase in numbers of microorganisms; Milosevic (145) has shown this for
dunes on the coast of Yugoslavia, and Webley et al. (238) showed that the
plants colonizing the partly reclaimed dunes on the Scottish coast had, in
their rhizospheres, very much larger numbers of microorganisms than were
found in the surrounding sand. It was known from early work that numbers
of organisms in soil fall off rapidly with distance from the root; some data on
this point have been provided by Glathe et al., who buried Cholodny slides
among and near the roots of growing plants (60). The validity of the qualita­
tive differences in bacteria claimed to exist as between rhizosphere and
control soil were questioned by Wallace & King as a result of a study of
cereal plots (232). This gave rise to a paper by Lochhead & Rouatt (124) who
criticised the taking of the control samples by Wallace & King and gave an
interesting summary of data from a considerable number of experiments
showing qualitative differences between rhizospheres and control soil, in
the percentage of bacteria requiring amino acids.
Compounds secreted by the roots of plants must obviously have a very
marked influence on the rhizosphere. Samtsevich found the highest numbers
of organisms in tree rhizospheres during the autumn, and suggests that root
 140 THORNTON AND MEIKLEJOHN
secretions may be most abundant at this time (183). Kerr found that some
roots secrete a substance stimulating the growth of fungi (104). Good prog­
ress in the study of the nature of the compounds secreted by roots is reported
by Katznelson, Rouatt & Payne (103) and by Rovira ( 1 78). The former au­
thors found that drying pla::1ts to wilting point and remoistening greatly in­
creased the secretion of amino acids, and enabled that of reducing substances
to be detected. They suggested that alternate drying and wetting of soil
may produce a similar and possibly important effect in the field (103). The
presence of growth factors in the rhizosphere can also be due to their syn­
thesis by microorganisms, as is shown by the work of Lochhead and his col­
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leagues referred to above (27). The specific effects on the microflora of liv­
ing roots in contrast to dead plant material is shown in a paper by Rouatt &
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Lochhead, who found higher percentages of bacteria requiring amino acids

in the rhizospheres of wheat, oats, flax, timothy, red clover and lucerne, than
in the control soil. When materials from the same plants were added to and
allowed to decompose in the soil, no important changes in the proportions of
different nutritional groups of the soil bacteria could be detected by the
same technique, with the i::lteresting exception of lucerne. The addition of
lucerne increased the proportion of bacteria requiring B12• known to be pro­
duced by Rhizobium meliloti in exceptionally large amounts (27, 177).

RHIZOBIUM

The wide and varied field covered by studies of legume nodules and of
Rhizobium has been the subject of review by Wilson & Burris (245), Thorn­
ton (215), Allen & Baldwin (2), Virtanen (225), and Nutman (154), the last
dealing more particularly with the relation of host plant physiology and
genetics to infection and nodule behaviour. It is not therefore proposed to
attempt any cover of this field in the present review. But one aspect of it
has come into prominence recently and may be briefly discussed, because of
its bearing on the ecology of microorganisms in soil. This is the competition
between strains of Rhizobium in the relation to the establishment of a culture
used for inoculation. The practical importance of this depends on the ex­
istence of areas where local strains of Rhizobium that are ineffective on the
crop that is to be sown, are prevalent in the soil.
Among clover nodule bacteria there is a tendency for strains isolated
from subterranean ( Trifolium subterraneum) crimson ( T. incarnatum) or
cluster ( T. glomerulum) to be ineffective on white clover T. repens and vice
versa [Baird (10), Vincent (223)]. One cause of the prevalence of strains
ineffective on the crop to be sown may thus be the natural prevalence or
frequent cultivation of other clovers on which these strains are effective.
Thus Vincent found that in the Lismore region of New South Wales, where
T. repens is the commonest species, nearly all the strains of Rhizobium tested
were ineffective on T. subterraneum and on T. incarnatum (223). It may,
therefore, be necessary to introduce an effective strain where it is desired
to sow a crop variety on land in which the predominant strains are ineffec-
 SOIL MICROBI OLOGY 141
tive, and this must be done in competition with the strains already existing
in the soil. It is known that strains of Rhizobium differ markedly in the ability
to compete with each other for growth and nodule formation in the host.
In choosing a strain for use as an inoculant it may be necessary to select one
not only effective on the crop but dominant in establishing itself in the crop
in competition with the strains already in the soil. The study of strain estab­
lishment has been facilitated by extensive surveys that have been made of
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the antigen relationships of clover nodule bacteria. The use of serologically

identifiable strains of Rhizobium has enabled the percentages of nodules pro­
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duced by each of a mixture of strains or by the inoculant strain in field

trials, to be determined. Read, using this method in field trials distributed
over Great Britain, found that strains used to inoculate T. pratense differed
greatly in the percentage of the total nodules that each produced in the crop
and that the most successful strains in this respect differed with the locality
(171). Vincent and his colleagues, using single strains and mixtures of them
as inocula, also found that strains differed markedly in the percentages of
the nodules that each produced, and also in their effect on crop growth. [see
Vincent & Waters (224), Jenkins, Vincent & Waters (94) and Baird (10)].
The factors involved in competition for nodule formation are complex.
They involve some, inherent in the host plant and the bacterial strain, that
influence the process of infection. These are discussed by Nutman (154).
Strains of Rhizobium also differ in ability to compete with each other outside
the root and are variously affected by other components of the soil micro­
population. These include antagonistic organisms [Hely et al., (75)], but
Harris also found organisms in the rhizosphere which increased nodule num­
bers produced by a strain of clover Rhizobium in in vitro culture (72). These
environmental factors will influence the proportions of different strains in
the rhizosphere, and hence the chances of infection of each strain. Plants
can receive sufficient effective nodulation by an effective strain even when
also bearing ineffective nodules, as was shown by Burton, Allen & Berger
with Phaseolus (26). On the other hand, Harris, in pot experiments in
sterilised soil and sand, found considerable competition between effective
and ineffective strains as judged by growth of the plants (73). The relative
numbers of effective and ineffective nodules produced by competing strains
is probably of importance beyond some limiting ratio, which may differ with
the type of nodulation of each strain and under different conditions. I t should
be remembered that the number of cells of Rhizobium introduced by seed
inoculation may be small compared with those in the soil, so that, when the
latter are ineffective, a competitive inoculant strain may be needed to ensure
a sufficient percentage of effective nodules.
 142 THORNTON AND MEIKLEJOHN

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