Advances in Microbiology, 2013, 3, 343-349
http://dx.doi.org/10.4236/aim.2013.34048 Published Online August 2013 (http://www.scirp.org/journal/aim)
Dinamic of Bacteria Desnitrificants and Nitrificants
in the Rizospheric of Wheat with Slow Release of
Fertilizer, Irrigated with Waste or Well Water
Sandra Grisell Mora-Ravelo1*, Francisco Gavi Reyes2, Jesús Pérez Moreno3,
Juan José Peña Cabriales2, Leonardo Tijerina Chávez4, Ma. de Lourdes de la Isla de Bauer2
1Posgrado en Biología, Instituto Tecnológico de Ciudad Victoria, Ciudad Victoria, México
2Programa de Hidrociencias, Colegio de Posgraduados, Montecillo, México
3Programa de Edafología, Colegio de Posgraduados, Montecillo, México
4Departamento de Biotecnología, CINVESTAV, Irapuato, México
Received May 30, 2013; revised June 30, 2013; accepted July 10, 2013
Copyright © 2013 Sandra Grisell Mora-Ravelo et al. This is an open access article distributed under the Creative Commons Attribu-
tion License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
ABSTRACT
The study of the paper about the rhizosphere in the transformation of nitrogen compounds can generate knowledge of
the microbial and biochemical atmosphere of the rhizosphere of wheat, for the understanding of the dynamics of the N
in agricultural zones, with the purpose of optimizing the fertilizer use and increasing the productivity of the cultures.
Therefore, the objective of the present work was to know the effect the rhizosphere in the dynamics of the bacterial
populations that take part in the cycle of the N in wheat nourished with slow release fertilizer and one commercial, irri-
gated with waste water or well. Analyses in the soil took place vertisol used in the experiment with the rhizospheric and
non rhizospheric fraction. The slow release fertilizer used has a matrix enriched with N and P and is in the process of
being patented (it explains in materials and methods). Each fertilizer was evaluated and the combination of the slow
release fertilizer with organic fertilizer. The technique of the number most probable was used (MNP) to carry out the
quantification of the nitrificants and denitrificants bacteria to the 55, 67 and 97 days after sowing (Dds). The results
obtained for the MNP of denitrificants bacteria and Nitrosomonas indicate that the effect average of the types of water,
soil and fertilizers, as well as their interaction to each other was not significant (p > 0.05). The effect of the fertilizing
type and soil (rhizospheric and non rhizospheric) in the MNP of Nitrobacter was significant (p < 0.05). The tendencies
show that the non rhizospheric soil is more favorable for the development of denitrificants bacteria and Nitrobacter,
whereas the MNP of Nitrosomonas was greater in rhizospheric soil.
Keywords: Nitrificants; Vermicompost; Nitrites; Nitrates; Ammonium
1. Introduction
The rhizosphere constitutes the surface and the immedi-
ate region the root surrounds, that provides with an eco-
logical niche to the microorganisms of the soil since in
her the nutriments are more available. The atmosphere
rhizospheric is a scene integrated by the interaction soil,
plants and organisms. Between these the bacteria and
fungi are in greater density in the rhizosphere than that in
the soil without roots [1]. The interactions between the
microorganisms and the roots determine the rhizosphere
effect, on same populations and the activity of the mi-
croorganisms on the availability of the nutriments for the
plants [2,3].
In nitrificants bacteria, rhizospheric are developed (Ni-
trobacter and Nitrosomonas); and denitrificants bacteria
(Brasilense Azospirillum, Bacillus azotoformas, thioba-
cillus desnitrificans, Pseudomonas, etc.), those alto-
gether play an important role inside of the cycle of the N.
The nitrificants bacteria they are of quimiotrofic me-
tabolism and the oxidation of the 4 to 2
NH NO

, it
serves like power plant as these microorganisms whereas
the Corg they obtain it from the fixation of the CO2, of the
air or the atmosphere of the soil. The growth of these
bacteria is smaller than the growth of the majority of the
*Corresponding author.
C
opyright © 2013 SciRes. AiM

S. G. MORA-RAVELO ET AL. 344
bacteria of the soil that are of quimiotrofic metabolism
[4,5].
Within the microorganisms, the bacteria constitute the
only group that has the physiological characteristic to
cause the denitrification. All the bacteria denitrificants
are anaerobic, with the exception of the species of the
sort Propionibacterium that fermenters anaerobic they
are forced that is able to carry out the denitrification.
Most of the denitrificants bacteria they are of quimio-
trofic metabolism since they use carbohydrates, organic
acids and diverse organic compounds like C and power
plant during their anaerobic cycle in the presence of di-
verse oxides of N [6].
The activity, diversity and structure of these microor-
ganisms are sensible to the changes in the edafic atmos-
phere caused by the carbon sources and energy, pressure,
ventilation and interaction between the microorganisms,
pH, humidity, temperature, content of oxygen and nutria-
ments available [7]. The most important factor is the
availability of nutriments because it promotes the activity
of the microorganisms in the rhizosphere, measurement
like rhizosphere phantom, which is of 2, 5 ground times
greater fertilized than in grounds non fertilized; also mic-
robiota measured with 14C is tripled when fertilizers are
applied.
2. Materials and Methods
This study was conducted in two phases. The first corre-
sponded to establishing a greenhouse test for generating
environments where microorganisms would study popu-
lations and the second consisted of determining the inci-
dence microbial laboratory. A haplic vertisol from Gua-
najuato, Mexico was used [8]. The physical and chemi-
cal properties of the studied soil and water are shown in
Tables 1 and 2. We used wheat (Triticum aestivum L.)
variety “Tlaxcala F2000” classified as having an inter-
mediate cycle and developed for natural rainfall condi-
tions by the INIFAP (Instituto Nacional de Investiga-
ciones Forestales, Agropecuarias y Pecuarias). This
wheat has an average cycle of 118 days, with a harvest-
ing interval from 107 to 135 days [9]. The applied fertili-
zers were: monoammonic phosphate plus urea termed a
“commercial fertilizer” (CF), a vermicompost termed
“organic fertilizer” (OF), and a slow release fertilizer
(SRF) called “GAPU” (constituted by a clay matrix en-
riched with 8.1 and 6.3% of N and P in weight, respec-
tively, in process to be patented). The treatments were
designed to evaluate the simple effect of each one of
these fertilizers and the combination of SRF plus OF.
Vermicompost (containing 1.37% and 0.75% of N and P,
respectively) was produced with residues of plants used
for gardening. Used waste and well waters came from
urban zones from Montecillo, Texcoco, Mexico. The
dose of fertilization of N and P used for the greenhouse
Table 1. Physical and chemical characteristics of the experi-
mental soil.
Variable Method Value Units
N MicroKjeldahl 0.07 %
Extractable P Olsen 34 mg kg−1
Organic matter Walkley and Black 1.4 %
CCI Extraction with
ammonium acetate 39 cmolc kg−1
pH (relation 2:1)Potentiometer 7.76
E.C. Conductimeter 0.69 dS m−1
Sand Bouyoucos 10 %
Lime 17 %
Clay 73 %
Textural class Clayish
E.C. = Electrical conductivity, CCI = Capacity of cationic interchange.
Table 2. Physical and chemical characteristics of the ex-
perimental water.
Variable Value Units
Waste water Well water
Total N 72 32.00 mg L−1
N-NO3 6 22.27 meq L−1
N-NH4 55 8.64 meq L−1
Soluble P-PO4 11 0.86 mg L−1
Total P 39 0.60 mg L−1
pH 7.05 7.45
E.C. 0.59 0.59 dS m−1
E.C. = Electrical conductivity.
experiment was greater than that recommended in the
studied area in eastern Mexico “Bajío Guanajuatense”
where the studied soil was collected. Following the re-
commendation of Terman, et al. (1962) [10] for green-
house experiments, the dose was equivalent to 360 and
257 kg of N and P per ha, respectively. All N and P were
applied at the time of sowing. The experimental units
(EU) consisted of cylindrical pots which contained 2 kg
of soil: without plants (designed to collect non rhizo-
spheric soil) and with three plants (from which the rhi-
zospheric soil was collected). The number of cylindrical
pots was calculated so that in every date of sampling
(55.67 and 97 days after sowing) three experimental units
by treatment were collected (Table 3).
In order to obtain the rhizospheric soil, the soil portion
used was that strongly adhered to the root. Ten grams
were weighed separately of rhizospheric and non rhizo-

S. G. MORA-RAVELO ET AL. 345
Table 3. Treatments in the experiment.
Number
of
treatment
Type
of
soil
Type of
fertilizer
Type of
water
Number
of
replicates
1 RS CF Waste water 3
2 RS CF Well water 3
3 NR CF Waste water 3
4 NR CF Well water 3
5 RS SRF Waste water 3
6 RS SRF Well water 3
7 NR SRF Waste water 3
8 NR SRF Well water 3
9 RS OF Waste water 3
10 RS OF Well water 3
11 NR OF Waste water 3
12 NR OF Well water 3
13 RS SRF + OF Waste water 3
14 RS SRF + OF Well water 3
15 NR SRF + OF Waste water 3
16 NR SRF + OF Well water 3
17 RS C Waste water 3
18 RS C Well water 3
19 NR C Waste water 3
20 NR C Well water 3
Total
units
number
of experimental 240 Unit
SR = Rhizospheric soil, NR = Non rhizospheric soil; CF = Commercial
fertilizer, SRF = Slow release fertilizer, OF = Organic fertilizer (vermicom-
post), C = Control.
spheric soil. Each of these samples was added to 90 mL
of Ringer solution. In the determination of the microbial
incidence, the technique of the most probable number
(MPN) was used for the quantification of nitrificant and
denitrificant bacteria [11]. Selective growth media for the
fractions of the rhizospheric and non rhizosphereic soil
were used. A series of ten dilutions was used to inoculate
five tubes with each level of dilution (10−8 to 10−5). The
cultures were incubated to 28˚C during 7 and 21 days for
the denitrificant and nitrificant bacteria, respectively and
their presence was identified by using specific diagnostic
tests. (CaCO3) NH4 was used for Nitrosomonas, (CaCO3)
NO2 for Nitrobacter and of Griess-Ilosvay reagent for
both groups [12].
3. Results
The experimental design did not allow statistical eva-
luation of sampling interaction with the other factors
evaluated: type of water, fertilizers and soil type (vs. rhi-
zosphere. Rhizospheric not) for any of the populations of
bacteria quantified. Figure 1 shows the temporal changes
of the populations of denitrificant bacteria of non
rhizospheric soil in relation to plant age with waste water
and well water. In general terms, there was an increase in
denitrificant bacteria populations, when the plan age in-
creased, indepently of type of water. The average effect
of the types of water, soil and fertilizers (as well as their
interactions between them) was not significant (p > 0.05)
on the development of the denitrificant bacteria popula-
tions, evaluated MPN. In general terms, The populations
denitrificant were higher in non rhizospheric in relation
to those found in rhizospheric soil, independently of the
type de water. In average, denitrificant from non rhizo-
spheric soil populations were higher in well water than in
waste water. Mean while, the opposite trend was obser-
ved in rhizospheric soil (Table 4).
(a)
(b)
Figure 1. MPN of denitrificant bacteri a in non-rhizospheric
soil irrigated with (a) waste water or (b) well water. CF =
Commercial fertilizer, SRF = Slow release fertilizer, OF =
Organic fertilizer (vermicompost), C = Control. Vertical
lines show 95% confidence intervals.

S. G. MORA-RAVELO ET AL. 346
In relation to fertilizers, the highest populations of de-
nitrificant bacteria were observed in Fertilizer slow re-
lease and the lowest ones were recorded in Commercial
Fertilizer (Table 5).
Pointed out that plant organic compounds can be used
as a source of nutrients energy to desnitrificants bacteria.
Also it is inferred, that the waste water can contain in its
M. O factors of growth for same the bacteria; neverthe-
less the toxic elements can predominate in their negative
effect that limits the increase of the bacterial population
[13]. It was observed (Table 5) that when SRF was ap-
plied there is minor proliferation of denitrificants bacteria,
compared with the witness and the application of other
fertilizers (OF and CF) and his combinations. This can
indicate that the N of the SRF is less susceptible to lose
itself by denitrification.
Figure 2 shows the temporal changes of the populations
of Nitrobacter bacteria of non rhizospheric soil in rela-
tion to plant age with waste water and well water. In
general terms, there was an increase in denitrificant bac-
teria populations, when the plan age increased, inde-
pently of type of water.
The average effect of the types of water, soil and fer-
tilizers (as well as their interactions between them) was
not significant (p > 0.05) on the development of the Ni-
trobacter bacteria populations, evaluated MPN. In gen-
eral terms, the populations Nitrobacter were higher in
non rhizospheric in relation to those found in rhizo-
Table 4. Average of MPN of denitrificant bacteria in two
types of water and soil during three samplings.
Type of water Rhizospheric
soil
Non rhizospheric
soil Average
Waste water 0.65 × 105 0.82 × 105 0.73 × 105
Well water 0.26 × 105 7.3 × 105 3.7 × 105
Average 0.45 × 105 4.1 × 105
Table 5. Average of the MPN of denitrificant bacteria in
rhizospheric soil and non rhizospheric soil with addition of
three types of fertilizer.
Fertilizer Rhizospheric soil Non rhizospheric
soil Average
CF 6.5 × 105 8.3 × 105 7.4 × 105
C 5.4 × 105 6.4 × 105 5.9 × 105
OF 0.31 × 105 0.83 × 105 0.57 × 105
SRF + OF 0.27 × 105 0.37 × 105 0.32 × 105
SRF 0.11 × 105 0.11 × 105 0.11 × 105
Average 2.52 × 105 3.2 × 105
CF = Commercial fertilizer, SRF = Slow release fertilizer, OF = Organic
fertilizer (vermicompost), C = Control.
(a)
(b)
Figure 2. MPN of Nitrobacter in non-rhizospheric soil irri-
gated with (a) waste water or (b) well water. CF = Com-
mercial fertilizer, SRF = Slow release fertilizer, OF = Or-
ganic fertilizer (vermicompost), C = Control. Vertical lines
show 95% confidence intervals.
spheric soil, independently of the type de water. In aver-
age, Nitrobacter from non rhizospheric soil populations
were higher in well water than in waste water. Mean
while, the opposite trend was observed in rhizospheric
soil (Table 6).
In relation to fertilizers, the highest populations of Ni-
trobacter bacteria were observed in Fertilizer slow re-
lease and the lowest ones were recorded in Commercial
Fertilizer (Table 7). Figure 3 shows the temporal
changes of the Nitrosomonas populations of bacteria of
non rhizospheric soil in relation to plant age with waste
water and well water. In general terms, there was an in-
crease in Nitrosomonas bacteria populations, when the
plan age increased, indepently of type of water (Table 8).
In Table 9, it was observed that the fertilizers that
promote the MNP of Nitrobacter are the SRF and the CF.
The most probable number of the denitrificants bacteria
is greater than in Nitrobacter and Nitrosomonas as it in-
dicates [14] that indicates for example the root of wheat
has a strong effect on the microbial populations within

S. G. MORA-RAVELO ET AL. 347
Table 6. Average of MPN of Nitrobacter in two types of wa-
ter and soil during three samplings.
Type of water Rhizospheric
soil
Non rhizospheric
soil Average
Waste water 7.2 × 105 10 × 105 8.6 × 105
Well water 3.5 × 105 2.6 × 105 3.1 × 105
Average 5.3 × 105 6.3 × 105
Table 7. Average of the MPN of Nitrobacter in rhizospheric
soil and non rhizospheric soil with addition of three types of
fertilizer.
Fertilizer Rhizospheric
soil
Non rhizospheric
soil Average
CF 12 × 105 1.3 × 105 6.7 × 105
C 9.2 × 105 6.3 × 105 7.7 × 105
SRF 1.9 × 105 0.9 × 105 1.4 × 105
SRF + OF 1.9 × 105 5.2 × 105 3.5 × 105
OF 1.1 × 105 6.4 × 105 3.7 × 105
Average 5.2 × 105 4.0 × 105
CF = Commercial fertilizer, SRF = Slow release fertilizer, OF = Organic
fertilizer (vermicompost), C = Control.
(a)
(b)
Figure 3. MPN of Nitrosomonas in non- rhizospheric soil
irrigated wi th (a) waste w ater or (b) well water. CF = Com-
mercial fertilizer, SRF = Slow release fertilizer, OF = Or-
ganic fertilizer (vermicompost), C = Control. Vertical lines
show 95% confidence intervals.
which denitrificant emphasizes the high number of bac-
teria.
4. Discussion
In this experiment, we possibly suppose that there was no
an independently marked rhizospheric effect of the type
of fertilizer and used water, had to that the sampled
rhizospheric zone was not the adapted one, due to the
space so reduced in that were the wheat plants. However,
the MNP of the bacteria studied in this work was not
affected by the zone by the roots nor by the fertilization
with N as it concludes [1,2,15]; which they investigated
that the composition of the community of bacteria in the
rhizosphere is affected by the complex interaction be-
tween the type of soil, species of plants location of the
zone by the roots and the nitrogen fertilization. Appar-
ently, there was no a marked rhizospheric effect on Ni-
trosomonas (Table 9), because the existing potential in
this zone to carry out the liberation of the 4
NH

, consti-
tutes necessary the power provision for the development
of this sort of nitrificants bacteria [16]. Contrary to the
referred thing by [17] on the inhibiting effect caused by
the organic compound presence on the development of
the nitrificantes populations, it was verified in the present
investigation that in the rhizosphere, in which a great
abundance of organic compounds exists, these popula-
tions were stimulated (Tables 6 and 7), which agrees
with the results obtained by [18], for the rhizosphere of
Table 8. Average of MPN of Nitrosomonas in two types of
water and soil during three samplings.
Type of waterRhizospheric
soil
Non rhizospheric
soil Average
Well water 6.1 × 105 3.1 × 105 4.6 × 105
Waste water 2.2 × 105 2.3 × 105 2.3 × 105
Average 4.1 × 105 2.7 × 105
Table 9. Average of the MPN of Nitrosomonas in rhizosphe-
ric soil and non rhizospheric soil with addition of three ty-
pes of fertilizer.
Fertilizar Rhizospheric
soil
Non rhizospheric
soil Average
CF 9.3 × 105 3.0 × 105 6.2 × 105
C 4.8 × 105 4.1 × 105 4.5 × 105
OF 3.1 × 105 2.2 × 105 2.7 × 105
SRF + OF2.1 × 105 2.8 × 105 2.5 × 105
SRF 1.6 × 105 1.7 × 105 1.7 × 105
Average 4.2 × 105 2.8 × 105
CF = Commercial fertilizer, SRF = Slow release fertilizer, OF = Organic
fertilizer (vermicompost), C = Control.

S. G. MORA-RAVELO ET AL. 348
some plants. However, the magnitude of the development
shown by the nitrificants bacteria in the rhizosphere of
wheat, and with its development in the fraction of the
rhizospheric soil (Figure 2), it suggests in her takes place
an effective process of nitrification [19]. Woldendorp
and Laanbroek (1989) [20] reported that the rate of nitri-
fication is a predominant process in the rhizosphere,
which can lead to a considerable production of 3 NO

in
this zone. However, it was difficult to make a real esti-
mation of the rate from production of 2
in the rhizo-
sphere, which can lead to a considerable production of
3 in that zone, since in her great part of the N avail-
able is directed towards immobilization and the absorp-
tion by the roots. The denitrificants bacteria also were
stimulated in greater number of cells as much in the
rhizosphere of the ground as in the non rhizospheric soil
the population increase can be in favor certain not only
of the great present availability of composed of carbon;
but also by the exudate production in the rhizosphere,
which can lead to a considerable production of 3
NO 
NO 
NO

on
the part of the nitrificants bacteria, since he himself ion is
used by the denitrificants bacteria like electron acceptor
before the reduced present oxygen concentration in the
rhizosphere [21]. The number of cells or MNP was ob-
tained in Nitrobacter and Nitrosomonas was greater to
which this is reported generally can be viable since al-
though the conditions in which work was of anaerobiosis
the sort of the Nitrobacter can grow occasionally under
anaerobic atmosphere breathing where the M. O. is min-
eralized [4,22,23]. Kowalchuk and Stephen, (2001) [4],
emphasized that when the technique of the MNP is used
the value of the Nitrosomonas underestimates low values
of the real number of cells caused by factors as pH and
the provision of N. Also, Watson [24] reported that the
count of Nitrobacter is influenced by pH. Although in
our case we discarded that pH has been the factor that I
influence in the number of cells that we reported for
these sorts. We agree with reported by Rice and Pan-
choly [25] who emphasize that the MNP can be a ques-
tionable procedure of count, this is important if they are
possible to be seen that they exist alternative in the inter-
pretation of the changes of and 3 in the soil.
The low concentrations of 3 can be the result of the
best efficiency in the conduction of these and the in-
crease of the 4 can be due to the increase of N in
the soil. A low concentration of 3 can as resulting
from happen in an actively nitrificant habitat the denitri-
fication or by the fast conduction towards the plants as it
indicates Allison and Prosser [26]. On the other hand,
also it can be that the efficiency of the method of the
MNP low is compared with other methods possibly this
must to the selectivity of means of used growth and to
the presence of added cells to the dissolutions as they
indicate [27]. However, the MNP of Nitrobacter and
4
NO 
NH
NH
NO 
NH 
NO 
Nitrosomonas of these sorts suggest both processes
(4

2 NO

and 2 NO

3) respectively are similar
so that both steps produce different amounts from energy.
From the uncertainty of the method of the MNP diverse
mechanisms exist that can explain this:
NO
3
NO
1) Nitrosomonas it has a greater mortality than the Ni-
trobacter. This happens particularly in soils where this
sort (Nitrosomonas) is died by the acid production [27,
28].
2) Heterotrofic development of Nitrobacter species
[29].
3) Anaerobic growth of Nitrobacter through

and organic substrat [30].
4) Denitrificants relation / between Nitro-
bacter and bacteria [31]. 2
NO
3
NO
NH
5. Conclusions
1) The effects of the types of water, fertilizer and ground
the MNP of denitrificants bacteria and those affected in
form differential that take part in the transformation of
4

to 3

(Nitrobacter and Nitrosomonas). NO
2) The MNP of the denitrificants bacteria was not af-
fected by the types of fertilizer, soil and water of irriga
tion.
3) The MNP of Nitrobacter was promoted positively
by the type of soil and fertilizer in average. Nitrobacter
was developed better in the non rhizospheric soil. This
sort of bacteria was stimulated by the OF and the combi-
nation of SRF + OF. The waste water did not have an
effect in the MNP of this group of bacteria compared
with the well water.
4) The MNP of Nitrosomonas. It was affected only by
the type of soil. This sort of bacteria have better devel-
opment in the rhizospheric soil.
6. Acknowledgments
This study was financed by project CONACYT 38999.
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