Soil Microbial Activity and its Relation to Soil Indigenous Properties in
Semi-arid Alluvial and Estuarine Soils of Mahi River Basin, Western India
Several studies on the continental Quaternary sedimentation, stratigraphy and landscape evolution of the Mahi River basin exist, however, the microbial activity including its relation with soil physical and chemical properties has not been explored. In the present investigation, estuarine and alluvial soil microbial activity (as an index of soil enzymes i.e., dehydrogenase and protease) and its relation with soil properties such as Soil Organic Matter (SOM), Soil Moisture Content (SMC), soil texture (sand, silt and clay) and soil pH has been addressed. The study was conducted at 7 sites spread over 3 locations (2 were from alluvial zone and 1 was from estuarine zone), each sampled at various depths along a 30 km long stretch of the Mahi River in western India. High microbial activity was noticed in estuarine soils than in alluvial soils. Dehydrogenase activity in both alluvial and estuarine soils indicated positive correlations with SOM, SMC and a moderate correlation with clay content. On the contrary, the protease activity showed poor correlation with SOM, SMC and clay content of alluvial soils however, significant positive correlations were noticed in estuarine soils. No correlation was observed between these two enzymes. A negative correlation existed between soil depth and both the enzymes in alluvial soils. The findings demonstrate that SOM and SMC, clay content and soil depth are the important determinants for dehydrogenase activity (indicative of organic matter transformation) in both alluvial and estuarine soils, whereas the soil depth is the lone determinant for protease in alluvial soils and its correlation with other properties in estuarine soils is site specific.
Received: February 22, 2011;
Accepted: March 21, 2011;
Published: July 12, 2011
Microbiology of the floodplains has received a lot of attention (Baldwin
and Mitcheel, 2000; Gergel et al., 2002;
Kang and Stanley, 2005). Microbial activity in floodplains
can control the ecosystem and metabolism of rivers (Fischer
and Pusch, 2001; Fischer et al., 2003) and
is significantly influenced by variability in hydrologic regimes, flow dynamics,
sediment movement (Baldwin and Mitcheel, 2000; Fischer
et al., 2003) and chemical pollutants (Onweremadu
and Nwufo, 2009). Investigations on the sediments of river channels have
shown that microbial activity is controlled by sediment structure, hydraulic
conditions and availability of organic carbon and nitrogen (Fischer
et al., 2005). Although microbial activity of river channels, streams,
sediments and hyporheic zone are well studied, microbial activity of the semiarid
alluvial plains is not yet established.
Soil enzymes are considered to be indicative measures of soil fertility (Zahir
et al., 2001). Soil enzymes derived primarily from soil microbes
are important due to the fact that they participate in elemental cycling and
decomposition of organic residues and are considered fundamentally good indicators
for soil quality (Abdalla and Langer, 2009; Kizilkaya
et al., 2007; Venkatesan and Senthurpandian,
2006; Caldwell, 2005). Dehydrogenase is one such
enzyme indicative of overall biological and microbial activity of soils (Quilchano
and Maranon, 2002) because it is associated with living cells and is linked
with microbial oxidoreduction processes (Alef and Nannipieri,
1995; Stepniewska et al., 2007) which are
important for organic matter degradation and transformation. Dehydrogenase activity
in soils is very sensitive to various natural and anthropogenic factors like
soil aggregation, soil aeration status (Brzezinska et
al., 2001), organic content (Gajananda, 2007;
Tirol-Padre et al., 2006) devegetation (Bastida
et al., 2006), agricultural management (Truu
et al., 2008), addition of pesticides (Stepniewska
et al., 2007), insecticides (Singh and Kumar,
2008) and heavy metal combined pollution (Gao et
al., 2010). Soil proteases are extra-cellular enzymes produced mainly
by bacteria which degrade proteins, release NH4-N and are very important
in nitrogen cycle (Sardans et al., 2008). Initial
breakdown of proteins from the Soil Organic Matter (SOM) is virtually mediated
by soil proteases. Estimation of proteases provides information on nitrogen
mediated biochemical processes in the soil (Sardans and
Mahi River originates near Moripara in Dhar district of Madhya Pradesh and
flows through the Precambrian Aravalli mountain range and the vast Gujarat alluvial
plains and merges in the Gulf of Cambay. The Mahi River basin falls under semiarid
climatic zone, a major climatic zone of India comprising 37% of the total geographical
area of the country and the alluvial soils are under intense weathering as well
as erosion which are significant processes in landscape evolution. In earlier
studies, the Mahi river basin has been investigated for understanding Quaternary
environmental and tectonic changes and their implications on the fluvial systems
and landscape of the dry lands of Gujarat (Chamyal et
al., 2003; Maurya et al., 2000). The
significance of the exposed sedimentary records in the cliffy banks of the Mahi
River is realized and used for reconstruction of Quaternary continental stratigraphy
and understanding the geomorphic evolution of the Mahi River basin (Sridhar,
2007; Chamyal et al., 2003; Juyal
et al., 2000). Since microbial activity is linked with several ecosystem
processes including soil formation, weathering and organic matter transformation,
it is important to understand the factors that control microbial distribution
and activities in alluvial soils. Realizing this, the present study was initiated
to investigate microbial parameters and their critical decisive determinants
in the soils of alluvial plains of Mahi River in western India.
MATERIALS AND METHODS
Study site description and sample collection: The sites studied are
located in the semi arid Mahi River basin, Western India (Fig.
1), with mean annual rainfall about 600 to 650 mm spanning three locations
Rayka, Dodka and Mujpur. The alluvial zone of the Mahi River basin at Rayka
(22° 26 56.59N, 73° 05 16.95E) comprises of
distinct geomorphic units and alluvial deposits of Pleistocene and Holocene
age (Juyal et al., 2000; Chamyal
et al., 2003; Maurya et al., 2000;
Rachna et al., 1998). River channel on the convex
banks is bordered by cliffs rising about 30-40 m from the river level (Juyal
et al., 2000).
||Location map of the study area showing the study sites and
generalised geomorphic and climatic zones. (a) Distribution of dry lands
in India. (b) Major climatic zones and rivers of Gujarat and (c) Geomorphic
zones in the Mahi River basin (after Rachna et al.,
1998). Sites sampled are marked with filled circles
The sediment and soil sequences along these cliffs have been dated back to
125 ka (Juyal et al., 2000). At Rayka, the sediments
comprising these cliffs are deeply incised inland forming ravines exposing sediment
sequences. The alluvial zone of the Mahi River basin at Dodka (22° 28
54.0N, 73° 06 5.67E) lies up stream of Rayka. The sediment
sequence at Dodka is capped by aeolian deposits which show intense weathering.
Significant soil erosion is also observed in Dodka section. In both Dodka and
Rayka, landscape is covered with Calotrophis procera, Zyzyphus nummulariea,
Acasia and grasses like Heterophogan, Setaria sp., Cymbopogon
sp., Digitaria sp. and Brachiaria sp. Mujpur section
lies in the estuarine zone located downstream of Rayka and is made up of sediments
of mid to late Holocene forming a younger terraced surface.
A total of 33 triplicate composite samples at an interval of 25 cm from the three exposed sections at Dodka, Rayka and Mujpur were collected for the present study. Due to lot of heterogeneity at alluvial sites and varied stratigraphy, more number of samples (twenty seven) were collected from alluvial zone. However, only six samples were collected from the estuarine zone of Mahi River basin because of low heterogeneity. All the sites selected were unexposed to anthropogenic activities. Prior to the collection of soil samples, the sites were cleaned by scraping the surface layer. Due to difference in geomorphic settings, at Rayka 5 different sites (each harbouring distinct soil sequences) such as Rayka Ravine soil (RR), Rayka Ravine Red soil (RRR), Rayka aeolian soil (RW), Rayka Surface soil (RS) and Rayka surface Red soil (RD) were selected and a total of 22 samples were collected. These 5 sites represent the overall soil sequences developed over river borne sediments along the bank of Mahi River at Rayka. Eleven samples were collected from 3 sites (RR, RRR and RW) at the Rayka section exposed along the Mahi River bank and remaining eleven samples were collected from other 2 sites (RS and RD) at a section exposed landward in a deeply incised ravine. Five samples were collected from Dodka section (D) and six samples from Mujpur (M) located in the estuarine zone of Mahi River. Due to distinct stratified soil successions that occurred in the exposed sites and the different thickness of the soil profiles, the material was available at different depths, therefore the gradient in depth was not same for all the samples. For example, at RW site, which is a soil profile developed over wind-borne material of above 75 cm thickness, the samples were collected up to a depth of 75 cm. Same case was observed in RRR but here the profile has been developed over a river-borne sediment layer measuring 125 cm. No distinct pedon was noticed below the 125 cm (D5) in the Dodka site which was comprised of loose fluvial sediments. Autoclaved polyethylene bags were used for sampling which were immediately kept on ice packs before being transported to the lab. All the samples were sieved (<4 mm), cleaned of visible roots and plant residues and stored at 4°C.
Determination of soil parameters: Soil samples were analysed for soil
moisture content, pH, soil texture according to the standard protocols (Alef
and Nannipieri, 1995). Soil Organic Matter (SOM) was determined by dichromate
digestion method (Walkley and Black, 1934). All the determinations
were performed in triplicate and values reported are mean with standard deviation.
Determination of soil enzymes: Dehydrogenase activity in soils was measured
by following the reduction of 2,3,5-Triphenylotetrazolium Chloride (TTC) as
an artificial electron acceptor to red-coloured formazons which were extracted
and determined colorimetrically (Alef and Nannipieri, 1995).
The amount of Triphenyl Formazan (TPF) extracted was calculated by reference
to a calibration graph prepared from TPF standards.The dehydrogenase activity
is expressed as μg of TPF g-1 24 h-1 oven dried soil.
Protease activity was determined by using the method given by Ladd
and Butler (1972) with sodium caseinate as a substrate.
Statistical analyses: The results obtained were examined statistically for linear regression and Pearson product moment correlations by Origin 6.0 statistical software (Microcal Software, Inc). For identification of meaningful variables in the studied samples Principle Component Analysis (PCA) was carried out by using XLSTAT version 2009.6.01 (trade mark of Adinosoft).
Soil parameters: Characteristics of soil samples taken from 3 locations are summarized in Table 1. All the 33 soil samples were neutral to slight alkaline in nature with a pH ranging from 6 to 7.6. Mujpur soils were characterised by a high content of Soil Organic Matter (SOM), Soil Moisture Content (SMC) and clay (%) in comparison to the other two sites (Table 1). This may be due to geographical location of Mujpur section which is near the estuarine zone of Gulf of cambay where frequent back waters inundate during high tides.
Soil enzymes and their correlation to soil parameters: Dehydrogenase
and protease activities of the 3 locations (Fig. 2) were varied
with the sampling site and soil properties. Both the enzyme activities are comparatively
high in Mujpur site indicating high microbial activity in the estuarine zone.
Significant positive correlation was noticed between Dehydrogenase activity
(cluster of 27 samples from both Rayka and Dodka) and SOM (Fig.
3, r = 0.786, p<0.001, n = 27) in alluvial soils and it is very well
correlated in estuarine zone (Fig. 3 inset, r = 0.955, p<0.001,
n = 6).
||Properties of soils used in this study. RR, RRR, RW, RS and
RD are samples series collected at Rayka section. D and M are soils taken
at Dodka and Mujpur respectively. Rayka and Dodka samples are obtained from
alluvial zone of Mahi River where as Mujpur soils were representative of
estuarine zone of Mahi River
Protease activity does not show any significant relation with SOM (Fig.
3, r = -0.312, p>0.11, n = 27). However, in estuarine soil samples, a
positive correlation with SOM (Fig. 3) was obtained and was
significant (r = 0.98, p<0.001, n = 6).
Positive correlation was noticed between dehydrogenase and SMC (r = 0.56, p<0.001 n = 27) in alluvial soils (data not shown). No statistical relationship is seen between overall protease activity and SMC (p>0.05) in alluvial soils however the positive correlation found in estuarine soils (Fig. 4, r = 0.94, p<0.001, n = 6) and this is in agreement with other results indicating that the Mujpur section is microbiologically more active than other two sites.
||Dehydrogenase and protease activities of soil samples. (a)
Dehydrogenase activities of alluvial (from RR1-D5) and estuarine samples
(M1-M6). (b) Protease activities of alluvial (from RR1-D5) and estuarine
||Correlation of dehydrogenase and protease activities with
SOM in alluvial soils. Regression line shown for significant positive correlation
in case of dehydrogenase activity (r = 0.786, p<0.001), whereas no correlation
was noticed with protease activity. Inset shows data for estuarine (Mujpur
soil) samples, where both dehydrogenase and protease activities showed significant
positive correlation (r = 0.95 and r = 0.98 respectively) with SOM at p≤0.001
||Correlation of dehydrogenase and protease activities with
SMC in estuarine soils (r = 0.99 and r = 0.94 respectively) at p≤0.001
|| Pearson product moment correlation between soil enzymes and
|Protease activity: Tyrosine (μg) d.wt. g-1
2 h-1., dehydrogenase activity: TPF (μg) d.wt. g-1
24 h-1, Protease activity/C: Tyrosine (μg) d.wt. g-1
C 2h-1, Dehydrogenase activity/C: TPF (μg) d.wt. g-1
C 24 h-1
The other variables considered in this study are the sand, silt and clay content
and soil depth. Since soils were collected at different depth gradients, correlations
have been made for individual sites. Soil depth showed a negative correlation
with dehydrogenase and protease activities in alluvial zone (sites RR, RRR,
RW, RS, RD and D, Table 2) however, in estuarine zone (site
M), significant positive correlations were noticed with dehydrogenase activity
( r = 0.98, p<0.001, Table 2) and with protease activity
(r = 0.96, p<0.001, Table 2). The dehydrogenase activity
shows a moderate positive correlation with clay content of the soils (Fig.
5, r = 0.52, p<0.004, n = 27). No significant correlation was however,
noticed with protease activity (r = -0.45, p<0.177, n = 27) barring a positive
correlation in Mujpur site (Fig. 5, r = 0.92, p<0.001).
No apparent relation was found for both enzymes with pH, sand and silt content
of the soils at p level 0.1 (data not shown) however a negative correlation
of dehydrogenase activity and protease activity with sand proportion (r = -0.85,
p<0.02, n = 6, r = -0.94, p<0.004, n = 6, respectively) was noticed in
Mujpur section and it is site specific.No significant correlation was observed
between the two enzymes (Fig. 6, r = -0.32, p>0.1, n =
27) in alluvial soils.
||Correlation of dehydrogenase and protease activities with
clay content in alluvial soils. Regression line shown for positive correlation
in case of dehydrogenase activity (r = 0.52, p<0.004) where both dehydrogenase
and protease activities showed significant positive correlation (r = 0.99
and r = 0.92 respectively) with clay at p = <0.001
On the contrary significant positive correlation was observed between dehydrogenase
and protease in estuarine zone of Mahi River (Fig. 6, r =
0.94, p<0.001, n = 6).
Since the studied soils possess variable amounts of SOM, specific enzyme activity indices were calculated per unit of total C. These activity indices were correlated with soil parameters (Table 3) and the results show that dehydrogenase specific activity is moderately correlated with clay content and significantly correlated with SMC and SOM in both alluvial and estuarine soils (Table 3). These results are in agreement with enzyme activity results, indicating that SMC and SOM content are critical determinants of dehydrogenase activity. Protease specific activity in the alluvial soils do not show any correlation with soil indigenous properties however a strong correlation was observed with SOM and clay percentage in estuarine soils (r = 0.857, p = 0.02 and r = 0.92, p<0.009, respectively Table 3).
Principle Component Analysis (PCA) is a variable reduction method which can
be used to identify groups of observed variables that tend to cluster together.
Present data were subjected to PCA analysis and principle components were extracted
by Scree test from both alluvial and estuarine soils (Fig. 7,
b). In both the cases, the first two components displayed Eigen values greater
than 1.5. This suggested that the first two components were meaningful. Therefore,
only the first two components were retained for rotation (varimax orthogonal).
||Correlation between dehydrogenase and protease activities
was not found in alluvial soils however inset data shown for estuarine samples
and a linear strong correlation (r = 0.94) was observed among both the enzymes
|| Correlations between soil characteristics and specific enzyme
activity indices in semiarid alluvial and estuarine soils
Combined, components 1 and 2 of alluvial soil variables accounted for 67.19%
of total variance (Fig. 7a) whereas combined components 1
and 2 of estuarine soil variables accounted for 90.63% of total variance (Fig.
7b). PCA plots (Fig. 7a, b) indicate
that SMC, SOM, clay, dehydrogenase of both alluvial and estuarine zone form
a closer cluster and hence are correlated with each other whereas sand, silt
and pH showed different patterns and are scattered from the cluster. Strong
correlation among both dehydrogenase and protease was observed in estuarine
soils (Fig. 7b).
||Principle Component Analysis (PCA) for soil properties and
enzymes. (a) PCA loading plot of alluvial zone variables. (b) PCA loading
plot of estuarine zone variables
The activities of soil enzymes (dehydrogenase and protease) and their relation
to soil characters were investigated in semiarid alluvial and estuarine soils
around Mahi River basin. Both the enzyme activities were relatively high in
estuarine soil samples indicating high microbial activity as well as high soil
quality in estuarine zone. The enzyme dehydrogenase being one of the principle
agent in the degradation of SOM (Tabatabai, 1994), it
is inferred that SOM transformation in estuarine zone (Mujpur soils) is more
than other two sites (Rayka and Dodka). Generally, protease activity depends
on the distribution of proteolytic bacteria and the amount of proteinaceous
substrate availability in the SOM. The results of protease activity indicate
that proteolytic bacteria and the amount of proteinaceous substrates are comparatively
high at Mujpur which lies in estuarine zone.
Present findings demonstrate that dehydrogenase activity is sensitive to SOM,
SMC, clay and soil depth. The SOM is one of the critical determinative parameter
of soil dehydrogenase because organic matter is substrate for microbial dehydrogenase
activity. Gajananda (2007) demonstrated similar relationship
between organic carbon and dehydrogenase (r = 0.85, p<0.001) and stated that
organic C is an important factor in controlling the development of dehydrogenase
in arctic soils. Similar kind of observation was made by Tirol-Padre
et al. (2006) during his study on organic amendments on soil hydrolytic
enzymes. We infer that the immobilization of organo-mineral complexes by clay
minerals allows retention of substrate to dehydrogenase. In contrast the protease
activity is poorly correlated with SOM in alluvial zone. This may be due to
either low amount of proteinaceous matter in SOM or less distribution of proteolytic
bacterial population in studied semiarid alluvial soils.
Mujpur is situated in the estuarine zone of Mahi River; it gets inundated frequently during annual floods, high tides and subsequently high availability of substrate enhancing the protease activity. Multiproxy study on Mujpur section may provide meaningful information in respect of enzyme dynamics vis-a-vis temporal changes.
Theoretically, a general consideration is that soils with high SMC content
should possess high dehydrogenase activities because SMC enhances the microbial
activities and dehydrogenase exists in soils as integral parts of intact cells.
This was seen in Mujpur soils where SMC is positively correlated with its corresponding
dehydrogenase activity (Fig. 4). Brzezinska
et al. (2001) determined the relationship between the enzyme activity
and soil aeration parameters in a pot experiment with barley vegetation and
envisaged a positive relation between SMC and dehydrogenase activity (r = 0.59).
Similar kind of observation was found in the present study (Fig.
In accordance to earlier studies (Griffiths et al.,
2003), present results also showed a significant negative impact of soil
depth on hydrolytic enzymes. Niemi et al. (2005)
demonstrated a negative correlation between soil depth and enzyme activities
and positive correlation between SOM and enzyme activities. In previous studies
Sardans and Penuelas (2005) found a negative correlation
between hydrolytic enzymes and soil depth. The present study and obtained data
are in general agreement to their observations (Table 2).
However, an increase in dehydrogenase with depth in the Mujpur section is suggestive
of the increased enzymatic activity of anaerobic and facultative bacteria. Increase
in protease activity with depth at Mujpur may be due to increased substrate
availability and microbial activity. Similar kind of observations were made
by Wright and Reddy (2001) and reported that the decreased
protease and glucosidase activity with depth is due to decrease in substrate
quality along with depth.
Both the enzymes in alluvial soils are independent of each other (Fig.
6) indicating soil organic matter transformation and initial breakdown of
proteins are self regulated processes in alluvial systems. However, a correlation
between higher dehydrogenase activity and higher protease activity was observed
in Mujpur soils (Fig. 2 and 6) indicating
high metabolic state of the estuarine soils. Initial organic matter transformation
by dehydrogenase during microbial respiration made available substrate to protease
and subsequently higher protease activity achieved in estuarine zone. In contrast,
the alluvial site may be lacking a high amount of proteinaceous substrate in
its integral part of SOM.
We presume that lower soil enzyme activities in alluvial soils were associated
with progressive soil erosion. It has been demonstrated that dehydrogenase activity
can be used as a sensitive marker of soil degradation in semiarid Mediterranean
region of Spain (Garcia et al., 1997). In the
same study it was found that no correlation between the dehydrogenase activity
of the soils and organic matter content (r = 0.32, p = 0.18) and it is contradictory
to present findings which are showing positive correlation between dehydrogenase
and SOM (r = 0.52, p<0.004, n = 27) in the semiarid alluvial zone which is
under intense weathering. In another investigation which is on soil quality
degradation processes along a deforestation chronosequence in the Ziwuling area,
China, it was found that the soil erosion was the primary process responsible
for the degradation of soil physical, chemical and microbiological properties
(An et al., 2008). However, they have studied
alkaline phosphatase activity and invertase activity. In another report from
northern China (Yong-Zhong et al., 2005), decreased
soil enzyme activities were observed in a degraded sandy grass land however
their studies were mainly focused on influences of continuous grazing and livestock
exclusion on sandy grass land soil erosion. Although restricted to a limited
number of soils, the present data suggests that, dehydrogenase and protease
activities could be considered as indicators for intense erosion of semiarid
In the alluvial soils, the decrease in the activity of soil enzymes with involved in recycling of nitrogen and carbon may effect long term soil nutrient availability and reducing the nutrient supply to plants. Moreover in both alluvial and estuarine ecosystems, oxidation of organic content and subsequent transformation could be depending on SMC, clay and soil depth.
Two soil enzymes dehydrogenase and protease showed different relationships with soil properties depending upon the alluvial and estuarine zones. SOM, SMC, clay content and soil depth are the main determinants for soil dehydrogenase activity and subsequent organic matter transformation in both zones. Soil protease activity and its critical determinates were found to be site specific. Relatively estuarine zone showed high microbial activity as compared to alluvial zone in the semiarid Mahi River region.
This work was funded by Department of Science and Technology (DST), Government of India as research grant (No. SR. S4/ES-21/Baroda Window/P3) to GA under the multi-disciplinary scheme Science of shallow subsurface (SSS).
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