Depth Integrated Microbial Community and Physico-Chemical Properties in Mangrove Soil of Sundarban, India

doi:10.4236/aim.2012.23028

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Advances in Microbiology, 2012, 2, 234-240

http://dx.doi.org/10.4236/aim.2012.23028 Published Online September 2012 (http://www.SciRP.org/journal/aim)

Depth Integrated Microbial Community and

Physico-Chemical Properties in Mangrove Soil of

Sundarban, India

Subhajit Das1, Minati De2, Dipnarayan Ganguly1, Tushar Kanti Maiti3, Abhishek Mukherjee1,

Tapan Kumar Jana1, Tarun Kuma De1*

1Department of Marine Science, Calcutta University, Kolkata, India

2Maniktala Siksha Bhavan, Kolkata, India

3Microbiology Laboratory, Department of Botany, Burdwan University, Burdwan, India

Email: *[email protected], [email protected]

Received January 18, 2012; revised March 20, 2012; accepted June 5, 2012

ABSTRACT

In the Sundarban Mangrove forest microbial activities are dominantly involved in both the mineralization and decom-

position processes that regulate nutrient profile in soil of different depth. It was found that besides changing the water

and soil quality, monsoonal cycle plays a crucial role in regulating microbial population distribution in the mangrove

soil. Statistical analyses revealed that organic carbon was the most significant factor that regulated the total microbial

population. The cellulose degrading bacteria, [mean value of CFU 14.32 × 106 (gm dry weight of soil)–1] was dominant

throughout the year. The sulfate reducing bacteria showed an increasing trend along depth with a minimum value at the

surface i.e. 6.113 × 106 (gm dry weight of soil)–1 and 12.312 × 106 (gm dry weight of soil)–1 at a depth of 60 cm. Inten-

sification of monsoonal cycle could heavily affect microbe dominated soil biogeochemistry and subsequent change in

the regional ecology of the Sundarban Mangrove Forest.

Keywords: Sundarban Mangrove; Microbial Population; Monsoonal Cycle; Nutrient Concentration

1. Introduction

Mangroves are highly productive marine ecosystem

where bacteria actively take part in biomineralization and

biotransformation of minerals [1]. The distribution of

microbial activities in estuarine systems is clearly com-

plex and variable. Much research remains to be done in

order to define the distributions of microbial activities

and the major factors involved in controlling these dis-

tributions in estuaries. Leaves and wood provided by

mangrove plants to the soil are degraded primarily by

large variety of microbes which actively participate in

the heterotrophic food chain [2-4]. Major products of

general recycling of organic matter are detritus which is

rich in enzymes and proteins and contains large micro-

bial population [5]. Bacteria are the major participants in

the carbon, sulfur, nitrogen and phosphorous cycles in

mangrove forest [6,7]. Bacterial activity is responsible

for most of the carbon recycling in mangrove soil under

both oxic and anoxic conditions. Many species of phos-

phate solubilizing rhizosphere bacteria associated with

black mangrove roots were found. The mechanism for

phosphate solubilization probably involves the produc-

tion of several organic acids [8]. Saprophytic fungi are

fundamental to many aspects of decomposition and en-

ergy flow in mangrove forests [9]. Most investigations of

anaerobic metabolism in natural ecosystem have dealt

with sulfate rich marine soils where sulfate reduction is

the dominating process or eutrophic lake soils where sul-

fate and nitrate are depleted in the hypolimnionn and in

the superficial soil layers leaving terminal carbon miner-

alization principally to methane producing bacteria

[10-12]. Sulfate reduction, methane production, denitri-

fication are the important processes for the terminal elec-

tron removal during decomposition of organic matter in

anoxic environment. The methanogens are characterized

by their ability to produce methane from hydrogen and

carbon di oxide, formate, acetate, methanol etc. [13].

Methanotrophs are a subset of a physiological group of

bacteria known as methylotrophs. They are unique in

their ability to utilize methane as a source of carbon and

energy [14]. Nitrogen fixing bacteria are the other group

of bacteria that are involved in formation of ammonia or

organic nitrogen from atmospheric nitrogen. They may

be free-living or symbiotic in Nature. It has been studied

*Corresponding author.

S. DAS ET AL. 235

that N2 fixation by heterotrophic bacteria are generally

regulated by specific environmental factors like Oxygen,

combined Nitrogen and the availability of Carbon source

for energy requirement [15]. Aerobic, autotrophic nitrifi-

ers oxidize ammonia to nitrite and nitrate, with molecular

oxygen as electron acceptor. Nitrite and nitrate are re-

duced to dinitrogen gas by heterotrophic denitrifying

bacteria that use NOx instead of oxygen as electron ac-

ceptor [16]. The purpose of the present study was to ex-

amine seasonal and spatial variations in microbial popu-

lation (bacteria and fungi) in mangrove soil and to find

out the correlation between different microbes with nu-

trients.

2. Materials and Methods

2.1. Study Area

The Sundarban Mangrove Forest is located between

21˚31′N and 22˚30′N and longitude 88˚10′E and 89˚51′E

along the North East coast of Bay of Bengal, India. This

mangrove forest is a part of the estuarine system of the

River Ganges, NE coast of Bay of Bengal (Figure 1).

The climate in the region is characterized by the south-

west monsoon (June-September), northeast monsoon or

post-monsoon (October-January), and pre-monsoon (Fe-

bruary-May); 70% - 80% of annual rainfall occurs dur-

ing the summer monsoon (southwest monsoon), The tide

in this estuarine complex is semidiurnal in nature with

spring tide ranging between 4.27 and 4.75 m and neap

tide range between 1.83 and 2.83 m. It is a unique bio-

climatic zone in between the land and ocean boundaries

of the Bay of Bengal and the largest delta on the globe.

The deltaic soil of Sundarban Biosphere Reserve com-

prises mainly saline alluvial soil consisting of clay, silt,

fine sand and coarse sand particles.

2.2. Sample Collections and Analyses

Soil samples were collected aseptically using a hand-

held stainless steel core sampler (3.2 cm diameter, 100

cm long) from six different depth i.e. 1) 0 - 10 cm; 2) 10

- 20 cm; 3) 20 - 30 cm; 4) 30 - 40 cm; 5) 40 - 50 cm and 6)

50 - 60 cm at five different sites in dense mangrove area

(Deep forest) covering different seasons. Samples were

collected into sterilized containers and immediately trans-

ported to the laboratory for analyses. Three replicates

Figure 1. Map showing the study area.

S. DAS ET AL.

236

from each site were analyzed for five sites at different

depths. The result represents the average value at each

depth.

2.3. Quantification of Bacteria and Fungi

Soil samples were stored at 4˚C immediately after

collection and transported to the laboratory, for analysis

with adequate care. 10 gm of sample from different depth

of different regions were homogenized with sterilized

phosphate buffer solution. Serial dilutions up to 10–4

were made and inoculation was done with 0.1 ml. Quan-

tification of bacteria and fungi from mangrove soils was

carried out by spread plate method for different types

of bacteria such as Phosphorous Solubilizing Bacteria

(PSB), Cellulose Degrading Bacteria (CDB), nitrifying

bacteria, free living nitrogen fixing bacteria and fungi

and they were incubated at different conditions [17].

Sulfate reducing bacteria was cultured in Starkey’s me-

dium in anaerobic condition [18].

2.4. Soil Quality Measurement

Concentration of Nitrate-Nitrogen, Nitrite-Nitrogen, Pho-

sphate-Phosphorous and Silicate in the soil sample was

measured at 10 cm interval (from 0 to 60 cm depth). 30 g

of soil subsample was collected from the different depth

and was immediately extracted in 75 mL of 2 mol·L−1

potassium chloride (KCl). The mixture was shaken until

well mixed and allowed to stand overnight [16]. After 24

h, 4 mL of the supernatant was collected for the estima-

tion of different nutrients using standard spectropho-

tometric methods [19]. Concentration of Sulfate-Sulphur

of the soil was measured using standard protocol [20].

The pH value was measured in a 1:5 (w/w) soil water

suspension using electric digital pH meter [21] and soil

organic carbon was measured by standard methods [22].

Salinity of a soil saturation extract (ECe) was determined

by measuring the electrical conductance of soil water

saturation extract with the help of a conductivity meter

[23]. Soil redox potentials (Eh) at each sampling site

were measured with brightened platinum electrodes

which were allowed to equilibrate in situ for 1 hr prior to

measurement. Each electrode was checked before use

with quinhydrone in pH 4 and 7 buffers (mV reading for

quinhydrone is 218 and 40.8, respectively, at 25˚C). The

potential of a calomel reference electrode (+244 mV)

was added to each value to calculate Eh value for the soil

samples [24].

3. Result and Discussion

Mangrove soil at Indian Sundarban showed seasonal

variation with respect to both major nutrient concen-

trations and microbial population. Beside monsoonal

influx of nutrients to the system, mangrove litters also

played a significant role in regulating the nutrient status

that in turn controlled the microbial population. Among

several physical factors tidal inundation, wave action,

presence of mangrove roots and bioturbation are the im-

portant ones considered for determining microbial abun-

dance in the mangrove soil from surface to a depth up to

60 cm. The physico-chemical parameters of the study are

shown in Table 1. Temperature and Eh value of soil

sample showed a decreasing trend from surface to 60

cm of depth during all season. A reverse profile was

Table 1. Seasonal variations of phys ico-chemical parameters of soil at d ifferent d epth in Sundarban mangrove environment.

Season Parameters (soil) 0 m 10 m 20 m 30 m 40 m 50 m 60 m

Eh (mV) –95 –100 –105 –112 –125 –135 –145

pH 7.95 8.25 8.27 8.23 8.25 8.21 8.19

Temp (˚C) 17.85 17.84 17.83 17.82 17.82 17.78 17.78

Pre-monsoon

Salinity (PSU) 16.80 16.96 17.05 17.20 17.35 17.40 17.60

Eh (mV) –100 –102 –110 –118 –145 –170 –175

pH 8.22 8.20 8.15 8.14 8.13 8.12 8.12

Temp (˚C) 24.71 24.69 24.67 24.65 24.60 24.59 24.59

Monsoon

Salinity (PSU) 14.99 15.01 15.05 15.15 15.20 15.35 15.41

Eh (mV) –121 –125 –128 –130 –139 –165 –187

pH 8.42 8.35 8.32 8.30 8.25 8.22 8.19

Temp (˚C) 12.90 12.94 12.98 12.99 13.05 13.12 13.12

Post-monsoon

Salinity (PSU) 15.35 15.39 15.45 15.50 15.60 15.65 15.69

S. DAS ET AL. 237

found for pH and salinity. During monsoon, the salinity

was found to be 14.99 psu in surface soil and it was

15.41 psu at 60 cm depth. Less soil salinity in monsoon

with respect to pre monsoon and post monsoon may be

due to maximum dilution by river run off during mon-

soon period [25]. Eh value showed a decreasing trend

from surface soil (–95 mV) to 60 cm of depth (–145 mV)

which represented more anoxicity of bottom soil than

that of surface during premonsoon (Table 1). Soil redox

potential value (Eh) from surface to 60 cm of depth re-

gion in three distinct seasons suggested that the soil of

deep forest region of Sundarban Mangrove is relatively

anoxic or it can be referred to as oxygen-starved soil.

During pre-monsoon nutrient concentration showed very

weak stratification from surface to 30 cm of depth with

almost uniform distribution. Intense bioturbation up to 30

cm depth by several benthic organisms could cause uni-

form mixing of soil nutrients.

No significant variation of silicate concentration was

found throughout the entire depth. Gradual decrease in

organic carbon and Phosphate-Phosphorous concentr-

ation was observed from depths of 30 to 60 cm.

During transportation of organic matter from surface

to bottom, it is decomposed by microbes. As a result,

organic content of soil decreased with increasing depth.

It could be attributed to mangrove litter fall with an an-

nual rate of 1603 g·m–2·year−1 [26]. Organic carbon was

found maximum during postmonsoon followed by pre

monsoon and monsoon (Figure 2(a)). Nitrate-Nitrogen

concentration was increased from surface to 40 cm of

depth but decreased from 40 cm to 60 cm. Vertical

movement of materials, nutrient cycling and reuse driven

by various burrowing organisms could have an effect on

this Nitrate-Nitrogen distribution along the depth profile

at up to 40 cm. Less abundance of bioturbation below 40

cm could enhance the anoxic condition which in turn

initiate denitrification causing sudden depletion of Nitrate-

Nitrogen. The Nitrite-Nitrogen concentration showed no

significant variation throughout depth but slight increased

below 50 cm of depth which may be an indication of deni-

trification. Population of SRB was found to increase with

increase in depth in all seasons. Thus, more anoxic con-

dition preferred the more population of SRB in the bot-

tom soil than that of surface soil. Fungal population

showed decreasing trend with increasing depth. Free liv-

ing nitrogen fixing bacterial population showed de-

creasing trend from surface to 30 cm depth and increased

again from 30 cm to 50 cm of depth. After the death of

plant, the woods are carried away by tidal action or con-

sumed by herbivorous animal but the root attached to the

bottom soil below the 50 cm depth seldom may act as the

source of Carbon to fungus and cellulose degrading

bacteria (Figure 2(a)).

During monsoon Nitrate-Nitrogen, organic carbon con-

tent of soil showed decreasing pattern along with de-

crease in population of nitrifying bacteria with increase

in depth. Silicate concentration showed little variation

with increasing depth. Population of PSB was found to

be decreased with increase in depth and at the same time,

Phosphate-Phosphorou s concentration was also found to

decrease with increase in depth. Population of CDB

decreased with increase in depth as the organic carbon

content of the soil was also found to decrease with

increase in depth. Population of SRB showed increasing

trend from surface to 60 cm of depth (Figure 2(b)).

During postmonsoon Nitrate-Nitrogen organic carbon

content of soil showed decreasing pattern along with

decrease in population of nitrifying bacteria with increase

in depth. Silicate concentration showed little variation

with increasing depth. Population of PSB was found to

be decreasing with increasing depth and at the same time,

Phosphate-Phosphorou s concentration was also decrea-

sing with increase in depth. Population of CDB de-

creased with increase in depth as the organic carbon

content of the soil was also decreasing with increase in

depth. Sulfate concentration did not show distinct strati-

fication though population of SRB showed increase in

trend from surface to bottom (Figure 2(c)). Free living

nitrogen fixing bacteria showed decrease in population up

to 30 cm of depth but below 30 cm to the next 30 cm of

depth their population was recorded to increase. Popu-

lation of PSB and free living nitrogen fixing bacteria was

more in proportion than population of nitrifying bacteria.

Organic carbon content of the soil was found to be most

significant factor on the growth rate of cellulose decom-

posing bacteria (Pearson correlation of OrgC (%) and

C.D.B. (CFUs × 106) = 0.500, P-Value = 0.000). The

populations of cellulose decomposing bacteria were

found to be more in post monsoon period than that of

premonsoon and monsoon. Again the zone with more

population of phosphate solubilizing bacteria showed

more concentration of available phosphate. Presence of

phosphatase enzyme within such type of bacteria might

be responsible for these findings [27]. It might be for

availability of more organic carbon source. Sulfate re-

ducing bacteria was found to be correlated with sulfate

concentration of soil sample (Pearson correlation of Sul-

fate-Sulphur mg·gm–1 dry wt of soil and S.R.B. (CFUs ×

106) = 0.595, P-Value < 0.001).

Phosphate solubilizing bacteria was also found to be

correlated with phosphate concentration of the Sundarban

mangrove soil (Pearson correlation of Phosphate-Phos-

phorous µg·gm–1 dry wt of soil and P.S.B. (CFUs × 106)

= 0.766, P-Value = 0.000). No such correlation was

found for nitrogen fixing bacteria with nitrate and nitrite

concentration. Organic carbon from the leaves, wood

from forest and other organic dead or waste products

from other living creatures are easily degraded by cellu-

lose degrading bacteria in the mangrove soil because

they are the most dominating group of microbes prior to

S. DAS ET AL.

238

D epth pro f ile of nutrient status and Org

deep forest region during premonsoon

00.511.52

Conc. of Nutrients and Org.Carbon

Depth (cm)

. C in

Nitrate-Nitrogen

µg/gm dry wt of

soil

Nitrite-Nitrogen

µg/gm dry wt o

soil

Org.C (%)

Phosphate-

Phosphorous µg/

gm dry wt of soi

Sulfate-Sulphur

mg/gm dry wt o

soil

Silicate µg/gm

dry wt of soil

(x10)

Verti cal Di stribut ion of Micro bes D uring Premonso on

0246

C.F.U X 10

-1

dry wt of soil

Depth (cm)

Ntrfyng Bacteria

P.S.B

N2-FIXER

C.D.B

Fungi

S.R.B

(1) (2)

(a)

D epth profi l e of nutri ent st atus and O r

deep forest region during monsoon

00.5 11.52

Conc. of Nutrients and Org.Carbon

Depth (cm)

g. C i n

Nitrate-

Nitrogen µg/g

dry wt of soil

Nitrite-

Nitrogen

µg/gm dry wt

of soil

Org.C (%)

Phosphate-

Phosphorous

µg/ gm dry wt

of soil

Sulfate- Sulp hu

mg/gm dry wt

of soil

Silicate µg/gm

dry wt of soil

(x10)

Vert ical Di stribu tion of Microbes Du rin g Monsoon

0246

C.F.U X 10

-1

d ry w t of soil

Depth (cm)

Ntrfyng Bacteria

P.S.B

N2-FIXER

C.D.B

Fungi

S.R.B

(1) (2)

(b)

Vertical D i stribution of Microbes During

Postmonsoon

02468

C.F.U X 10

-1

dry wt of soil

Depth (cm)

D epth pr ofil e of nutri ent status and Or g

deep forest r egi on during postmonso

0123

Conc. of Nutrients and Org .C arbo n

Depth (cm)

. C i n

o n

Nitrate-

itrogen µg/g

dry wt of soil

itrite-Nitrogen

µg/gm dry wt

of soil

Org.C (%)

Phosphate-

Phosphorous

µg/ gm dry wt

of soil

Su lfa te -Sulphur

mg/g m dry wt

of soil

Silicate µg/gm

dry wt of soil

(x10)

Ntrfyng

Bacteria

P.S.B

N2-FIXER

C.D.B

Fungi

S.R.B

(1) (2)

(c)

Figure 2. (a) Depth profile of organic carbon, nutrient concentrations (1) and microbial populations (CFUs) (2) during

pre-monsoon at different depth; (b) Depth profile of organic carbon, nutrient concentrations (1) and microbial populations

(CFUs) (2) during monsoon at different depth; (c) Depth profile of organic carbon, nutrient concentrations (1) and microbial

opulations (CFUs) (2) during post-monsoon at different depth. p

S. DAS ET AL. 239

fungi. Other groups of microbes have also shown sig-

nificant population which is a good sign for a mangrove

forest with respect to mineralization of organic debris

and as a result mangrove plants can easily get nutrients in

their simplest forms. From seasonal perspective, the

monsoon period was significantly different (Student’s t

test, P < 0.01) than other periods of the year in terms of

total bacterial abundance and other key parameters. Sea

level rise due to global warming may hamper the stable

ecological zone of Sundarban mangrove forest which

may ultimately reflect to net flux of several biologically

active trace gases between soil and atmosphere. Intro-

duction of huge amount of nutrients during monsoon

have a positive feedback on the bacterial population of

mangrove sediment. Beside the changes in several phys-

icochemical parameters, transport of huge amount of

aquatic microbes could lead to the significant increase in

the microbial population in the soil of this mangrove eco-

system. This may contribute to the aquatic biogeochem-

istry of this tropical wetland.

4. Acknowledgements

The financial assistance from DOEn, Govt. of West

Bengal and U.G.C., New Delhi are gratefully acknowl-

edged. The authors are also grateful to the Forest De-

partment, Govt. of West Bengal for assisting the research

team in collecting data and providing all infrastructural

facilities to reach the remote island.

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