Indian Journal of Geo-Marine Sciences Vol. 41(5), October 2012, pp. 405-411 Distribution of Aerobic and Anaerobic Bacteria along the Intertidal Zones of Sunderban Mangrove Ecosystems, NE Coast of Bay of Bengal, India S.Das1, M.De2, T.K.De1*, R. Ray1, T.K. Jana1 P. K. Ghosh3 & T.K.Maiti3 1 Department of Marine Science, Calcutta University, 35, B.C. Road, Kolkatta-700 019, India 2 Manicktala Siksha Bhavan, 304/B/1 Bagmari Road, Kolkata-700 054, India 3 Microbiology Laboratory, Department of Botany, Burdwan University, Burdwan-713 104, India * [E:mail: [email protected]; [email protected]] Received 11 March 2011; revised 16 November 2011 Population of aerobic and anaerobic bacteria along the different tidal zones of Sundarban Mangrove forest sediment was studied to determine their distribution with the availability of different nutrients and other physicochemical parameters. Lower littoral zone (LLZ) along the shore which remains inundated by sea water showed more population of anaerobic bacteria (212 x 104 CFUg-1) than that of mid littoral zone(MLZ) (102 x 104 CFUg-1) and upper littoral zone(ULZ) (60 x 104 CFUg-1). Population of aerobic bacteria was found to be maximum in ULZ (57 x 104 CFUg-1) compared to MLZ (46 x 104 CFUg-1) and LLZ (14 x 104 CFUg-1). Population of methanogens increased with rise of sea level which in turn emitted more methane than CO2. A stable dynamic equilibrium for growth rate of aerobic and anaerobic bacteria observed in ULZ and is ecologically more consistent than LLZ particularly with respect to methane emission from sediment. Anaerobic bacteria are relatively more tolerant to variable salinity, pH and other physicochemical factors than the aerobic bacteria. [Keywords: Aerobic, Anaerobic, Bacteria, Sediment, Population] Introduction Mangrove forests are usually considered to be high productive areas that support highly developed detritus-based food webs1. High primary productivity of mangroves implies a high demand for nutrients essential to plant growth and this demand appears to be met by a highly efficient system of nutrient trapping, uptake and recycling2,3. Organisms within mangrove ecosystems, including microorganisms, plants and animals, show complex interactions. Microorganisms are intimately involved in biogeochemical cycling and in many instances are the only biological agents capable of regenerating forms of the elements used by other organisms, particularly plants4. Therefore, Mangrove provides a unique ecological niche to different microbes which play various roles in nutrient recycling as well as different environmental activities5. The decomposition in this forest involves microorganisms at various tropic groups acting in a multi step process The first step is an enzymatic hydrolysis of polymeric material to soluble monomeric and oligomeric compounds6. Under oxic conditions the soluble compounds are directly mineralized to carbon dioxide and water where as under anoxic conditions various physiological groups are involved in degradation after the initial depolymerisation. Fermentative bacteria convert the products of hydrolysis to a variety of products, mainly short chain fatty acids, carbon dioxide and hydrogen. Further conversion through the action of secondary fermenters, sulphate-reducers, acetogens and methanogens produces the end products CO2, CH4 and H2S, which may escape into the atmosphere7. All three are important greenhouse gases. The organisms within mangrove ecosystems, including microorganisms, plants and animals, show complex interactions. Microorganisms are intimately involved in biogeochemical cycling and in many instances are the only biological agents capable of regenerating forms of the elements used by other organisms, particularly plants. Earlier Thomas et al8 established an ecological relationship between aerobic and anaerobic bacteria available in the coastal sediment. There are two distinct zones in soil i.e. aerobic zone (Soil Surface) and anaerobic zone (below 30 cm from soil surface) were studied to examine the growth of two above mentioned bacteria type (Fig. 1). The range of depth of these two zones varied with different geochemical parameters. In anaerobic zone methane is produced from carbon dioxide and H+ ion by several methanogenic bacteria which are anaerobic in nature. Hydrogen sulfide gas is 406 INDIAN J. MAR. SCI., VOL. 41 NO. 5 OCTOBER 2012 also produced from this zone by anaerobic bacteria. These reduced molecules when reach aerobic zone, they get oxidized by aerobic bacteria present in this zone. Methanogens have the ability to obtain energy by oxidizing hydrogen or formate and utilizing the electrons thus generated to reduce carbon dioxide with the formation of methane gas9. When this methane when reaches to aerobic zone it is utilized by aerobic bacteria to form carbon dioxide; unutilized methane comes out from the soil and contributes to the atmospheric trace gas composition. Therefore more consumption of methane in aerobic zone will result less emission from sediments. Thus a significant interaction between aerobic and anaerobic bacteria is necessary for the ecologically consistent of the environment. Present study consists of the comparison between population of aerobic and anaerobic bacteria and their interaction in the different tidal zones of Sunderban mangrove forest along the coastal zone of North East coast of Bay of Bengal, India. It also elucidated some light on the sediment with relatively population of anaerobic methanogenic bacteria and effect of changing different physicochemical parameters on aerobic and anaerobic bacterial population of the change of sea level. Materials and Methods Study area Sunderban Mangrove forest is located geographically in between 21º 31’ N and 22º 30’ N and longitude 88º 10’ E and 89º 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 (Fig. 2), which covers 9630 km2, out of which comprise of inter-tidal area, covered with thick mangroves, is subdivided as forest sub-ecosystem and 1781 km2 of water area as aquatic sub-ecosystem. The tide in this estuarine complex is semidiurnal in nature with spring tide to range between 4.27 m and 4.75 m and neap tide range between 1.83 m and 2.83 m. It is a unique bioclimatic zone in Land Fig 1 Gaseous exchange between soil sediment and atmosphere Ocean boundaries of Bay of Bengal. In the southern part of the island, the ground level is high while in the northern areas the land is low and gets inundated during highest high tide. Avicennia alba, Avicennia marina and Avicennia officinalis are the dominant mangrove species, Excoecaria agallocha and Heritiera fomes are thinly distributed and Ceriops decandra is found scattered all over the island. The deltaic soil of Sunderban Biosphere Reserve comprises mainly saline alluvial soil consisting of clay, silt, fine sand and coarse sand particles. It is described as very deep, poorly drained, fine soils occurring on lower to nearly lower level delta with loamy surface, severe flooding and very strong salinity (extensive extent) associated with very deep, very poorly drained, fine loamy soil. Sediment samples were collected monthly from three intertidal zones of Sunderban mangrove ecosystem during February 2008 to January 2009. Replicate Soil samples were collected aseptically by using a hand–held stainless steel corer sampler from the top 30 (3.2 cm diameter, 30 cm long) from Upper Littoral Zone (ULZ), Middle Littoral Zone (MLZ), and Lower Littoral Zone (LLZ) and average values were taken. Soil samples were brought back to the laboratory in iced condition in sterilized container. Quantification of aerobic and anaerobic bacteria Samples (about 10 g) from different tidal zone of were homogenized with sterilized phosphate buffer solution. Serial dilutions up to 10-4 were made and inoculation was done with 0.1 mL. Quantification of bacteria from mangrove sediments was carried out by spread plate method Bacteria present in sediment were cultured in Marine Agar 2216 Medium after isolation by phosphate buffer solution10. In medium for anaerobic Fig.2 Map showing the location of study area DAS et al.: DISTRIBUTION OF AEROBIC AND ANAEROBIC BACTERIA IN SUNDERBAN MANGROVE ECOSYSTEMS Bacteria, sodium sulfide was added as reducing agent. It was incubated in anaerobic environment in Gaspak anaerobic jar for cultivation of anaerobic bacteria11. After same incubation period Colony Forming Unit (CFU) of aerobic and anaerobic bacteria present in soil surface sediment were counted to compare their growth rate in different oxic and anoxic conditions Table 1. Different kind of aerobic and anaerobic bacteria was cultured in different selective medium with appropriate condition for enumeration of bacterial population12. Sediment quality measurement Bio-available nitrate present in the sediment sample was extracted with 2 M KCL solution and the extract was used to estimation of nitrate spectrophotometrically. The absorbance of the resulting pink solution was measured photo-metrically at 543 nm against a reagent blank13. For estimation of sulphate in the sediment 20 gm of it was dissolved in 100 mL distilled water. After vigorous shaking for 1 hr the solution were filtered through Millipore filter paper (0.45µm). The filtrate was used to determine sulphate concentration turbidometrically13. Soil was dissolved in distilled water and chlorinity (Cl) of the water were determined by Mohr-Knudsen titration method and standard seawater of chlorinity 19.374 procured from the National Institute of Oceanography Goa, was used for the standardization. From the knowledge of chlorinity, salinity (S) was calculated using the Knudsen relation: S (× 10-3) = 1.80655 × Cl (× 10-3). The soil pH was determined following a water paste and determined by using micro pH meter (Systronics, model No, 362). The organic matter was determined by the modified Wakly–Black method (oxidation with potassium dichromate in sulphuric acid solution to obtain organic carbon). Result and Discussion Soil salinity varied in decreasing order from ULZ to LLZ with highest and lowest values of 30.1±3.53 and 15.8±1.98 in ULZ and LLZ, respectively (Table 1). Both Eh and pH values decrease from ULZ to LLZ which indicates the oxic/anoxic nature of sediment. Oxic conditions with relatively higher Eh values in the sediment are favoarable for aerobic bacteria but unfavourable for the anaerobic bacteria. Sediment in the LLZ experience frequent tidal inundation at a daily basis. Submergence may cause more anoxicity relative to the sediment exposed to air. Maximum and minimum concentrations of both organic carbon and inorganic nitrogen were found in the ULZ and LLZ sediments, respectively. Regular tidal flushing which was more frequent in LLZ than the ULZ could transfer more organic carbon and other nutrients from the sediment from the former. An ecological balance between the aerobic and anaerobic bacterial population was recorded in the sediment collected from ULZ. On the contrary anaerobic bacterial population in the LLZ sediment was found almost 12 times higher than its aerobic counterpart. After similar incubation period Colony Forming Unit (CFU) of aerobic bacteria present in soil surface sediment of ULZ was found more than that of the aerobic bacteria present in surface soil sediment collected from LLZ. This could indicate the persistence of relatively greater anoxic condition at the lower littoral zone than that of the upper littoral zone14. Fig. 3 represents the growth curve for both the mean anaerobic Fig 3 Mean growth curve of aerobic and anaerobic bacteria in three zones Table 1 Physico-chemical parameters and CFUs of aerobic and anaerobic microbes in three intertidal zone (Average values of 12 months are given with standard deviation) Soil Parameters Salinity (psu) pH Eh (mV) Org Matter(%) NO3-N-1 (µg g-1 dry soil) SO4-S-2 (mg g-1 dry soil) Mean CFU (Anaerobic) Mean CFU (Aerobic) 407 ULZ MLZ LLZ 30.10±3.53 8.01±0.2 -94.60±8.9 2.28±0.4 0.97±0.12 6.21±0.82 54.00 ± 6 61.00 ± 4.6 20.30±2.14 7.88±0.12 -127.00±10.2 2.17±0.7 0.88±0.08 3.12±0.75 138.00 ± 36 41.00 ± 5 15.80±1.98 7.22±0.08 -212.00±28.8 1.65±0.4 0.79±0.06 2.60±0.34 220.00 ± 8 19.00 ± 5 408 INDIAN J. MAR. SCI., VOL. 41 NO. 5 OCTOBER 2012 and aerobic bacterial population. Higher C.F.U of anaerobic bacteria in LLZ was observed relative to the aerobic bacterial population where as in ULZ, C.F.U of aerobic bacteria was found more than that of anaerobic bacteria. This result strongly indicates that the upper littoral zone is more oxic than that of lower littoral zone. In upper littoral zone a significant interaction was seen between aerobic and anaerobic bacteria which reflects good environmental health of the ecosystem resulting an efficient oxidation of the reduced and harmful gases like hydrogen sulfide, methane etc. in the sediment column before reaching the environment15. Both the lower littoral and middle littoral zone showed more population of methanogens than methanotroph which could convert the system as a net emitter of methane to the atmosphere. The methanogenic bacterial population depends on temperature, pH, redox potential and salinity of the water and sediments16. The presence of sulphate reducing bacteria limits the proliferation of methanogens17. Sulfate and nitrate concentration was found to show an increasing trend from LLZ to ULZ which is reflected in Fig. 4 and Fig. 5 respectively. Fig 4 Mean C.F.U of aerobic and anaerobic bacteria in different sulfate Concentration in three zones During transportation from riverine system to terrestrial environment biomineralization are slowly performed on the way by the decomposers which may contribute more nitrate and sulfate to the ULZ than that of LLZ. Population of aerobic bacteria showed increasing trend from LLZ to ULZ where as reverse profile was found for anaerobic bacteria18. found higher population of anaerobic bacteria in the sulfate rich sediment dominated by Avecennia marina. Mangrove sediments are mainly anaerobic with an overlying thin aerobic sediment layer. Degradation of organic matter in the aerobic zones occurs principally through aerobic respiration whereas in the anaerobic layer decomposition occurs mainly through sulphate reduction19, 20. The availability of iron and phosphorous in mangrove sediments may depend on the activity of sulphate reducing bacteria20. In Florida’s mangrove sediments contained a significant population of sulphate reducing bacteria were also able to fix N221. This present study supported this observation. Benner et al. (1984)22 and Lee (1992)23 found that in any sediment column rate of decomposition of organic matter by aerobic bacteria was more than that of anaerobic bacteria. Our present study supported this surveillance because in the present study the population of anaerobic bacteria was found to show a decreasing trend with increase in organic matter content of the soil sample of LLZ, MLZ and ULZ respectively. A reverse profile was found for the population of aerobic bacteria (Fig. 6). Higher population of aerobic bacteria in the sediment of more organic matter may be due to faster decomposition rate24. Salinity of soil sample was found to show an increasing trend from LLZ to ULZ. At the same salinity of LLZ region population of anaerobic bacteria was found to be more in Fig 5 Mean C.F.U of aerobic and anaerobic bacteria in different N-NO3- concentration in three zones Fig 6 Mean C.F.U of aerobic and anaerobic bacteria in different organic matter concentration in three different zones DAS et al.: DISTRIBUTION OF AEROBIC AND ANAEROBIC BACTERIA IN SUNDERBAN MANGROVE ECOSYSTEMS 409 Fig7 Mean C.F.U of aerobic and anaerobic bacteria in different salinity in three different zones et al (2000)26 the optimum range of pH for anaerobic methanogen in mangrove sediment varied between 6.5 and 7.5. In this present study identical observation was found. Soil sample collected from LLZ with relatively lower pH value of 7.22 was dominated by higher number of anaerobic bacteria than that of aerobic bacteria (Fig. 8). On the contrary, in the sediment collected from ULZ with mean pH value of 8.01, slight dominance of the aerobic bacteria was recorded over their anaerobic counterpart. Influence of salinity on the growth rate of both aerobic and anaerobic bacteria was examined by growing them in the selective medium with different salinity of 10, 15, 20, and 25 PSU which is represented in Fig. 9. A consistent interaction was found between aerobic and anaerobic bacteria near salinity range between 22 and 24 PSU. On the other hand an inconsequential interaction was recorded in the rest part of the salinity range. Variation in soil salinity was found more in surface sediment (aerobic) than the bottom (anaerobic) sediments which was collected below the 30 cm from the surface. This was due to the routine effect of high tide and low tide affecting the surface more efficiently than the deeper part. This indicates that the growth rate of aerobic bacteria was more influenced by daily variation of salinity whereas anaerobic bacteria were less influenced. It can also be said from Fig. 9 that the aerobic bacteria are more sensitive to variation in salinity than that of anaerobic bacteria. These observations were found similar to that by Rietz and Haynes et al. (2003)27 in wetland sediment. Aerobic bacteria are less resistant to salinity fluctuation25, which in turn may hamper oxidation process of methane. This may cause more methane emission than the carbon dioxide from the sediment. Fig 8 Mean C.F.U of aerobic and anaerobic bacteria in different pH value in three zones Fig 9 Effect of salinity on growth of both aerobic and anaerobic bacteria comparison with population of aerobic bacteria. Same profile was also found in MLZ. This observation can be explained from the study by Lowe et al. (1993)25. According to their report it can be predicted that anaerobic bacteria can grow at environmental extremes of temperature, pH, salinity, substrate toxicity, or available free energy and anaerobes, unlike aerobes, appear to have evolved more energyconserving mechanisms for physiological adaptation to environmental stresses such as novel enzyme activities and stabilities and novel membrane lipid compositions and functions. In upper littoral zone salinity was found to be maximum but population of aerobic bacteria was found to be little more than that of anaerobic bacteria. It can be explained by the fact that the ULZ remains exposed maximum period of time to cause oxic environment which may promote the growth of aerobic bacteria even with higher salinity zone (Fig. 7). Sediment profile of different tidal zone showed an increasing trend for pH value from LLZ to ULZ. According to the study by Lyimo 410 INDIAN J. MAR. SCI., VOL. 41 NO. 5 OCTOBER 2012 Any perturbation in the sediment biogeochemistry of Sunderban mangrove forest due to climate change may alter the magnitude of methane emission from the biosphere than present. Organic matter showed prominent effect on the growth rate of both for aerobic and anaerobic bacteria28. It is well documented in several reports that more the organic carbon in the sediment more would be the consumption of oxygen. This in turn favors the growth of anaerobic bacteria but inhibits growth of aerobic bacteria. Organic products from mangrove litter falls and other anthropogenic sources increase concentration of organic carbon in soil. This supply of organic carbon along with enhanced submergence of mangrove sediment due to sea level rise could fuel the anoxic condition of mangrove sediment. This may result a higher growth rate of anaerobic bacteria than the aerobic bacteria in this wetland sediment. Production of methane may also get increase by several times than its consumption by aerobic bacteria. As a result Sunderban mangrove forest may act as stronger net emitter of methane to the atmosphere than the present. Conclusion Mangrove ecosystem provides shelter and nurturing sites for many marine micro organisms. The present study of interaction between aerobic and anaerobic bacteria present in sediment of NE Coast of Bay of Bengal infers the following. Viable count of both aerobic and anaerobic bacteria in coastal zone replicates the depth profile of soil biogeochemical characteristics regarding oxic and anoxic conditions. Thus microbiological study on soil sample will be an effective clue for determination of soil quality. Organic waste product must be treated properly before discharging into natural body of water; otherwise such organic waste will make the environment ideal for the methanogenic bacteria causing more emission of methane from wetland soil to the atmosphere. Anaerobic bacteria are more resistant to the soil salinity fluctuation than that of aerobic bacteria. Sea level rising due to global warming may cause fluctuation of water as well as soil salinity which may ultimately hamper the activity of aerobic bacteria a little more than that of anaerobic bacteria. Thus oxidation of the reduced trace gas like methane by aerobic bacteria like methanotrophs could be hindered more than that of in present. In such condition mangrove sediment may emit more methane to the atmosphere. Sea level rise due to global warming may act adversely to the stable ecological zone of Sunderban Mangrove Forest which may ultimately reflect to net flux of several biologically active trace gases between soil and atmosphere. Acknowledgments The financial assistance from Department of Science and Technology, New Delhi, Govt. of India and Department of Environment, Govt. of West Bengal, are gratefully acknowledged. Authors are also grateful to the Forest Department, Govt. of West Bengal for assisting the research team in collecting data and providing all infrastructural facilities to reach the remote island. References 1 Robertson, A.I., leaf-burying crabs: Their influence on energy flow and export from mixed mangrove forests (Rhizophora spp.) in northeastern Australia. J. Exp. Mar. Biol. Ecol. 102 (1976) 237–248. 2 Kristensen, E., King, G.M., Holmer, M., Banta, G.T., Jensen, M.H., Hansen K. & Bussarawit, N., Sulfate reduction, acetate turnover and carbon metabolism in sediments of Ao Nam Bor mangrove, Phuket, Thailand. Mar. Ecol. Prog. Ser 109 (1994) 245–255. 3 Alongi, D.M, Zonation and seasonality of benthic primary production and community respiration in tropical mangrove forests. Oecologia 98 (1994a) 320–327. 4 Alongi, D.M, The role of bacteria in nutrient recycling in tropical mangrove and other coastalbenthic ecosystems. Hydrobiology 295 (1994b) 19–32. 5 Sahoo K & Dhal N K, Potential microbial diversity in mangrove ecosystems: A review of Indian J.Mar.Sci.,Vol. 38 (2) (2009) 249-256. 6 Holguin G., Bashan, Y,& Vazavez P., The role of sediment microorganism in the productivity, conservation and rehabilitation of mangrove ecosystem: An Overview. Biology of Fertile Soils, 33 (2001) 265-278. 7 Senior; E., Lindstrom, E.B., Banat, I. M.& Nedwell, D.B., Sulfate reduction and mathanogenesis in the sediment of a saltmarsh on the eastcoast of the United Kingdom. Applied Environmental Microbiology, 43 (1982) 987-996. 8 Thomas J. Lyimo, Arjan P., Huub J.M., & Op den Camp, Methane Emission, Sulphide Concentration and Redox Potential Profiles in Mtoni Mangrove Sediment, Tanzania Western Indian Ocean J. Mar. Sci. Vol. 1, No. 1,(2002) 71–80. 9 Mohanraju, R. & Natarajan, R., Methanogenic bacteria in mangrove sediment. Hydrobiologia, 247 (1992) 187-193. 10 Sana B, Ghosh D, Saha M, & Mukherjee J., Purification and characterization of a salt, Solvent, detergent and bleach tolerant protease from a new gamma-Proteobacterium isolated from the marine environment of the Sundarbans. Process Biochem. 41 (2006) 208–15. 11 Fathul K. S., Zaharer I, Adibah Y & Madzlan A., Isolation and Identification of Marine Sulfate Reducing Bacteria Desulfovibrio sp and Citrobacter freundii from Pasir Gudang, Malaysia. Sains Malyasiana 37 (4) (2008) 365-371. DAS et al.: DISTRIBUTION OF AEROBIC AND ANAEROBIC BACTERIA IN SUNDERBAN MANGROVE ECOSYSTEMS 12 Ramanathan A.L.,Singh,G., Majumder,J., Samal, A.C., Chowhan, R., Rayan, R.K., Roykumar, K.& Santra,S.C., A study of microbial diversity and its interaction with nutrients in the sediments of Sunderban mangroves. Indian Journal of Marine Science, 37 (2) (2008) 159-165. 13 Grasshoff, K, Determination of salinity and oxygen, pp. 31– 72 (Determination of nutrients, pp. 125–187). In: Grasshoff, K., Ehrhard, M., Kremling, K. (Eds.)1983, Methods of Seawater Analysis. Verlag Chemie, Weinheim. 14 Biswas H , Mukhopadhyay S K ,Sen S &. Jana TK .Spatial and temporal patterns of methane dynamics in the tropical mangrove dominated es(1992)tuary, NE coast of Bay of Bengal, India Journal of marine science vol:68 issue 1-2 (2007). 55-64. 15 Tam NFY, Wong AHY,Wong MH & Wong YS, Mass balance of nitrogen in constructed mangrove wetlands receiving ammonium-rich wastewater: Effects of tidal regime and carbon supply Ecological Engineering Vol:3 Issue-4 (2009) 453-462. 16 Mohanraju R &Natarajan R, Methanogenic bacteria in mangrove sediments. Hydrobiol., 247 (1992) 187-193. 17 Ramamurty T Raju R M &Natarajan R, Distribution and ecology of metbanogenic bacteria in mangrove sediment os pichavaram,east coast of India J.Mar.Sci., 19 (1990) 269-273. 18 T L Lyimo, D Mushi .Sulfide Concentration and Redox Potential Patterns in Mangrove Forests of Dar es Salaam: Effects on Avicennia Marina and Rhizophora Mucronata Seedling Establishment. Western Indian Ocean Journal of Marine Science vol-4 no-2 (2005) (163-173) 19 Nedwell D B, Blackburn T H &Wiebe WJ, Dynamic nature of the turnover of organic carbon, nitrogen and sulpher in the sediment of a Jamaican mangrove forest. Mar.Ecol.Prog.Ser.,110 9 (1994) 223-231. 411 20 Sherman R E, Fahey T J &Howarth R W, Soil –plany interaction in a neotropical mangrove forest: iron, phosphorus and sulpher dynamic. Oecologia, 115 (1998) 553-563. 21 Zuberer D A & Silver W S , Biological di-nitrogen fixation (Acetylene reduction) associated with Florida Mangrove. Appl. Environ. Microbiol ,35 (1978) 567-575. 22 Benner, R.A.E.Maccubbin & R.E.Hodson, Anaerobic biodegradation of the lignin and polysaccharide components of lignocellulose and synthetic lignin by sediment microflora. Appl. Environ. Microbiol. 47 (1984) 998-1004. 23 LEE, C. 1992. Controls on organic carbon preservation: The use of stratified water bodies to compare intrinsic rates of decomposition in oxic and anoxic systems. Geochim. Cosmochim. Acta 56: 3323-3335.) 24 Westrich J.T.,& R.A.Berner., The role of sedimentary organic matter in bacterial sulfate reduction. Limnol. Oceanogr .29 (1984) 236-249. 25 Lowe S E, Jain M K & Zeikus J G., Biology, ecology, and biotechnological applications of anaerobic bacteria adapted to environmental stresses in temperature, pH, salinity, or substrates. Microbiol Mol Biol Rev.; 57 (2) (1993) 451-509. 26 Lyimo T J, Pol A, Camp HJM Op den, Harhangi HR & Vogels GD., Methanosarcina semesiae sp. nov., a dimethylsulfide-utilizing methanogen from mangrove sediment. International Journal of Systematic and Evolutionary Microbiology, Vol 50, (2000) 171-178. 27 Rietz D N& Haynes R J, Effects of irrigation-induced salinity and sodicity on soil microbial activity Soil biology and biochemistry vol 35 (6) (2003) 845-854. 28 Kristensen E, Saiyed I. Ahmed,& Allan H, Aerobic and Anaerobic Decomposition of Organic Matter in Marine Sediment: Which isFastest? American Society of Limnology and Oceanography Vol. 40, (8) (1995) 1430-1437
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