Annual Variation in Soil Enzyme Activity in a Paddy Field: Soil Temperature and Nutrient Availability Are Important for Controlling Enzyme Activities

Kunito, Takashi; Shiroma, Takashi; Moro, Hitoshi; Sumi, Hirotaka

doi:https://doi.org/10.1155/2018/4093219

Applied and Environmental Soil Science

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Abstract Introduction Materials and Methods Results and Discussion Conclusions Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2018 | Article ID 4093219 | https://doi.org/10.1155/2018/4093219

Annual Variation in Soil Enzyme Activity in a Paddy Field: Soil Temperature and Nutrient Availability Are Important for Controlling Enzyme Activities

Takashi Kunito,¹Takashi Shiroma,¹Hitoshi Moro,¹and Hirotaka Sumi²

Academic Editor: Rafael Clemente

Received05 Jun 2018

Revised22 Aug 2018

Accepted19 Sept 2018

Published10 Oct 2018

Abstract

Annual variations in enzyme activities involved in carbon (C), nitrogen (N), phosphorus (P), and sulfur (S) cycling and soil physicochemical properties were examined in a Japanese paddy field. All the enzyme activities determined at the field soil temperature (range, 2.2°C–28.3°C) increased exponentially with soil temperature (). Significant negative correlations were found between Bray-2P concentration and the ratio of acid phosphatase to β-D-glucosidase activity (Spearman r = −0.631, p = 0.005) and between total N and the ratio of L-asparaginase to β-D-glucosidase activity (r = −0.612, ), suggesting that in accordance with the resource allocation model, acid phosphatase and L-asparaginase were synthesized by microorganisms depending on the temporal changes in soil P and N availability. These results suggest the significance of soil temperature in controlling in situ enzyme activities in paddy soil and also that the stoichiometry of enzyme activities associated with C, N, and P acquisition reflects the soil nutrient availability.

1. Introduction

Rice cultivation in paddy soils is a vital component of global agriculture [1, 2]; rice is the main staple food for more than half of the world’s population and it provides about 20% of the world’s dietary energy supply [3, 4]. Paddy soils experience temporal variation in redox conditions: paddy fields are kept flooded during the rice growing season, whereas they are drained during the nongrowing season. Variations in redox conditions cause complicated biogeochemical processes in paddy soils, mostly mediated by microorganisms [5–8], and lead to fluctuations in the soil nutrient availability [2]. The fluctuations in nutrient availability influence microbial activities in paddy soils, and vice versa.

Microorganisms produce various enzymes that are involved in organic matter degradation [9] and therefore influence nutrient cycling and soil fertility [10]. In spite of the significant roles of soil enzymes in nutrient cycling in paddy fields, limited information is available about the annual dynamics of enzyme activities and the factors controlling them in paddy soils. In the present study, we hypothesized that enzyme activities involved in carbon (C), nitrogen (N), phosphorus (P), and sulfur (S) cycling would vary according to the fluctuations in the soil nutrient availability caused by flooding and draining in paddy fields. The annual variations in enzyme activities and soil physicochemical properties were determined and compared to reveal possible links between them.

2. Materials and Methods

2.1. Soil Sampling

Soil samples were collected 18 times from November 2007 to October 2008 from a paddy field (1400 m²) in Matsumoto, Nagano Prefecture, Japan. The mean annual temperature was 11.8°C, and mean annual precipitation was 1,031 mm. The soil was classified as Gray Lowland soil in the Japanese system, which corresponds to Gleyic Fluvisol in the World Reference Base classification. The paddy field received cow manure (1.43 kg·m⁻²), compost (0.17 kg·m⁻²), and bone meal (0.04 kg·m⁻²) on May 1, 2008. The field was flooded on May 6, and rice seedlings were transplanted on May 17. The field remained flooded until late August and was then drained. The rice plants were harvested on September 25.

On each sampling date, soil sampling was conducted at around 2 p.m., and air and soil temperatures were measured in the paddy field. Soil samples were collected from five plots to 15 cm depth on each sampling occasion. After putting each sample into a polyethylene bag, air and water were removed from the bag, and then the samples were transported to the laboratory within 30 min after collection. Soil redox potential (Eh) and pH were measured for three soil samples as soon as possible; for the other measurements, the same amount of five soil samples were pooled and mixed together as a composite sample, and then they were stored at −80°C in bottles purged with N₂ gas until analysis.

2.2. Soil Physicochemical Analyses

Eh was measured as described in Onikura and Goto [11]. In brief, deoxygenated water was gently added to the wet soil, and then a Pt electrode was inserted into the soil. After leaving it to stand for 1 h under N₂ gas, Eh was determined using an Eh meter (PRN-41, Fujiwara Scientific Company, Tokyo, Japan) with a Pt-AgCl combination reference electrode. Soil pH was measured with a glass electrode in the water just above the soil. We did not correct the Eh for pH in this study, because there is a wide range of reported changes in Eh per unit of pH [12].

Acid-volatile sulfide (AVS) was measured by the cold-acid purge and trap technique described by Allen et al. [13]. AVS is defined as the reactive fraction of sulfide in soil that releases H₂S when exposed to cold HCl; it includes dissolved sulfide species and metastable iron sulfide minerals [14]. Briefly, the wet soil was treated with deoxygenated HCl, adjusted to a final concentration of 1 M, for 30 min in the reactor under a continuous flow of N₂ gas, and the evolved H₂S was trapped in 0.5 M NaOH. The sulfide content in the trap was measured by the methylene blue spectrophotometric technique. The recovery of sulfide added as Na₂S∙9H₂O to the reactor was 116.5 ± 19.6% (). Exchangeable manganese (Mn) was extracted from the wet soil with deoxygenated 0.05 M CaCl₂ for 24 h [15, 16] under N₂ gas and then determined with an atomic absorption spectrometer (Perkin Elmer 5100 PC, Tokyo, Japan). Mn was selected as a metal sensitive to soil reduction [17]. Modified Bray-2P was extracted from the wet soil using deoxygenated dilute acid fluoride (0.03 M NH₄F, 0.1 M HCl) at a 1 : 20 soil : solution ratio (w/v) [18]. Concentrations of inorganic P (Pi) in the extracts were determined by the ammonium molybdate-ascorbic acid method [19]. In the colorimetric determination of Pi for the extract of the modified Bray-2 test, fluoride can interfere with color formation, and thus boric acid was added to form noninterfering fluoroborate [18]. For total C and N measurements, air-dried soil samples were used; the amounts were determined using an NC analyzer (Thermo Finnigan Flash EA1112, Thermo Fisher Scientific, Waltham, MA, USA). These analyses were performed in triplicate for each sample, and the mean values are expressed on a dry weight basis.

2.3. Soil Enzyme Analyses

We measured soil enzyme activities involved in C, N, P, and S cycling in soils stored at −80°C. β-D-glucosidase activity was chosen as a representative C-acquiring enzyme because this enzyme is involved in hydrolysis of cellobiose, the main product in hydrolysis of cellulose by cellulases [20], and it was measured with p-nitrophenyl-β-D-glucopyranoside as the substrate in a modified universal buffer (MUB) (tris(hydroxymethyl)aminomethane, 2.42 g; maleic acid, 2.32 g; citric acid, 2.8 g; boric acid, 1.26 g; and distilled water, 1 L) at pH 6.0 [20]. L-asparaginase activity was measured with L-asparagine as the substrate in a phosphate buffer at pH 7.6 [21]. L-asparaginase was selected as the N-acquiring enzyme, because it was reported that among several N-acquiring enzymes, L-asparaginase was the most representative of the N availability in soils [22]. Acid phosphatase activity was determined as the P-acquiring enzyme with p-nitrophenyl phosphate as the substrate in a MUB at pH 6.5 [20], because this enzyme plays an important role in P cycling in soils (e.g., [23, 24]). Arylsulfatase activity, which is partly responsible for S cycling in soils [20], was chosen as a representative S-acquiring enzyme and was determined with p-nitrophenyl sulfate as the substrate in an acetate buffer at pH 5.8 [20]. These assays were conducted in triplicate at the field soil temperature when the soil was collected. A standard curve was prepared on each occasion of measurement. The activities are expressed on a dry weight basis.

3. Results and Discussion

3.1. Annual Variations in Soil Physicochemical Properties

The lowest soil temperature (2.2°C) was observed on February 24, and the highest (28.3°C) was recorded on August 8 (Figure 1). Soil total C and N contents were slightly elevated during June and July. This increase might reflect a large input of organic matter through rice plants [25] and algae [26] in this period. Some soil physicochemical properties were drastically changed by water management practices. Soil Eh began to decrease after flooding on May 6 because of the oxygen depletion and stayed stable (−11 ± 31 mV to 53 ± 34 mV) under the flooded condition. Simultaneously with the decline in Eh, exchangeable Mn and Bray-2P concentrations and pH increased in the soil. The increase in pH with reduction in soil Eh is a well-known phenomenon (e.g., [16, 27]), which is caused by proton consumption through the formation of various reductants [28]: Ox + ne⁻ + mH⁺ = Red + (m/2)H₂O, where Ox is the oxidized species and Red is the reduced species, and m and n are stoichiometric factors. The increase in exchangeable Mn concentration with reduction in soil Eh results from the reduction of Mn(IV) oxides to Mn(II) primarily by microorganisms [5, 29]. An increase in Bray-P concentration by soil flooding was also reported in other studies [30, 31, 32]. Such an enhancement of P availability has long been known in flooded paddy soils (e.g., [33, 34], primarily caused by the reduction of Fe(III) compounds holding P on their surfaces and by reduction of insoluble ferric phosphate to more soluble ferrous phosphate [2, 35]).

(a)

(b)

(c)

(d)

(e)

(f)

(g)

On September 28, a steep rise in Eh concurrent with soil draining caused a rapid drop in Bray-2P concentration from 119 ± 5 to 68 ± 1 µg·P·g⁻¹ (Figure 1). In contrast, exchangeable Mn concentration declined gradually with soil oxidation, and an increased concentration of exchangeable Mn was still observed on October 9. Gotoh and Yamashita [36] and Phillips [37] also observed the slow reoxidation of Mn(II) formed in the reduced soil. These results indicate that Mn(IV) oxides are rapidly reduced by flooding, but the reoxidation of Mn(II) seems to be slow during the oxidation of anoxic soils. In stark contrast, the AVS concentration increased very slowly after flooding (beginning a month later than that of exchangeable Mn and Bray-2P) and decreased sharply from 66.4 ± 2.8 to 9.2 ± 3.3 µg·g⁻¹ on September 9, more than a month ahead of the decline of exchangeable Mn. This behavior of AVS can be explained by the low Eh (<0 mV) at which sulfide is formed through microbial respiratory sulfate reduction [5] and by the rapid oxidation of sulfide via some oxidizable substances [13].

3.2. Soil Enzyme Activities

In this study, enzyme activities were determined at the field soil temperature when the soil was collected to reflect the annual changes of in situ activity in the paddy field. All the activities of four enzymes were high in summer (Figure 2(a)) and increased exponentially with soil temperature (Figure 3). Because soil temperature correlated positively with total C, total N, Bray-2P, and pH and negatively with Eh, most of these variables also correlated with enzyme activities (Table 1). However, these correlations were weaker than those between soil temperature and enzyme activities. These results might imply that soil temperature had a larger influence on in situ enzyme activities than flooding.

(a)

(b)

Figure 2

Annual variations in enzyme activities involved in C, N, P, and S cycling (a) and the ratios of N-, P-, and S-acquiring enzymes to β-D-glucosidase activity (b). (a) Filled triangle, arylsulfatase (µmol p-nitrophenol g⁻¹·h⁻¹); open circle, L-asparaginase (µmol NH₄⁺-N g⁻¹·h⁻¹); filled circle, acid phosphatase (µmol p-nitrophenol g⁻¹·h⁻¹); open triangle, β-D-glucosidase (µmol p-nitrophenol g⁻¹·h⁻¹). (b) Open circle, ratio of L-asparaginase to β-D-glucosidase activity; filled triangle, ratio of arylsulfatase to β-D-glucosidase activity; filled circle, ratio of acid phosphatase to β-D-glucosidase activity. Data points represent means, and the error bars represent standard deviations.

(a)

(b)

(c)

(d)

The effects of season and flooding/draining condition on the enzyme pool might be small in the paddy field, because the exponential relationship between enzyme activities and soil temperature (Figure 3) could be explained by temperature sensitivity of the structure and catalytic activity of the enzyme itself [38], which is described from first principles of thermodynamics. Inconsistent results have been reported regarding the effects of flooding and season on enzyme activities among soils and among enzymes in laboratory soil incubation studies [39, 40, 41] and field studies [42, 43]. Ishida and Shiraishi [42] found elevated levels of saccharase but similar levels of amylase activities under flooded conditions in summer compared with those under drained conditions in winter in a paddy field, whereas Kanazawa [43] reported a slight decrease in β-D-glucosidase and N-acetyl-β-glucosaminidase activities during the flooded period when compared with other periods in a paddy field (in both studies, enzyme activities were measured at a single reference temperature, not at the field soil temperature). High enzyme activity during the flooded period might be the result of the large input of organic matter from rice plants and algae as mentioned above. The decreased activity associated with flooding would not be related to the disappearance of O₂ because of the insensitivity of hydrolase to O₂ levels [44] but might be caused by the accumulation of phenolic compounds in the flooded paddy soil [44–46]. Alternatively, the decreases in the enzyme activities under flooded conditions might be a consequence of decreased microbial biomass size [39]. Further studies are necessary to understand the influence of flooding and season on enzyme activities and pools in paddy fields.

Variation in the stoichiometry of enzyme activities associated with nutrient acquisition can be explained by the resource allocation model for extracellular enzyme synthesis [47, 48] in which microorganisms will preferentially allocate their resources to enzymes for acquiring an element limiting their productivity. In aerobic agricultural and forest soils, the ratio of phosphatase to β-D-glucosidase activity and the ratio of L-asparaginase to β-D-glucosidase activity reflect P [49, 50] and N [22, 50] bioavailability, respectively. Thus, in the present study, we determined these enzyme ratios to evaluate annual variation in bioavailability of nutrients in the paddy field. The ratios of L-asparaginase to β-D-glucosidase activity and arylsulfatase to β-D-glucosidase activity exhibited similar temporal patterns: these ratios were generally higher in winter than in summer (Figure 2). In contrast, annual variation in the ratio of acid phosphatase to β-D-glucosidase activity was small. In agreement with the results of aerobic agricultural and forest soils [22, 49, 50], significant negative correlations were observed between Bray-2P concentration and the ratio of acid phosphatase to β-D-glucosidase activity (Spearman r = −0.631, ) and between total N and the ratio of L-asparaginase to β-D-glucosidase activity (r = −0.612, ; Figure 4), which were comparable to those in previous studies. Therefore, it is suggested that acid phosphatase and L-asparaginase were synthesized by microorganisms depending on the temporal changes in soil P and N availability, although the microbial community, in particular the active microbial community, is known to vary substantially with redox conditions in paddy soils [5, 7, 51].

(a)

(b)

4. Conclusions

Exchangeable Mn, Bray-2P, and AVS concentrations and pH increased as the soil became more reduced under flooded conditions, and vice versa under drained conditions in the paddy field. Contrasting behavior was observed between exchangeable Mn and AVS: the exchangeable Mn concentration increased simultaneously with the decline in Eh after flooding and declined gradually with soil oxidation after draining, whereas the AVS concentration increased very slowly after flooding and decreased sharply after draining. Enzyme activities determined at the field soil temperature were high in summer, with the activity increasing exponentially with soil temperature. The ratio of acid phosphatase to β-D-glucosidase activity increased with a decrease in Bray-2P concentration and the ratio of L-asparaginase to β-D-glucosidase activity increased with a decrease in total N, indicating that acid phosphatase and L-asparaginase were synthesized by microorganisms depending on the temporal changes in soil P and N availabilities, although the microbial community is known to vary substantially with redox conditions in paddy soils. These results suggest the significance of soil temperature in controlling in situ enzyme activities in the paddy soil and also that the stoichiometry of extracellular enzyme activity associated with C, N, and P acquisition reflects the soil nutrient availability. Further studies are needed to confirm the usefulness of the stoichiometry of extracellular enzyme activity as an index of nutrient availability in paddy soils.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This study was supported by the Management Expenses Grant from Shinshu University.

References

N. K. Fageria, N. A. Slaton, and V. C. Baligar, “Nutrient management for improving lowland rice productivity and sustainability,” Advances in Agronomy, vol. 80, pp. 63–152, 2003.
View at: Publisher Site | Google Scholar
K. Kyuma, Paddy Soil Science, Kyoto University Press, Kyoto, Trans Pacific Press, Melbourne, Australia, 2004.
FAO, The International Year of Rice 2004: Concept Paper, FAO, Rome, Italy, 2003.
FAO, Rice and Human Nutrition, FAO, Rome, Italy, 2004.
M. Kimura, “Anaerobic microbiology in waterlogged rice fields,” in Soil Biochemistry, J.–M. Bollag and G. Stotzky, Eds., vol. 10, pp. 35–138, Marcel Dekker, New York, NY, USA, 2000.
View at: Google Scholar
I. Kögel-Knabner, W. Amelung, Z. Cao et al., “Biogeochemistry of paddy soils,” Geoderma, vol. 157, no. 1-2, pp. 1–14, 2010.
View at: Publisher Site | Google Scholar
I. Watanabe and C. Furusaka, “Microbial ecology of flooded rice soils,” in Advances in Microbial Ecology, M. Alexander, Ed., vol. 4, pp. 125–168, Plenum Press, New York, NY, USA, 1980.
View at: Google Scholar
T. Yoshida, “Microbial metabolism of flooded soils,” in Soil Biochemistry, E. A. Paul and A. D. McLaren, Eds., vol. 3, pp. 83–122, Marcel Dekker, New York, NY, USA, 1975.
View at: Google Scholar
M. D. Wallenstein and R. G. Burns, “Ecology of extracellular enzyme activities and organic matter degradation in soil: a complex community-driven process,” in Methods of Soil Enzymology, R. P. Dick, Ed., pp. 35–55, Soil Science Society of America, Madison, WI, USA, 2011.
View at: Google Scholar
R. P. Dick, “Soil enzyme activities as integrative indicators of soil health,” in Biological Indicators of Soil Health, C. E. Pankhurst, B. M. Doube, and V. V. S. R. Gupta, Eds., pp. 121–156, CAB International, Wallingford, UK, 1997.
View at: Google Scholar
Y. Onikura and S. Goto, “Soil redox potential,” in Analytical Methods for Soil Nutrients, Committee for Analytical Methods for Soil Nutrients, Ed., pp. 53–69, Yokendo, Tokyo, Japan, 1970, in Japanese.
View at: Google Scholar
K. R. Reddy and R. D. DeLaune, Biogeochemistry of Wetlands: Science and Applications, CRC Press, Boca Raton, FL, USA, 2008.
H. E. Allen, G. Fu, and B. Deng, “Analysis of acid-volatile sulfide (AVS) and simultaneously extracted metals (SEM) for the estimation of potential toxicity in aquatic sediments,” Environmental Toxicology and Chemistry, vol. 12, no. 8, pp. 1441–1453, 1993.
View at: Publisher Site | Google Scholar
J. W. Morse and D. Rickard, “Chemical dynamics of sedimentary acid volatile sulfide,” Environmental Science and Technology, vol. 38, no. 7, pp. 131A–136A, 2004.
View at: Publisher Site | Google Scholar
T. Kunito, K. Saeki, H. Oyaizu, and S. Matsumoto, “Influences of copper forms on the toxicity to microorganisms in soils,” Ecotoxicology and Environmental Safety, vol. 44, no. 2, pp. 174–181, 1999.
View at: Publisher Site | Google Scholar
T. Kunito, H. Toya, H. Sumi et al., “Evaluating the effects of metals on microorganisms in flooded paddy soils using the SEM/AVS-based approach and measurements of exchangeable metal concentrations,” Archives of Environmental Contamination and Toxicology, vol. 72, no. 3, pp. 402–417, 2017.
View at: Publisher Site | Google Scholar
Y. Takai and T. Kamura, “The mechanism of reduction in waterlogged paddy soil,” Folia Microbiologica, vol. 11, no. 4, pp. 304–313, 1966.
View at: Publisher Site | Google Scholar
M. Nanzyo, “Available phosphorus,” in Analytical Methods for Soil Environment, Editorial Committee for Analytical Methods for Soil Environment, Ed., pp. 267–273, Hakuyusha, Tokyo, Japan, 1997, in Japanese.
View at: Google Scholar
J. Murphy and J. P. Riley, “A modified single solution method for the determination of phosphate in natural waters,” Analytica Chimica Acta, vol. 27, pp. 31–36, 1962.
View at: Publisher Site | Google Scholar
M. A. Tabatabai, “Soil enzymes,” in Methods of Soil Analysis, Part 2, Microbiological and Biochemical Properties, R. W. Weaver, S. Angle, P. Bottomley et al., Eds., pp. 775–833, Soil Science Society of America, Madison, WI, USA, 1994.
View at: Google Scholar
S. Kanazawa and H. Kiyota, “Estimation of L-glutaminase and L-asparaginase activities in soils by the indophenol method,” Soil Science and Plant Nutrition, vol. 41, no. 2, pp. 305–311, 1995.
View at: Publisher Site | Google Scholar
K. Fujita, T. Kunito, J. Matsushita et al., “Nitrogen supply rate regulates microbial resource allocation for synthesis of nitrogen-acquiring enzymes,” PLoS One, vol. 13, no. 8, Article ID e0202086, 2018.
View at: Publisher Site | Google Scholar
T. Kunito, M. Tsunekawa, S. Yoshida et al., “Soil properties affecting phosphorus forms and phosphatase activities in Japanese forest soils: soil microorganisms may be limited by phosphorus,” Soil Science, vol. 177, no. 1, pp. 39–46, 2012.
View at: Publisher Site | Google Scholar
T. Kunito, T. Tobitani, H. Moro, and H. Toda, “Phosphorus limitation in microorganisms leads to high phosphomonoesterase activity in acid forest soils,” Pedobiologia, vol. 55, no. 5, pp. 263–270, 2012.
View at: Publisher Site | Google Scholar
Y. Lu, A. Watanabe, and M. Kimura, “Input and distribution of photosynthesized carbon in a flooded rice soil,” Global Biogeochemical Cycles, vol. 16, no. 4, p. 1085, 2002.
View at: Publisher Site | Google Scholar
T. Yamagishi, J. Watanabe, K. Okada, T. Hayashi, A. Kumura, and Y. Murata, “Cycling of carbon in a paddy field. II. Biomass and gross production of algae,” Japanese Journal of Crop Science, vol. 49, no. 1, pp. 146–155, 1980.
View at: Publisher Site | Google Scholar
H. Sumi, T. Kunito, Y. Ishikawa, K. Nagaoka, H. Toda, and Y. Aikawa, “Effects of adding alkaline material on the heavy metal chemical fractions in soil under flooded and non-flooded conditions,” Soil and Sediment Contamination: An International Journal, vol. 23, no. 8, pp. 899–916, 2014.
View at: Publisher Site | Google Scholar
G. Sposito, The Chemistry of Soils, Oxford University Press, New York, NY, USA, 2nd edition, 2008.
F. N. Ponnamperuma, “The chemistry of submerged soils,” Advances in Agronomy, vol. 24, pp. 29–96, 1972.
View at: Publisher Site | Google Scholar
J. Bradley, I. Vimpany, and P. J. Nicholls, “Effects of waterlogging and subsequent drainage of a pasture soil on phosphate sorption, extractable phosphate and oxalate-extractable iron,” Australian Journal of Soil Research, vol. 22, no. 4, pp. 455–461, 1984.
View at: Publisher Site | Google Scholar
H. Shiga, “Effect of phosphorus fertility of soils and phosphate application on rice culture in cool region. Part 1. Measurement of phosphorus supplying ability of paddy soils,” Research Bulletin of the Hokkaido National Agricultural Experiment Station, vol. 105, pp. 31–49, 1973.
View at: Google Scholar
T. S. Verma and B. R. Tripathi, “Evaluation of chemical methods for the determination of available phosphorus in waterlogged Alfisols: 1. Phosphate-availability indices in relation to phosphate fractions,” Soil Science, vol. 134, no. 4, pp. 258–264, 1982.
View at: Publisher Site | Google Scholar
M. Aoki, “Studies on the behavior of soil phosphoric acid under paddy field condition (I),” Journal of the Science of Soil and Manure, vol. 15, pp. 182–201, 1941, in Japanese.
View at: Google Scholar
W. H. Patrick Jr. and I. C. Mahapatra, “Transformation and availability to rice of nitrogen and phosphorus in waterlogged soils,” Advances in Agronomy, vol. 20, pp. 323–359, 1968.
View at: Publisher Site | Google Scholar
G. Kirk, The Biogeochemistry of Submerged Soils, John Wiley & Sons, Chichester, UK, 2004.
S. Gotoh and K. Yamashita, “Oxidation-reduction potential of a paddy soil in situ with special reference to the production of ferrous iron, manganous manganese and sulfide,” Soil Science and Plant Nutrition, vol. 12, no. 6, pp. 230–238, 1966.
View at: Publisher Site | Google Scholar
I. R. Phillips, “Phosphorus availability and sorption under alternating waterlogged and drying conditions,” Communications in Soil Science and Plant Analysis, vol. 29, no. 19-20, pp. 3045–3059, 1998.
View at: Publisher Site | Google Scholar
M. Wallenstein, S. D. Allison, J. Ernakovich, J. M. Steinweg, and R. Sinsabaugh, “Controls on the temperature sensitivity of soil enzymes: a key driver of in situ enzyme activity rates,” in Soil Enzymology, G. Shukla and A. Varma, Eds., pp. 245–258, Springer-Verlag, Berlin, Germany, 2011.
View at: Google Scholar
G. P. McLatchey and K. R. Reddy, “Regulation of organic matter decomposition and nutrient release in a wetland soil,” Journal of Environmental Quality, vol. 27, no. 5, pp. 1268–1274, 1998.
View at: Publisher Site | Google Scholar
I. D. Pulford and M. A. Tabatabai, “Effect of waterlogging on enzyme activities in soils,” Soil Biology and Biochemistry, vol. 20, no. 2, pp. 215–219, 1988.
View at: Publisher Site | Google Scholar
X.-C. Wang and Q. Lu, “Effect of waterlogged and aerobic incubation on enzyme activities in paddy soil,” Pedosphere, vol. 16, no. 4, pp. 532–539, 2006.
View at: Publisher Site | Google Scholar
H. Ishida and M. Shiraishi, “Enzyme activity in paddy soils,” Soil Microorganisms, vol. 20, pp. 11–18, 1978, in Japanese.
View at: Google Scholar
S. Kanazawa, “Soil enzyme in paddy soil,” Pedologist, vol. 24, pp. 69–93, 1980, in Japanese.
View at: Google Scholar
C. Freeman, N. Ostle, and H. Kang, “An enzymic “latch” on a global carbon store,” Nature, vol. 409, p. 149, 2001.
View at: Publisher Site | Google Scholar
N. Fenner and C. Freeman, “Drought-induced carbon loss in peatlands,” Nature Geoscience, vol. 4, no. 12, pp. 895–900, 2011.
View at: Publisher Site | Google Scholar
N. Fenner and C. Freeman, “Carbon preservation in humic lakes; a hierarchical regulatory pathway,” Global Change Biology, vol. 19, no. 3, pp. 775–784, 2013.
View at: Publisher Site | Google Scholar
R. L. Sinsabaugh and J. J. Follstad Shah, “Ecoenzymatic stoichiometry and ecological theory,” Annual Review of Ecology, Evolution, and Systematics, vol. 43, no. 1, pp. 313–343, 2012.
View at: Publisher Site | Google Scholar
R. L. Sinsabaugh and D. L. Moorhead, “Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition,” Soil Biology and Biochemistry, vol. 26, no. 10, pp. 1305–1311, 1994.
View at: Publisher Site | Google Scholar
K. Fujita, T. Kunito, H. Moro, H. Toda, S. Otsuka, and K. Nagaoka, “Microbial resource allocation for phosphatase synthesis reflects the availability of inorganic phosphorus across various soils,” Biogeochemistry, vol. 136, no. 3, pp. 325–339, 2017.
View at: Publisher Site | Google Scholar
H. Moro, T. Kunito, and T. Sato, “Assessment of phosphorus bioavailability in cultivated Andisols from a long-term fertilization field experiment using chemical extractions and soil enzyme activities,” Archives of Agronomy and Soil Science, vol. 61, no. 8, pp. 1107–1123, 2015.
View at: Publisher Site | Google Scholar
H. Itoh, S. Ishii, Y. Shiratori et al., “Seasonal transition of active bacterial and archaeal communities in relation to water management in paddy soils,” Microbes and Environments, vol. 28, no. 3, pp. 370–380, 2013.
View at: Publisher Site | Google Scholar

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Copyright © 2018 Takashi Kunito et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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