Extracellular enzyme kinetics scale with resource availability

Biogeochemistry

Volumn 121, Issue 2, 2014, Pages 287-304

  Sinsabaugh, Robert L ^a   Belnap, Jayne ^b   Findlay, Stuart G ^c   Shah, Jennifer J Follstad ^d   Hill, Brian H ^e   Kuehn, Kevin A ^f   Kuske, Cheryl R ^g   Litvak, Marcy E ^a   Martinez, Noelle G ^a   Moorhead, Daryl L ^h   Warnock, Daniel D ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b DENVER FEDERAL CENTER   (United States)

^c CARY INSTITUTE OF ECOSYSTEM STUDIES   (United States)

^d UTAH STATE UNIVERSITY   (United States)

^e U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^f University of Southern Mississippi   (United States)

^g LOS ALAMOS NATIONAL LABORATORY   (United States)

^h UNIVERSITY OF TOLEDO   (United States)

Author keywords

Ecological stoichiometry; Enzyme kinetics; Extracellular enzymes; Microbial community; Microbial metabolism

Indexed keywords

BIOGEOCHEMISTRY; ENZYME ACTIVITY; HOMEOSTASIS; MICROBIAL COMMUNITY; ORGANIC CARBON; REACTION KINETICS; RESOURCE AVAILABILITY; STOICHIOMETRY;

EID: 84918514518     PISSN: 01682563     EISSN: 1573515X     Source Type: Journal    
DOI: 10.1007/s10533-014-0030-y     Document Type: Article

References (95)

1. Abdelmagid HM, Tabatabai MA (1987) Nitrate reductase activity in soils. Soil Biol Biochem 19:421–428
2. Abichou T, Mahieu K, Chanton J, Romdhane M, Mansouri I (2011) Scaling methane oxidation: from laboratory incubation experiments to landfill cover field conditions. Waste Manag 31:978–986
3. Acosta-Martinez V, Tabatabai MA (2000) Arylamidase activity in soil. Soil Sci Soc Am J 64:215–221
4. Akatsuka T, Mitamura O (2011) Response of denitrification rate associated with wetting and drying cycles in a littoral wetland area of Lake Biwa, Japan. Limnology 12:127–135
5. Allison SD (2005) Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol Lett 8:626–635
6. Bar-Even A, Noor E, Savir Y, Liebermeister W, Davidi D, Tawfik DS, Milo R (2011) The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50:4402–4410
7. Bartholemew GW, Alexander M (1981) Soil as a sink for atmospheric carbon monoxide. Science 212:1389–1391
8. Bender M, Conrad R (1993) Kinetics of methane oxidation in oxic soils. Chemosphere 26:687–696
9. Burns RG, DeForest JL, Marxsen JC, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MH, Zoppini A (2013) Soil enzyme research: current knowledge and future directions. Soil Biol Biochem 58:216–234
10. Cartes P, Jara AA, Demanet R, de la Luz Mora M (2009) Urease activity and nitrogen mineralization kinetics as affected by temperature and urea input rate in sourthern Chilean andisols. J Plant Sci Plant Nut 9:69–82
11. Christian JR, Karl DM (1998) Ectoaminopeptidase specificity and regulation in Antarctic marine pelagic microbial communities. Aquatic Microb Ecol 15:303–310
12. Chróst RJ, Riemann B (1994) Storm-stimulated enzymatic decomposition of organic matter in benthic/pelagic coastal mesocosms. Mar Ecol Prog Series 108:185–192
13. Cleveland CC, Liptzin D (2007) C:N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252
14. Cornish-Bowden A (2012) Fundamentals of Enzyme Kinetics, 4th edn. Wiley-Blackwell, Weinheim
15. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappinscott HM (1995) Microbial biofilms. Annu Rev Microb 49:711–745
16. Deng SP, Tabatabai MA (1994) Cellulase activity of soils. Soil Biol Biochem 26:1347–1354
17. Dote Y (2002) Kinetics of CH4 oxidation in mixed culture. Waste Manag Res 20:494–500
18. Dubey SK, Sinha ASK, Singh JS (2000) Spatial variation in the capacity of soil for CH4 uptake and population size of methane oxidizing bacteria in dry-land rice agriculture. Curr Sci 78:617–620
19. Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606
20. Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbors. FEMS Microb Rev 36:990–1004
21. Fanin N, Fromin N, Buatois B, Hattenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter–microbe system. Ecol Lett 16:764–772
22. Farrell RE, Gupta VVSR, Germida JJ (1994) Effects of cultivation on the activity and kinetics of arylsulfatase in Saskatchewan soils. Soil Biol Biochem 26:1033–1040
23. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microb 10:538–550
24. Fontigny A, Billen G, Vives-Rigo J (1987) Some kinetic characteristics of exoproteolytic activity in coastal seawater. Estuarine Coastal and Shelf Sci 25:127–133
25. Foreman CM, Franchini P, Sinsabaugh RL (1998) The trophic dynamics of riverine bacterioplankton: relationships among substrate availability, ectoenzyme kinetics and growth. Limnol Oceanogr 43:1344–1352
26. Frankenberger WT, Tabatabai MA (1980) Amidase activity in soils: II kinetic parameters. Soil Sci Soc Am J 44:532–536
27. Frankenberger WT, Tabatabai MA (1991a) L-asparaginase activity of soils. Biol Fertility of Soils 11:6–12
28. Frankenberger WT, Tabatabai MA (1991b) L-glutaminase activity of soils. Soil Biol Biochem 23:869–874
29. German DP, Marcelo KRB, Stone MM, Allison SD (2012) The Michaelis-Menten kinetics of soil extracellular enzymes in response to temperature: a cross-latitudinal study. Global Change Biol 18:1468–1479
30. Grandy AS, Sinsabaugh RL, Neff JC, Stursova M, Zak DR (2008) Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry 91:37–49
31. Guo R, Conrad R (2008) Extraction and characterization of soil hydrogenases oxidizing atmospheric hydrogen. Soil Biol Biochem 40:1149–1154
32. Hashimoto LK, Kaplan WA, Wofsy SC, McElroy MB (1983) Transformations of fixed nitrogen and N2O in the Cariaco Trench. Deep Sea Res 30:575–590
33. Hill BH, Elonen CM, Seifert LR, May AA, Tarquinio A (2012) Microbial enzyme stoichiometry and nutrient limitation in US streams and rivers. Ecol Indic 18:540–551
34. Hill BH, Elonen CM, Anderson LE, Lehter JC (2014a) Microbial respiration and ecoenzyme activity in sediments from the Gulf of Mexico hypoxic zone. Aquatic Microb Ecol 72:105–116
35. Hill BH, Elonen CM, Jicha TM, Kolka RK, Lehto LLP, Sebestyen SD, Seifert-Monson LR (2014b) Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry. doi:10.1007/s10533-014-9991-0
36. Hobbie JE, Hobbie EA (2012) Amino acid cycling in planktonic and soil microbes studied with radioisotopes: measured amino acids in soil do not reflect bioavailability. Biogeochemistry 107:339–360
37. Hobbie JE, Hobbie EA (2013) Microbes in nature are limited by carbon and energy: the starving survival lifestyle in soils and consequences for estimating microbial rates. Frontiers in Microbiol 4 article 324
38. 2O reduction. Soil Biol Biochem 32:833–843
39. Horz H-P, Raghubanshi AS, Heyer J, Kammann C, Conrad R, Dunfield PF (2002) Activity and community structure of methane-oxidising bacteria in a wet meadow soil. FEMS Microb Ecol 41:247–257
40. Huang YL, Zeng YH, Yu ZL, Zhang J, Feng H, Lin XC (2013) In silico and experimental methods revealed highly diverse bacteria with quorum sensing and aromatics biodegradation systems: a potential broad application on bioremediation. Biores Technol 148:311–316
41. Hwang S-J, Havens KE, Steinman AD (1998) Activity and community structure of methane-oxidising bacteria in a wet meadow soil. Freshw Biol 40:729–745
42. Juan YH, Chen LJ, Wu ZJ, Wang R (2009) Kinetics of soil urease affected by urease inhibitors at contrasting moisture regimes. J Plant Sci Plant Nut 9:125–133
43. Kaiser C, Franklin O, Dieckmann U, Richter A (2014) Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol Lett. doi:10.1111/ele.12269
44. Kempes C, Dutkiewicz S, Follows M (2012) Growth, metabolic partitioning, and the size of microorganisms. Proc Natl Acad Sci 109:495–500
45. King GM (1999) Attributes of atmospheric carbon monoxide oxidation by Maine forest soils. Appl Environ Microbiol 65:5257–5264
46. Kirkby CA, Kirkegaard JA, Richardson AE, Wade LJ, Blanchard C, Batten G (2011) Stable soil organic matter: a comparison of stable C:N:P: S ratios in Australian and other world soils. Geoderma 163:197–208
47. Klipp E, Heinrich R (1994) Evolutionary optimization of enzyme kinetic parameters; effect of constraints. J Theor Biol 171:309–323
48. Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106
49. Manzoni S, Schaeffer SM, Katul G, Porporato A, Schimel JP (2014) A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils. Soil Biol Biochem 73:69–83
50. Martiny AC, Vrugt JA, Primeau FW, Lomas MW (2013) Regional variation in the particulate organic carbon to nitrogen ratio in the surface ocean. Global Biogeochem Cycles 27:723–731
51. Marx M-C, Wood M, Jarvis SC (2001) A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol Biochem 33:1633–1640
52. Marx M-C, Kandeler E, Wood M, Wermbter N, Jarvis SC (2005) Exploring the enzymatic landscape: distribution and kinetics of hydrolytic enzymes in soil particle-size fractions. Soil Biol Biochem 37:35–48
53. McCarthyl JJ, Garside C, Nevins JL (1992) Nitrate supply and phytoplankton uptake kinetics in the euphotic layer of a Gulf stream warm-core ring. Deep Sea Res 39:S393–S403
54. McLaren AD (1978) Kinetics and consecutive reactions of soil enzymes. In: Burns RG (ed) soil enzymes. Academic Press, New York, pp 97–116
55. Michaelis L, Menten MI (1913) Die Kinetik der Invertinwirkung. Biochemische Zeitschrift 49:333–369
56. Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174
57. Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities balancing microbial demands during decomposition. Soil Biol Biochem 53:131–141
58. Moscatelli MC, Lagomarsino A, Garzillo AMV, Pignatora A, Grego S (2012) β-Glucosidase kinetic parameters as indicators of soil quality under conventional and organic cropping systems applying two analytical approaches. Ecol Indic 13:332–337
59. Münster U (1994) Studies on phosphatase activities in humic lakes. Environ Int 20:49–59
60. Nannipieri P, Gelsomino A, Felici M (1991) Method to determine guaiacol oxidase activity in soil. Soil Sci Soc Am J 55:1347–1352
61. Nedoma J, Van Wambeke F, Strojsova A, Strojsova M, Duhamel S (2007) Affinity of extracellular phosphatases for ELF97 phosphate in aquatic environments. Mar Freshw Res 58:454–460
62. Nor YM (1982) Soil urease activity and kinetics. Soil Biol Biochem 14:63–65
63. Olson RJ (1981) 15 N tracer studies of the primary nitrite maximum. J Mar Res 39:203–226
64. Quiquampoix H, Servagent-Noinville S, Baron M-H (2002) Enzyme adsorption on soil mineral surfaces and consequences for catalytic activity. In: Burns RG, Dick RP (eds) Enzymes in the environment. Marcel Dekker, New York, pp 285–306
65. Rath J, Schiller C, Herndl GJ (1993) Ectoenzymatic activity and bacterial dynamics along a trophic gradient in the Caribbean Sea. Mar Ecol Prog Series 102:89–96
66. Rich JJ, King GM (1999) Carbon monoxide consumption and production by wetland peats. FEMS Microb Ecol 28:215–224
67. Saliot A, Cauwet G, Cahet G, Mazaudier D, Daumas R (1996) Microbial activities in the Lena River delta and Laptev Sea. Mar Chem 53:247–254
68. Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563
69. Seip KL, Reynolds CS (1995) Phytoplankton functional attributes along trophic gradient and season. Limnol Oceanogr 40:589–597
70. Senwo ZN, Tabatabai MA (1996) Aspartase activity of soils. Soil Sci Soc Am J 60:1416–1422
71. Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–342
72. Sinsabaugh RL, Findlay S, Franchini P, Fischer D (1997) Enzymatic analysis of riverine bacterioplankton production. Limnol Oceanogr 42:29–38
73. Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop M, Wallenstein M, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264
74. Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798
75. Sinsabaugh RL, Follstad Shah JJ, Hill BH, Elonen CM (2012) Ecoenzymatic stoichiometry of stream sediments with comparison to terrestrial soils. Biogeochemistry 111:455–467
76. Siuda W, Chróst RJ (2002) Decomposition and utilization of particulate organic matter by bacteria in lakes of different trophic status. Polish J Environ Studies 11:53–65
77. Siuda W, Kiersztyn B, Chróst RJ (2007) The dynamics of protein decomposition in lakes of different trophic status—reflections on the assessment of the real proteolytic activity in situ. J Microb Biotechnol 17:897–904
78. Somville M, Billen G (1983) A method for determining exoproteolytic activity in natural waters. Limnol Oceanogr 28:190–193
79. Sorrell BK, Downes MT, Stanger CL (2002) Methanotrophic bacteria and their activity on submerged aquatic macrophytes. Aquat Bot 72:107–119
80. Stark JM, Firestone MK (1996) Kinetic characteristics of ammonium-oxidizer communities in a California oak woodland-annual grassland. Soil Biol Biochem 28:1307–1317
81. Stone MM, Plante AF (2014) Changes in phosphatase kinetics with soil depth across a variable tropical landscape. Soil Biol Biochem 71:61–67
82. Stone MM, Weiss MS, Goodale CL, Adams MB, Fernandez IJ, German DP, Allison SD (2012) Temperature sensitivity of soil enzyme kinetics under N-fertilization in two temperate forests. Global Change Biol 18:1173–1184
83. Strickland MS, McCulley RL, Bradford MA (2013) The effect of a quorum-quenching enzyme on leaf litter decomposition. Soil Biol Biochem 64:65–67
84. Tabatabai MA, Garcia-Manzanedo AM, Acosta-Martinez V (2002) Substrate specificity of arylamidase in soils. Soil Biol Biochem 34:103–110
85. Thompson A, Sinsabaugh RL (2000) Matric and particulate phosphatase and leucine aminopeptidase activity in limnetic biofilms. Aquatic Microb Ecol 21:151–159
86. Toetz DW, Varga LP, Loughran ED (1973) Half-saturation constants for uptake of nitrate and ammonia by reservoir plankton. Ecology 54:903–908
87. Vega LM, Alvarez PJ, McLean RJC (2014) Bacterial signaling ecology and potential applications during aquatic biofilm construction. Microb Ecol 68:24–44
88. Wagai R, Kishimoto-Mo AW, Yonemura S, Shirato Y, Hiradate S, Yagasaki Y (2013) Linking temperature sensitivity of soil organic matter decomposition to its molecular structure, accessibility, and microbial physiology. Global Change Biol 19:1114–1125
89. Westerhoff HV, Hellingworth KJ, Van Dam K (1983) Thermodynamic efficiency of microbial growth is low but optimal for maximal growth rate. Proc Natl Acad Sci 80:305–309
90. Wetzel RG (1991) Extracellular enzymatic interactions: storage, redistribution and interspecific communication. In: Chrost RJ (ed) Microbial enzymes in aquatic environments. Springer-Verlag, New York, pp 6–28
91. Whalen SC, Reeburgh WS (2001) Carbon monoxide consumption in upland boreal forest soils. Soil Biol Biochem 33:1329–1338
92. Williams PJI (1973) The validity of the application of simple kinetic analysis to heterogeneous microbial populations. Limnol Oceanogr 18:159–165
93. Zhang YHP (2011) Substrate channeling and enzyme complexes for biotechnological applications. Biotechnol Adv 29:715–725
94. Zhang YL, Chen LJ, Sun CX, Li DP, Wu ZJ, Duan ZH (2010) Kinetic and thermodynamic properties or hydrolases in northeastern Chinese soils affected by temperature. Agrochimica 46:232–243
95. Zhuang XL, Gao J, Ma AZ, Fu SL, Zhuang GQ (2013) Bioactive Molecules in Soil Ecosystems: masters of the Underground. Int J Mol Sci 5:8841–8868