Extracellular enzymes in terrestrial, freshwater, and marine environments: perspectives on system variability and common research needs

Abstract

Extracellular enzymes produced by heterotrophic microbial communities are major drivers of carbon and nutrient cycling in terrestrial, freshwater, and marine environments. Although carbon and nutrient cycles are coupled on global scales, studies of extracellular enzymes associated with terrestrial, freshwater, and marine microbial communities are not often compared across ecosystems. In part, this disconnect arises because the environmental parameters that control enzyme activities in terrestrial and freshwater systems, such as temperature, pH, and moisture content, have little explanatory power for patterns of enzyme activities in marine systems. Instead, factors such as the functional diversity of microbial communities may explain varying patterns of enzyme activities observed in the ocean to date. In any case, many studies across systems focus on similar issues that highlight the commonalities of microbial community organization. Examples include the effective lifetime of enzymes released into the environment; the extent to which microbial communities coordinate enzyme expression to decompose complex organic substrates; and the influence of microbial community composition on enzyme activities and kinetics. Here we review the often-disparate research foci in terrestrial, freshwater, and marine environments. We consider the extent to which environmental factors may regulate extracellular enzyme activities within each ecosystem, and highlight commonalities and current methodological challenges to identify research questions that may aid in integrating cross-system perspectives in the future.

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References

  1. Allison SD (2005) Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol Lett 8:626

    Google Scholar 

  2. Allison SD (2006) Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochem 81:361–373

    Google Scholar 

  3. Allison SD (2012) A trait-based approach for modeling microbial litter decomposition. Ecol Lett 15:1058–1070

    Google Scholar 

  4. Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340

    Google Scholar 

  5. Alonso-Saez L, Sanchez O, Gasol JM (2012) Bacterial uptake of low molecular weight organics in the subtropical Atlantic: are major phylogenetic groups functionally different? Limnol Oceanogr 57:798–808

    Google Scholar 

  6. Araújo A, Plassard C, Drevon J (2008) Phosphatase and phytase activities in nodules of common bean genotypes at different levels of phosphorus supply. Plant Soil 312:129–138

    Google Scholar 

  7. Arnosti C (1995) Measurement of depth- and site-related differences in polysaccharide hydrolysis rates in marine sediments. Geochim Cosmochim Acta 59:4247–4257

    Google Scholar 

  8. Arnosti C (2000) Substrate specificity in polysaccharide hydrolysis: contrasts between bottom water and sediments. Limnol Oceanogr 45:1112–1119

    Google Scholar 

  9. Arnosti C (2003) Fluorescent derivatization of polysaccharides and carbohydrate-containing biopolymers for measurement of enzyme activities in complex media. J Chromatogr B 793:181–191

    Google Scholar 

  10. Arnosti C (2008) Functional differences between Arctic sedimentary and seawater microbial communities: contrasts in microbial hydrolysis of complex substrates. FEMS Microbiol Ecol 66:343–351

    Google Scholar 

  11. Arnosti C (2011) Microbial extracellular enzymes and the marine carbon cycle. Ann Rev Mar Sci 3:401–425

    Google Scholar 

  12. Arnosti C, Holmer M (2003) Carbon cycling in a continental margin sediment: contrasts between organic matter characteristics and remineralization rates and pathways. Estuar Coast Shelf Sci 58:197–208

    Google Scholar 

  13. Arnosti C, Repeta DJ (1994) Extracellular enzyme activity in anaerobic bacterial cultures: evidence of pullulanase activity among mesophilic marine bacteria. Appl Environ Microbiol 60:840–846

    Google Scholar 

  14. Arnosti C, Durkin S, Jeffrey WH (2005) Patterns of extracellular enzyme activities among pelagic marine microbial communities: implications for cycling of dissolved organic carbon. Aquat Microb Ecol 38:135–145

    Google Scholar 

  15. Arnosti C, Steen AD, Ziervogel K, Ghobrial S, Jeffrey WH (2011) Latitudinal gradients in degradation of marine dissolved organic carbon. PLoS ONE 6(12):e28900

    Google Scholar 

  16. Arnosti C, Fuchs B, Amann R, Passow U (2012) Contrasting extracellular enzyme activities of particle associated bacteria from distinct provinces of the North Atlantic Ocean. Front Microbiol 3:425. doi:10.3389/fmicb.2012.00425

    Google Scholar 

  17. Arrieta JM, Herndl GJ (2002) Changes in bacterial β-glucosidase diversity during a coastal phytoplankton bloom. Limnol Oceanogr 47:594–599

    Google Scholar 

  18. Baldwin AJ, Moss JA, Pakulski JD, Catala P, Joux F, Jeffrey WH (2005) Microbial diversity in a Pacific Ocean transect from the Arctic to Antarctic circles. Aquat Microb Ecol 41:91–102

    Google Scholar 

  19. Baltar F, Aristegui J, Sintes E, van Aken HM, Gasol JM, Herndl GJ (2009) Prokaryotic extracellular enzymatic activity in relation to biomass production and respiration in the meso- and bathypelagic waters of the (sub)tropical Atlantic. Environ Microbiol. doi:10.1111/j.1462-2920.2009.01922.x

    Google Scholar 

  20. Baltar F, Aristegui J, Gasol JM, Sintes E, van Aken HM, Herndl GJ (2010) High dissolved extracellular enzyme activity in the deep central Atlantic Ocean. Aquat Microb Ecol 58:287–302

    Google Scholar 

  21. Baltar F, Aristegui J, Gasol JM, Yokokawa T, Herndl GJ (2013) Bacterial versus archaeal origin of extracellular enzymatic activity in the Northeast Atlantic deep waters. Microb Ecol 65:277–288

    Google Scholar 

  22. Baty AM III, Eastburn CC, Diwu Z, Techkarnjanaruk S, Goodman AE, Geesey GG (2000a) Differentiation of chitinase-active and non-chitinase-active subpopulations of a marine bacterium during chitin degradation. Appl Environ Microbiol 66:3566–3573

    Google Scholar 

  23. Baty AM III, Eastburn CC, Techkarnjanaruk S, Goodman AE, Geesey GG (2000b) Spatial and temporal variations in chitinolytic gene expression and bacterial biomass production during chitin degradation. Appl Environ Microbiol 66:3574–3585

    Google Scholar 

  24. Bauer M, Kube M, Telling H, Richter M, Lombardot T, Allers E, Wurdemann CA, Quast C, Kuhl H, Knaust F, Woebken D, Bischof K, Mussmann M, Choudhuri JV, Meyer F, Reinhardt R, Amann RI, Glockner FO (2006) Whole genome analysis of the marine Bacteroidetes ‘Gramella forsetii’ reveals adaptations to degradation of polymeric organic matter. Environ Microbiol 8:2201–2213

    Google Scholar 

  25. Beier, Bertilsson (2011) Uncoupling of chitinase activity and uptake of hydrolysis products in freshwater bacterioplankton. Limnol Oceanogr 56(4):1179–1188

    Google Scholar 

  26. Bell TH, Henry HAL (2011) Fine scale variability in soil extracellular enzyme activity is insensitive to rain events and temperature in a mesic system. Pedobiology 54:141–146

    Google Scholar 

  27. Benz R, Bauer K (1988) Permeation of hydrophilic molecules through the outer membrane of gram-negative bacteria. Eur J Biochem 176:1–19

    Google Scholar 

  28. Bird JA, Herman DJ, Firestone MK (2011) Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol Biochem 43:718–725

    Google Scholar 

  29. Boetius A, Lochte K (1994) Regulation of microbial enzymatic degradation of organic matter in deep-sea sediments. Mar Ecol Prog Ser 104:299–307

    Google Scholar 

  30. Boetius A, Lochte K (1996) High proteolytic activities of deep-sea bacteria from oligotrophic polar sediments. Arch Hydrobiol 48:269–276

    Google Scholar 

  31. Boetius A, Ferdelman T, Lochte K (2000) Bacterial activity in sediments of the deep Arabian Sea in relation to vertical flux. Deep-Sea Res II 47:2835–2875

    Google Scholar 

  32. Bong CW, Obayashi Y, Suzuki S (2013) Succession of protease activity in seawater and bacterial isolates during starvation in a mesocosm experiment. Aquat Microb Ecol 69:33–46

    Google Scholar 

  33. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781

    Google Scholar 

  34. Bouvier TC, del Giorgio PA (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47:453–470

    Google Scholar 

  35. Bradford MA, Keiser AD, Davies CA, Mersmann CA, Strickland MS (2013) Empirical evidence that soil carbon formation from plant inputs is positively related to microbial growth. Biogeochemistry 113:271–281

    Google Scholar 

  36. Burns RG (ed) (1978) Soil enzymes. Academic Press, New York

    Google Scholar 

  37. Campbell BM, Yu L, Heidelberg JF, Kirchman DL (2011) Activity of abundant and rate bacteria in a coastal ocean. Proc Natl Acad Sci USA 108:12776–12781

    Google Scholar 

  38. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard, Henrissat B (2008) The carbohydrate-active enzyme database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:233–238

    Google Scholar 

  39. Chang A, Scheer M, Grote A, Schomburg I, Schomburg D (2009) BRENDA, AMENDA and FRENDA the enzyme information system: new content and tools in 2009. Nucleic Acids Res 37:D588–D592

    Google Scholar 

  40. Christian JR, Karl DM (1995) Bacterial ectoenzymes in marine waters: activity ratios and temperature responses in three oceanographic provinces. Limnol Oceanogr 40:1042–1049

    Google Scholar 

  41. Chróst RJ (ed) (1991) Microbial enzymes in aquatic environments. Springer, New York

    Google Scholar 

  42. Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252

    Google Scholar 

  43. Coolen MJL, Overmann J (2000) Functional exoenzymes as indicators of metabolically active bacteria in 124,000 year old sapropel layers of the eastern Mediterranean Sea. Appl Environ Microb 66:2589–2598

    Google Scholar 

  44. Coolen MJL, Cyprionka H, Sass AM, Sass H, Overmann J (2002) Ongoing modification of Mediterranean Pleistocene sapropels mediated by prokaryotes. Science 296:2407–2410

    Google Scholar 

  45. Cotta MA, Zeltwanger RL (1995) Degradation and utilization of xylan by the ruminal bacteria Butyrivibrio fibrisolvens and Selenomonas ruminantium. Appl Environ Microbiol 61:4396–4402

    Google Scholar 

  46. Cowie GL, Hedges JI, Prahl FG, De Lange J (1995) Elemental and major biochemical changes across an oxidation front in a relict turbidite: an oxygen effect. Geochim Cosmochim Acta 59:33–46

    Google Scholar 

  47. Crump BC, Hopkinson CS, Sogin ML, Hobbie JE (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 70:1494–1505

    Google Scholar 

  48. de Graaff MA, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064

    Google Scholar 

  49. Dell’Anno A, Fabiano M, Mei ML, Danovaro R (2000) Enzymatically hydrolysed protein and carbohydrate pools in deep-sea sediments: estimates of the potentially bioavailable fraction and methodological considerations. Mar Ecol Prog Ser 196:15–23

    Google Scholar 

  50. Dinkelaker B, Marschner H (1992) In vivo demonstration of acid phosphatase activity in the rhizosphere of soil-grown plants. Plant Soil 144:199–205

    Google Scholar 

  51. Drake JE, Darby BA, Giasson M-A, Kramer MA, Phillips RP, Finzi AC (2013) Stoichiometry constrains microbial response to root exudation-insights from a model and a field experiment in a temperate forest. Biogeosciences 10:821–838

    Google Scholar 

  52. Faugeron C, Mollet J-C, Karamanos Y, Morvan H (2006) Activities of de-& N-glycosylation are ubiquitously found in tomato plant. Acta Physiol Plant 28:557–565

    Google Scholar 

  53. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017

    Google Scholar 

  54. Folse HJ, Allison SD (2012) Cooperation, competition, and coalitions in enzyme-producing microbes: social evolution and nutrient depolymerization rates. Front Microbiol 3:338

    Google Scholar 

  55. Friedline CJ, Franklin RB, McCallister SL, Rivera MC (2012) Bacterial assemblages of the eastern Atlantic Ocean reveal both vertical and latitudinal biogeographic signatures. Biogeosciences 9:2177–2193

    Google Scholar 

  56. Frossard ALG, Mutz M, Gessner MO (2012) Disconnect of microbial structure and function: enzyme activities and bacterial communities in nascent stream corridors. ISME J 6:680–691

    Google Scholar 

  57. Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. Proc Natl Acad Sci USA 105:7774–7778

    Google Scholar 

  58. Fukuda R, Sohrin Y, Saotome N, Fukuda H, Nagata T, Koike I (2000) East-west gradient in ectoenzyme activities in the subarctic Pacific: possible regulation by zinc. Limnol Oceanogr 45:930–939

    Google Scholar 

  59. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397

    Google Scholar 

  60. Glöckner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig W, Gade D, Borzym K, Heitmann K, Rabus R, Schlesner H, Amann R, Reinhardt R (2003) Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci USA 100:8298–8303

    Google Scholar 

  61. Gomez-Pereira PR, Fuchs BM, Alonso C, Oliver MJ, van Beusekom JEE, Amann R (2010) Distinct flavobacterial communities in contrasting water masses of the North Atlantic Ocean. ISME J 4:472–487

    Google Scholar 

  62. Gomez-Pereira PR, Schuler M, Fuchs BM, Bennke CM, Teeling H, Waldmann J, Richter M, Barbe V, Bataille E, Glockner FO, Amann R (2012) Genomic content of uncultured Bacteroidetes from contrasting oceanic provinces in the North Atlantic Ocean. Environ Microb 14:52–66

    Google Scholar 

  63. Gram L, Grossart H-P, Schlingloff A, Kiorboe T (2002) Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl Environ Microbiol 68:4111–4116

    Google Scholar 

  64. Grossart HP, Simon M (1999) Bacterial colonization and microbial decomposition of limnetic organic aggregates (lake snow). Aquat Microb Ecol 15:127–140

    Google Scholar 

  65. Hedges JI (1992) Global biogeochemical cycles: progress and problems. Mar Chem 39:67–93

    Google Scholar 

  66. Hedges JI, Eglinton G, Hatcher PG, Kirchman DL, Arnosti C, Derenne S, Evershed RP, Kögel-Knabner I, de Leeuw JW, Littke R, Michaelis W, Rullkötter J (2000) The molecularly-uncharacterized component (MUC) of nonliving organic matter in natural environments. Organ Geochem 31:945–958

    Google Scholar 

  67. Hmelo LR, Mincer TJ, Van Mooy BAS (2011) Possible influence of bacterial quorum sensing on the hydrolysis of sinking particulate organic carbon in marine environments. Environ Microbiol Rep 3:682–688

    Google Scholar 

  68. Hoppe H-G (1983) Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar Ecol Prog Ser 11:299–308

    Google Scholar 

  69. Jackson C, Foreman C, Sinsabaugh RL (1995) Microbial enzyme activities as indicators of organic matter processing rates in a Lake Erie coastal wetland. Freshw Biol 34:329–342

    Google Scholar 

  70. Jobbágy EG (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423

    Google Scholar 

  71. Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2004) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515

    Google Scholar 

  72. Kallmeyer J, Pockalny R, Adhikari RR, Smith DC, D’Hondt S (2012) Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci USA. doi:10.1073/pnas.1203849109

    Google Scholar 

  73. Kirchman DL, Elifantz H, Dittel AI, Malmstrom RR, Cottrell MT (2007) Standing stocks and activity of archea and bacteria in the western Arctic Ocean. Limnol Oceanogr 52:495–507

    Google Scholar 

  74. Kobayashi T, Koide O, Mori K, Shimamura S, Matsuura T, Miura T, Takaki Y, Morono Y, Nunoura T, Imachi F, Takai K, Horikoshi K (2008) Phylogenetic and enzymatic diversity of deep subseafloor aerobic microorganisms in organics- and methane-rich sediments off Shimokita Peninsula. Extremophiles 12:519–527

    Google Scholar 

  75. Krauss G-J, Solé M, Krauss G, Schlosser D, Wesenberg D, Bärlocher F (2011) Fungi in freshwaters: ecology, physiology and biochemical potential. FEMS Microbiol Rev 35:620–651

    Google Scholar 

  76. Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci 165:382–396

    Google Scholar 

  77. Lam SK, Ng TB (2001) Isolation of a small chitinase-like antifungal protein from Panax notoginseng (sanchi ginseng) roots. Int J Biochem Cell Biol 33:287–292

    Google Scholar 

  78. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Google Scholar 

  79. Lawrence CR, Neff JC, Schimel JP (2009) Does adding microbial mechanisms of decomposition improve soil organic matter models? A comparison of four models using data from a pulsed rewetting experiment. Soil Biol Biochem 41:1923–1934

    Google Scholar 

  80. Lee C, Wakeham SG, Arnosti C (2004) Particulate organic matter in the sea: the composition conundrum. Ambio 33:559–568

    Google Scholar 

  81. Lennon JT, Aanderud ZT, Lehmkuhl BK, Schoolmaster DR (2012) Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 93:1867–1879

    Google Scholar 

  82. Liang C, Cheng G, Wixon DL, Balser TC (2011) An absorbing Markov chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry 106:303–309

    Google Scholar 

  83. Liu Z, Kobiela ME, McKee GA, Tang T, Lee C, Mulholland MR, Hatcher PG (2010) The effect of chemical structure on the hydrolysis of tetrapeptides along a river-to-ocean transect: AVFA and SWGA. Mar Chem 119:108–120

    Google Scholar 

  84. Lloyd KG, Schreiber L, Petersen DG, Kjeldsen KU, Lever MA, Steen AD, Stepanauskas R, Richter M, Kleindienst S, Lenk S, Schramm A, Jørgensen BB (2013) Predominant archaea in marine sediments degrade detrital proteins. Nature 496:215–218

    Google Scholar 

  85. Mackelprang R, Waldrop MP, DeAngelis KM, David MM, Chavarria KL, Blazewicz SJ, Rubin EM, Jansson JK (2011) Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480:368–371

    Google Scholar 

  86. Maire V, Alvarez G, Colombet J, Comby A, Despinasse R, Dubreucq E, Joly M, Lehours A-C, Perrier V, Shahzad T, Fontaine S (2012) An unknown respiration pathway substantially contributes to soil CO2 emissions. Biogeosci Discuss 6:8663–8691

    Google Scholar 

  87. Martinez J, Smith DC, Steward GF, Azam F (1996) Variability in ectohydrolytic enzyme activities of pelagic marine bacteria and its significance for substrate processing in the sea. Aquat Microb Ecol 10:223–230

    Google Scholar 

  88. Martinez-Garcia M, Brazel DM, Swan BK, Arnosti C, Chain PSG, Reitenga KG, Xie G, Poulton NJ, Gomez ML, Masland DED, Thompson B, Bellows WK, Ziervogel K, Lo C–C, Ahmed S, Gleasner CD, Detter CJ, Stepanauskas R (2012) Capturing single cell genomes of active polysaccharide degraders: an unexpected contribution of Verrucomicrobia. PLoS ONE 7:e35314

    Google Scholar 

  89. Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2011) SOM genesis: microbial biomass as a significant source. Biogeochemistry 39:1–15

    Google Scholar 

  90. Moora M, Berger S, Davison J, Öpik M, Bommarco R, Bruelheide H, Kühn I, Kunin WE, Metsis M, Rortais A, Vanatoa A, Vanatoa E, Stout JC, Truusa M, Westphal C, Zobel M, Walther G-R (2011) Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J Biogeogr 38:1305–1317

    Google Scholar 

  91. Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174

    Google Scholar 

  92. Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities, which balances microbial demands during decomposition. Soil Biol Biochem 53:133–141

    Google Scholar 

  93. Nannipieri P (2006) Role of stabilised enzymes in microbial ecology and enzyme extraction from soil with potential applications in soil proteomics. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil. Springer, Berlin, pp 75–94

    Google Scholar 

  94. Nikrad MP, Cottrell MT, Kirchman DL (2012) Abundance and single-cell activity of heterotrophic bacterial groups in the western Arctic Ocean in summer and winter. Appl Environ Microbiol 78:2402–2409

    Google Scholar 

  95. Obayashi Y, Suzuki S (2005) Proteolytic enzymes in coastal surface seawater: significant activity of endopeptidases and exopeptidases. Limnol Oceanogr 50:722–726

    Google Scholar 

  96. Obayashi Y, Suzuki S (2008) Occurrence of exo- and endopeptidases in dissolved and particulate fractions of coastal seawater. Aquat Microb Ecol 50:231–237

    Google Scholar 

  97. Orwin KH, Buckland SM, Johnson D, Turner BL, Smart S, Oakley S, Bardgett RD (2010) Linkages of plant traits to soil properties and the functioning of temperate grassland. J Ecol 98:1074–1083

    Google Scholar 

  98. Pantoja S, Lee C (1999) Peptide decomposition by extracellular hydrolysis in coastal seawater and salt marsh sediment. Mar Chem 63:273–291

    Google Scholar 

  99. Pantoja S, Lee C, Marecek JF (1997) Hydrolysis of peptides in seawater and sediments. Mar Chem 57:25–40

    Google Scholar 

  100. Parkin TB (1987) Soil microsites as a source of denitrification variability. Soil Sci Soc Am J 51:1194–1199

    Google Scholar 

  101. Piontek J, Borchard C, Sperling M, Schulz KG, Riebesell U, Engel A (2012) Response of bacterioplankton activity in an Arctic fjord system to elevated pCO2: results from a mesocosm perturbation study. Biogeosci Discuss 9:10467–10511

    Google Scholar 

  102. Pommier T, Canback B, Riemann L, Bostrom KH, Simu K, Lundberg P, Tunlid A, Hagstrom A (2007) Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 16:867–880

    Google Scholar 

  103. Posada RH, Madriñan S, Rivera E-L (2012) Relationships between the litter colonization by saprotrophic and arbuscular mycorrhizal fungi with depth in a tropical forest. Fungal Biol 116:747–755

    Google Scholar 

  104. Resat H, Bailey V, McCue LA, Konopka A (2012) Modeling microbial dynamics in heterogeneous environments: growth on soil carbon sources. Microb Ecol 63:883–897

    Google Scholar 

  105. Richardson AD (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Funct Plant Biol 287:897–906

    Google Scholar 

  106. Rinkes ZL, Weintraub MN, DeForest JL, Moorhead DL (2011) Microbial substrate preference and community dynamics during decomposition of Acer saccharum. Fungal Ecol 4:396–407

    Google Scholar 

  107. Rout ME, Callaway RM (2012) Interactions between exotic invasive plants and soil microbes in the rhizosphere suggest that ‘everything is not everywhere’. Ann Bot 110(2):213–222

    Google Scholar 

  108. 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

    Google Scholar 

  109. Schneider T, Keiblinger KM, Schmid E, Sterflinger-Gleixner K, Ellersdorfer G, Roschitzki B, Richter A, Eberl L, Zechmeister-Boltenstern S, Riedel K (2012) Who is who in litter decomposition? Metaproteomics reveals major microbial players and their biogeochemical functions. ISME J 6:1749–1762

    Google Scholar 

  110. Sexstone AJ, Revsbech NP, Parkin TB, Tiedje JM (1985) Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci Soc Am J 49:645–651

    Google Scholar 

  111. Silveira CB, Vieira RP, Cardoso AM, Paranhos R, Albano RM, Martins OB (2011) Influence of salinity on bacterioplankton communities from the Brazilian rain forest to the coastal Atlantic Ocean. PLoS ONE 6(3):e17789. doi:10.1371/journal.pone.0017789

    Google Scholar 

  112. Simon M, Grossart H-P, Schweitzer B, Ploug H (2002) Microbial ecology of organic aggregates in aquatic ecosystems. Aquat Microb Ecol 28:175–211

    Google Scholar 

  113. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Google Scholar 

  114. Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic stoichiometry and ecological theory. Annu Rev Ecol Evol Syst 43:313–343

    Google Scholar 

  115. Sinsabaugh RL, Moorhead DL (1997) Synthesis of litter quality and enzymic approaches to decomposition modelling (Chapter 27). In: Cadisch G, Giller K (eds) Driven by nature: plant litter quality and decomposition. CAB International, Wallingford, pp 363–375

    Google Scholar 

  116. Sinsabaugh RL, Benfield EF, Linkins AE (1981) Cellulase activity associated with the decomposition of leaf litter in a woodland stream. Oikos 36:184–190

    Google Scholar 

  117. Sinsabaugh RL, Osgood M, Findlay M (1994) Enzymatic models for estimating decomposition rates of particulate detritus. J Am Benthol Soc 13:160–169

    Google Scholar 

  118. 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 MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Google Scholar 

  119. Sinsabaugh RL, Van Horn DJ, Shah JJF, Findlay S (2010) Ecoenzymatic stoichiometry in relation to productivity for freshwater biofilm and plankton communities. Microb Ecol 60:885–893

    Google Scholar 

  120. Sinsabaugh RL, Shah JJF, Hill BH, Elonen CM (2012) Ecoenzymatic stoichiometry of stream sediments with comparison to terrestrial soils. Biogeochemistry 111:455–467

    Google Scholar 

  121. Smith DC, Simon M, Alldredge AL, Azam F (1992) Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359:139–142

    Google Scholar 

  122. Somville M, Billen G (1983) A method for determining exoproteolytic activity in natural waters. Limnol Oceanogr 28:109–193

    Google Scholar 

  123. Steen AD, Arnosti C (2013) Extracellular peptidase and carbohydrate hydrolase activities in an Arctic Fjord (Smeerenburgfjord, Svalbard). Aquat Microb Ecol 69:93–99

    Google Scholar 

  124. Steen AD, Arnosti C, Ness L, Blough NV (2006) Electron paramagnetic resonance spectroscopy as a novel approach to measuring macromolecule-surface interactions and activities of extracellular enzymes. Mar Chem 101:266–276

    Google Scholar 

  125. Steen AD, Hamdan L, Arnosti C (2008) Dynamics of high molecular weight dissolved organic carbon in the Chesapeake Bay: insights from enzyme activities, carbohydrate concentrations, and microbial metabolism. Limnol Oceanogr 53:936–947

    Google Scholar 

  126. Steen AD, Ziervogel K, Ghobrial S, Arnosti C (2012) Functional variation among polysaccharide-hydrolyzing microbial communities in the Gulf of Mexico. Mar Chem 138:13–20

    Google Scholar 

  127. Stromberger ME, Shah Z, Westfall DG (2011) High specific activity in low microbial biomass soils across a no-till evapotranspiration gradient in Colorado. Soil Biol Biochem 43:97–105

    Google Scholar 

  128. Tarafdar JC, Claassen N (1988) Organic phosphorus compounds as a phosphorus source for higher plants through the activity of phosphatases produced by plant roots and microorganisms. Biol Fertil Soils 5:308–312

    Google Scholar 

  129. Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glöckner FO, Schweder T, Amann R (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336:608–611

    Google Scholar 

  130. Teske A, Durbin A, Ziervogel K, Cox C, Arnosti C (2011) Microbial community composition and function in permanently cold seawater and sediments from an Arctic fjord of Svalbard. Appl Environ Microbiol 77:208–218

    Google Scholar 

  131. Tietjen T, Wetzel RG (2003) Extracellular enzyme-clay mineral complexes: enzyme adsorption, alteration of enzyme activity, and protection from photodegradation. Aquat Ecol 37:331–339

    Google Scholar 

  132. Treseder KK, Vitousek PM (2001) Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiin rain forests. Ecology 82:946–954

    Google Scholar 

  133. Van Mooy B, Hmelo LR, Sofen LE, Campagna SR, May AL, Dyhrman ST, Heithoff A, Webb EA, Momper L, Mincer TJ (2012) Quorum sensing control of phosphorus acquisition in Trichodesmium consortia. ISME J 6:422–429

    Google Scholar 

  134. Vetter Y-A, Deming JW, Jumars PA, Krieger-Brockett BB (1998) A predictive model of bacterial foraging by means of freely released extracellular enzymes. Microb Ecol 36:75–92

    Google Scholar 

  135. Wakeham SG, Lee C, Hedges JI, Hernes PJ, Peterson ML (1997) Molecular indicators of diagenetic status in marine organic matter. Geochim Cosmochim Acta 61:5363–5369

    Google Scholar 

  136. Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846

    Google Scholar 

  137. Wallenstein MD, Weintraub MN (2008) Emerging tools for measuring and modeling the in situ activity of soil extracellular enzymes. Soil Biol Biochem 40:2098–2106

    Google Scholar 

  138. Wallenstein MD, Haddix ML, Ayres E, Steltzer H, Magrini-Bair KA, Paul EA (2012) Litter chemistry changes more rapidly when decomposed at home but converges during decomposition-transformation. Soil Biol Biochem. doi:10.1016/j.soilbio.2012.09.027

    Google Scholar 

  139. Warren RAJ (1996) Microbial hydrolysis of polysaccharides. Annu Rev Microbiol 50:183–212

    Google Scholar 

  140. Wegner C-E, Richter-Heitmann T, Klindworth A, Klockow C, Richter M, Achstetter T, Glöckner FO, Harder J (2013) Expression of sulfatases in Rhodopirellula baltica and the diversity of sulfatases in the genus Rhodopirellula. Mar Genomics 9:51–61

    Google Scholar 

  141. Weiner RM, Taylor LE II, Henrissat B, Hauser L, Land M, Coutinho PM, Rancurel C, Saunders EH, Longmire AG, Zhange H, Bayer EA, Gilbert HJ, Larimer F, Zhulin IB, Ekborg NA, Lamed R, Richardson PM, Borovok I, Hutcheson S (2008) Complete genome sequence of the complex carbohydrate-degrading marine bacterium, Saccharophagus degradans Strain 2-40T. PLoS Genet 5:e1000087

    Google Scholar 

  142. Wetzel R (1993) Humic compounds from wetlands: complexation, inactivation and reactivation of surface-bound and extracellular enzymes. Verhandlungen der Internationalen Vereingang fur Liminologie 25:122–128

    Google Scholar 

  143. Wickings K, Grandy AS, Reed SC, Cleveland CC (2012) The origin of litter chemical complexity during decomposition. Ecol Lett 15:1180–1188

    Google Scholar 

  144. Zak DR, Holmes WE, White DC, Peacock AD, Tilman D (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84:2042–2050

    Google Scholar 

  145. Ziervogel K, Steen AD, Arnosti C (2010) Changes in the spectrum and rates of extracellular enzyme activities in seawater following aggregate formation. Biogeosciences 7:1007–1017

    Google Scholar 

  146. Zinger L, Amaral-Zettler LA, Fuhrman JA, Horner-Devine MC, Huse SM, Welch DBM, Martiny JBH, Sogin ML, Boetius A, Ramette A (2011) Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. PLoS ONE 6:e24570

    Google Scholar 

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Acknowledgments

We would like to thank the Enzymes in the Environment Research Coordination Network for organizing the 2nd International RCN Workshop: Incorporating Enzymes into Biogeochemistry: Paradigms, Models & Classes workshop. Discussions at the workshop, which was funded by the US National Science Foundation under award number 0840869, spurred us to write this review. This work was also supported by National Science Foundation grants OCE-0848703 to Arnosti; Ecosystems Program 0918718 to Weintraub, Moorehead, and Sinsabaugh; and 1020540 to Bell and Wallenstein. This manuscript is also a C-DEBI contribution (number 175; grant 36202823 to Steen; 161533 to Arnosti; C-DEBI is funded by NSF award OCE-0939564). We thank Leigh McCallister, as well as four anonymous reviewers, for their thoughtful comments that considerably improved the manuscript.

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Arnosti, C., Bell, C., Moorhead, D.L. et al. Extracellular enzymes in terrestrial, freshwater, and marine environments: perspectives on system variability and common research needs. Biogeochemistry 117, 5–21 (2014). https://doi.org/10.1007/s10533-013-9906-5

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Keywords

  • Extracellular enzymes
  • Soil
  • Aquatic
  • Terrestrial
  • Marine
  • Microbial communities