Changes in extracellular enzyme activity and microbial community structure with soil depth at the Luquillo Critical Zone Observatory

Abstract Extracellular enzymes in soils mediate the decomposition of organic matter and catalyze key transformations in carbon, nitrogen and phosphorus cycling. However, most studies of extracellular enzyme activity have focused exclusively on relatively carbon and nutrient-rich surface soils. In tropical forests, several centimeters of nutrient-rich surface soil can overlay meters of resource-poor subsoil, of which the microbial ecology is poorly characterized. The goal of this study was to determine how extracellular enzyme activity changes as a function of depth across two soil orders (Oxisols and Inceptisols) and two forest types that occur at different elevations (Tabonuco, lower elevation; Colorado, higher elevation) at the Luquillo Critical Zone Observatory in northeast Puerto Rico. We excavated three soil pits to 140 cm at four different sites representing the four soil × forest combinations, and measured potential activities of four carbon-acquiring enzymes (α-glucosidase, β-glucosidase, β-xylosidase, cellobiohydrolase), one nitrogen-acquiring enzyme (N-acetyl glucosaminidase) and one organic phosphorus-acquiring enzyme (acid phosphatase) at six discrete depth intervals. We used phospholipid fatty acid (PLFA) analysis to assess viable microbial biomass and community structure. Overall, microbial biomass, specific enzyme activities and community structure were similar across the two soil and forest types, in spite of higher carbon concentrations and C:N ratios in the Colorado forest soil. Soil nutrients, microbial biomass and potential enzyme activities all declined exponentially with depth. However, when normalized to microbial biomass, specific enzyme activities either did not change with depth (β-glucosidase, β-xylosidase, cellobiohydrolase and N-acetyl glucosaminidase) or increased significantly with depth (α-glucosidase and acid phosphatase, P P

[1]  S. Hallam,et al.  Bacterial, archaeal and eukaryal community structures throughout soil horizons of harvested and naturally disturbed forest stands. , 2009, Environmental microbiology.

[2]  I. Kögel‐Knabner,et al.  Deep soil organic matter—a key but poorly understood component of terrestrial C cycle , 2010, Plant and Soil.

[3]  C. Trasar-Cepeda,et al.  Hydrolytic enzyme activities in agricultural and forest soils. Some implications for their use as indicators of soil quality , 2008 .

[4]  G. Gleixner,et al.  Soil organic matter in soil depth profiles: Distinct carbon preferences of microbial groups during carbon transformation , 2008 .

[5]  Marie-France Dignac,et al.  Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation , 2005, Plant and Soil.

[6]  S. Allison Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes , 2006 .

[7]  S. Allison,et al.  Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes , 2013, The ISME Journal.

[8]  L. Øvreås,et al.  Microbial diversity and function in soil: from genes to ecosystems. , 2002, Current opinion in microbiology.

[9]  W. Silver Is nutrient availability related to plant nutrient use in humid tropical forests? , 1994, Oecologia.

[10]  J. DeForest The influence of time, storage temperature, and substrate age on potential soil enzyme activity in acidic forest soils using MUB-linked substrates and L-DOPA. , 2009 .

[11]  Donald L. Sparks,et al.  Methods of soil analysis. , 2015 .

[12]  I. Kögel‐Knabner,et al.  Soil organic matter stabilization in acidic forest soils is preferential and soil type‐specific , 2008 .

[13]  P. L. Weaver Environmental gradients affect forest structure in Puerto Rico's Luquillo Mountains , 2000 .

[14]  Durell C. Dobbins,et al.  Microbial Biomass, Activity, and Community Structure in Subsurface Soils , 1986 .

[15]  T. Heimburg,et al.  Voltage-Gated Lipid Ion Channels , 2012, PloS one.

[16]  J. Moncrieff,et al.  The variation of soil microbial respiration with depth in relation to soil carbon composition , 2004, Plant and Soil.

[17]  T. Cajthaml,et al.  Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil , 2008 .

[18]  E. A. Greathouse,et al.  Geographic and ecological setting of the Luquillo Mountains , 2012 .

[19]  J. DeForest,et al.  Soil microbial responses to elevated phosphorus and pH in acidic temperate deciduous forests , 2012, Biogeochemistry.

[20]  P. Nannipieri,et al.  Kinetics of enzyme reactions in soil environments , 1998 .

[21]  E. Kandeler,et al.  Microbial Population Structures in Soil Particle Size Fractions of a Long-Term Fertilizer Field Experiment , 2001, Applied and Environmental Microbiology.

[22]  C. Francis,et al.  Changes in Bacterial and Archaeal Community Structure and Functional Diversity along a Geochemically Variable Soil Profile , 2008, Applied and Environmental Microbiology.

[23]  D. Moorhead,et al.  Resource allocation to extracellular enzyme production: A model for nitrogen and phosphorus control of litter decomposition , 1994 .

[24]  R. Sinsabaugh,et al.  Ecoenzymatic Stoichiometry and Ecological Theory , 2012 .

[25]  M. Gessner,et al.  Disconnect of microbial structure and function: enzyme activities and bacterial communities in nascent stream corridors , 2011, The ISME Journal.

[26]  S. Brantley,et al.  The coupling of biological iron cycling and mineral weathering during saprolite formation, Luquillo Mountains, Puerto Rico , 2005 .

[27]  William B. Bowden,et al.  Riparian nitrogen dynamics in two geomorphologically distinct tropical rain forest watersheds: subsurface solute patterns , 1992 .

[28]  W. Silver,et al.  Nutrient availability in a montane wet tropical forest: Spatial patterns and methodological considerations , 1994, Plant and Soil.

[29]  C. Rasmussen,et al.  Geologic controls of soil carbon cycling and microbial dynamics in temperate conifer forests , 2009 .

[30]  P. Bodelier,et al.  Phosphatases relieve carbon limitation of microbial activity in Baltic Sea sediments along a redox‐gradient , 2011 .

[31]  Ingrid Kögel-Knabner,et al.  The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter , 2002 .

[32]  R. Burns,et al.  Comparison of microbial numbers and enzymatic activities in surface soils and subsoils using various techniques , 2002 .

[33]  R. Burns Enzyme activity in soil: Location and a possible role in microbial ecology , 1982 .

[34]  B. Jørgensen,et al.  Microbial life under extreme energy limitation , 2013, Nature Reviews Microbiology.

[35]  R. Sinsabaugh,et al.  Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils , 2013, Biogeochemistry.

[36]  V. M. Seiders Geologic map of the El Yunque Quadrangle, Puerto Rico , 1971 .

[37]  D. Bossio,et al.  Impacts of Carbon and Flooding on Soil Microbial Communities: Phospholipid Fatty Acid Profiles and Substrate Utilization Patterns , 1998, Microbial Ecology.

[38]  A. Lugo,et al.  Geomorphology, disturbance, and the soil and vegetation of two subtropical wet steepland watersheds of Puerto Rico , 1995 .

[39]  W. Silver,et al.  Iron oxidation stimulates organic matter decomposition in humid tropical forest soils , 2013, Global change biology.

[40]  S. Marhan,et al.  Temporal variation in surface and subsoil abundance and function of the soil microbial community in an arable soil , 2013 .

[41]  S. Ullrich,et al.  Profiles of ectoenzymes in the Indian Ocean: phenomena of phosphatase activity in the mesopelagic zone , 1999 .

[42]  S. P. Anderson,et al.  Digging deeper to find unique microbial communities: The strong effect of depth on the structure of bacterial and archaeal communities in soil , 2012 .

[43]  A. Lugo,et al.  Luquillo Experimental Forest: Research History and Opportunities , 2012 .

[44]  Noah Fierer,et al.  Variations in microbial community composition through two soil depth profiles , 2003 .

[45]  L. Ranjard,et al.  Quantitative and qualitative microscale distribution of bacteria in soil. , 2001, Research in microbiology.

[46]  L. Zelles,et al.  Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review , 1999, Biology and Fertility of Soils.

[47]  Jason D. Gans,et al.  Computational Improvements Reveal Great Bacterial Diversity and High Metal Toxicity in Soil , 2005, Science.

[48]  S. Venkatesan,et al.  Comparison of enzyme activity with depth under tea plantations and forested sites in south India , 2006 .

[49]  L. Gianfreda,et al.  Stabilizing Enzymes as Synthetic Complexes , 2015 .

[50]  R. Burns,et al.  Ecology of Extracellular Enzyme Activities and Organic Matter Degradation in Soil: A Complex Community‐Driven Process , 2015 .

[51]  Sarah D Burton,et al.  Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. , 2011, Ecology.

[52]  A. Lugo,et al.  Research History and Opportunities in the Luquillo Experimental Forest , 1983 .

[53]  P. Setlow I will survive: DNA protection in bacterial spores. , 2007, Trends in microbiology.

[54]  R. Knight,et al.  Soil bacterial and fungal communities across a pH gradient in an arable soil , 2010, The ISME Journal.

[55]  F. Scatena An Introduction to the Physiography and History of the Bisley Experimental Watersheds in the Luquillo Mountains of Puerto Rico , 1989 .

[56]  E. Bååth,et al.  Use and misuse of PLFA measurements in soils , 2011 .

[57]  R. B. Jackson,et al.  THE VERTICAL DISTRIBUTION OF SOIL ORGANIC CARBON AND ITS RELATION TO CLIMATE AND VEGETATION , 2000 .

[58]  Benjamin L Turner,et al.  Stability of hydrolytic enzyme activity and microbial phosphorus during storage of tropical rain forest soils , 2010 .

[59]  S. Allison,et al.  Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems , 2007 .

[60]  K. Pregitzer,et al.  Compositional and functional shifts in microbial communities due to soil warming , 1997 .

[61]  Y. Kuzyakov,et al.  Phosphorus mineralization can be driven by microbial need for carbon , 2013 .

[62]  L. Holdridge Life zone ecology. , 1967 .

[63]  S. Fonte,et al.  Decomposition of Greenfall vs. Senescent Foliage in a Tropical Forest Ecosystem in Puerto Rico , 2004 .

[64]  G. Gee,et al.  Particle-size Analysis , 2018, SSSA Book Series.

[65]  S. Allison,et al.  Evolutionary-Economic Principles as Regulators of Soil Enzyme Production and Ecosystem Function , 2010 .

[66]  G. Nausch,et al.  Bioavailable dissolved organic phosphorus and phosphorus use by heterotrophic bacteria , 2007 .

[67]  A. Azzellino,et al.  Multivariate analysis of soils: microbial biomass, metabolic activity, and bacterial-community structure and their relationships with soil depth and type , 2011 .

[68]  S. Hobbie,et al.  The effects of substrate composition, quantity, and diversity on microbial activity , 2010, Plant and Soil.

[69]  Arthur H. Johnson,et al.  Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure , 2003, Oecologia.

[70]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[71]  H. Tiessen,et al.  Characterization of Available P by Sequential Extraction , 2007 .

[72]  W. Silver,et al.  Microbial communities acclimate to recurring changes in soil redox potential status. , 2010, Environmental microbiology.

[73]  S. Allison Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments , 2005 .

[74]  P. G. Murphy,et al.  Forest structure and productivity in Puerto Rico's Luquillo Mountains. , 1990 .

[75]  S. Jagadamma,et al.  Activation Energy of Extracellular Enzymes in Soils from Different Biomes , 2013, PloS one.

[76]  N. Fierer,et al.  Controls on microbial CO2 production: a comparison of surface and subsurface soil horizons , 2003 .

[77]  D. White,et al.  Determination of the sedimentary microbial biomass by extractible lipid phosphate , 2004, Oecologia.

[78]  R. Tate Microbial Activity in Organic Soils as Affected by Soil Depth and Crop , 1979, Applied and environmental microbiology.

[79]  Kristofer D. Johnson,et al.  Atypical soil carbon distribution across a tropical steepland forest catena , 2011 .

[80]  V. M. Seiders Cretaceous and lower Tertiary stratigraphy of the Gurabo and El Yunque quadrangles, Puerto Rico , 1971 .

[81]  D. Moorhead,et al.  Microbial substrate preference and community dynamics during decomposition of Acer saccharum , 2011 .

[82]  S. Allison,et al.  Stoichiometry of soil enzyme activity at global scale. , 2008, Ecology letters.

[83]  W. Wieder,et al.  Organic matter inputs shift soil enzyme activity and allocation patterns in a wet tropical forest , 2013, Biogeochemistry.

[84]  Andrew Simon,et al.  The role of soil processes in determining mechanisms of slope failure and hillslope development in a humid-tropical forest eastern Puerto Rico , 1990 .

[85]  T. Daufresne,et al.  SCALING OF C:N:P STOICHIOMETRY IN FORESTS WORLDWIDE: IMPLICATIONS OF TERRESTRIAL REDFIELD‐TYPE RATIOS , 2004 .

[86]  R. Sinsabaugh,et al.  The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil , 2002 .

[87]  A. Mccarthy,et al.  Actinomycetes as agents of biodegradation in the environment--a review. , 1992, Gene.

[88]  B. Griffiths,et al.  Soil microbial community structure: Effects of substrate loading rates , 1998 .

[89]  P. Vitousek,et al.  Responses of extracellular enzymes to simple and complex nutrient inputs , 2005 .

[90]  Peter D. Nichols,et al.  Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments , 1985 .

[91]  M. Kleber,et al.  Stabilisation of soil organic matter by interactions with minerals as revealed by mineral dissolution and oxidative degradation , 2003 .

[92]  A. Konopka,et al.  Surface and subsurface microbial biomass, community structure and metabolic activity as a function of soil depth and season , 2002 .

[93]  C. Cleveland,et al.  C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? , 2007 .

[94]  S. Allison,et al.  Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies , 2011 .

[95]  D. Bates,et al.  Linear Mixed-Effects Models using 'Eigen' and S4 , 2015 .

[96]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[97]  Julie E. Jones,et al.  Interactions between crop residue and soil organic matter quality and the functional diversity of soil microbial communities , 2002 .

[98]  S. Christensen,et al.  Distribution with depth of protozoa, bacteria and fungi in soil profiles from three Danish forest sites , 2001 .

[99]  S. Geisser,et al.  On methods in the analysis of profile data , 1959 .

[100]  B. Hill,et al.  Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment , 2009, Nature.

[101]  S. Brantley,et al.  Phosphorus and iron cycling in deep saprolite, Luquillo Mountains, Puerto Rico , 2010 .