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Soil Extracellular Enzyme Activities Correspond with Abiotic Factors More Than Fungal Community Composition

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Soil Extracellular Enzyme Activities Correspond with Abiotic Factors More Than Fungal Community Composition Biogeochemistry (2014) 117:23–37 DOI 10.1007/s10533-013-9852-2 Soil extracellular enzyme activities correspond with abiotic factors more than fungal community composition Stephanie N. Kivlin • Kathleen K. Treseder Received: 1 November 2012 / Accepted: 13 April 2013 / Published online: 20 April 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract Soil extracellular enzymes are the proxi- at the species, genus, family or order levels. The mal drivers of decomposition. However, the relative hyphal length of fungi was correlated with EEA during influence of climate, soil nutrients and edaphic factors the growing season while relative abundance of taxa compared to microbial community composition on within fungal phyla, in particular Chytridiomycota, extracellular enzyme activities (EEA) is poorly was correlated with the EEA of beta-glucosidase, resolved. Determining the relative effects of these cellobiohydrolase, acid phosphatase and beta-xylosi- factors on soil EEA is critical since changes in climate dase in the dry season. Overall, in the dry season, and microbial species composition may have large 35.3 % of the variation in all enzyme activities was impacts on decomposition. We measured EEA from accounted for by abiotic variables, while fungal five sites during the growing season in March and 17 composition accounted for 27.4 %. Because global sites during the dry season in July throughout southern change is expected to alter precipitation regimes and California and simultaneously collected data on increase nitrogen deposition in soils, EEA may be climate, soil nutrients, soil edaphic factors and fungal affected, with consequences for decomposition. community composition. The concentration of carbon and nitrogen in the soil and soil pH were most related Keywords 454 pyrosequencing Á Climate Á Deserts Á to hydrolytic EEA. Conversely, oxidative EEA was Mediterranean ecosystems Á Soil nutrients Á Soil pH mostly related to mean annual precipitation. Fungal community composition was not correlated with EEA Introduction Extracellular enzymes are the proximal drivers of decomposition in soils (Sinsabaugh et al. 2008). Electronic supplementary material The online version of this article (doi:10.1007/s10533-013-9852-2) contains Traditionally, soil extracellular enzyme activity supplementary material, which is available to authorized users. (EEA) has been explained by correlations with abiotic factors (Sinsabaugh et al. 2008); however, because soil S. N. Kivlin Á K. K. Treseder Ecology and Evolutionary Biology, University of fungi are responsible for a large portion of enzyme California Irvine, Irvine, CA 92697, USA production (Schneider et al. 2012), they may also play a role in determining soil EEA. The relative influence & S. N. Kivlin ( ) of abiotic factors such as climate, soil pH, and soil Section of Integrative Biology, Patterson Labs, University of Texas at Austin, Austin, TX 78712, USA nutrient concentrations compared to fungal commu- e-mail: [email protected] nity composition on EEA is unknown. Understanding 123 24 Biogeochemistry (2014) 117:23–37 the drivers of EEA is critical, as EEA can impact the growing season (Averill and Finzi 2011). Taken decomposition in current and future climates and together, this evidence predicts that soil EEA should global change conditions. be highest during the growing season and lowest Correlations between abiotic factors and soil EEA during the dry season. However, synthesis based on have been examined more thoroughly than the rela- previous studies remains enigmatic. While some tionships between microbial communities and EEA. evidence supports seasonal variability in EEA that For example, in a synthesis of 40 studies, EEA was corresponds to C and nutrient availability (Boerner largely affected by soil organic matter content, soil et al. 2005; Wallenstein et al. 2009), other studies have pH, and climate (Sinsabaugh et al. 2008). Soil nutrient shown the EEA can actually increase in the nutrient- and carbon (C) concentrations may affect soil EEA poor dry seasons (Parker and Schimel 2011), which through a variety of mechanisms. Stoichiometric has been suggested as a microbial increase in EEA constraints on soil microorganism biomass (Cleveland production in anticipation of rain events. Still other and Liptzin 2007) may influence EEA, such that soil studies observe no seasonality in EEA (Choi et al. microorganisms produce enzymes to target the most 2009). limiting nutrient (Allison and Vitousek 2005; Sinsab- While the impact of climatic and soil factors on soil augh and Moorhead 1994). Alternatively, soil C and EEA have received much attention, the role of nutrient stoichiometry may predict EEA based on microbial community composition on EEA is less microbial demands (Sinsabaugh et al. 2009), such that well understood. Recent meta-genomic and proteomic EEA of C-acquiring enzymes is positively correlated studies have shown that fungi produce the majority of with nitrogen (N) and phosphorus (P) acquiring extracellular enzymes in litter and soil that degrade enzymes in a 1:1:1 ratio. Soil pH can also have large labile and recalcitrant C, organic N, and organic P impacts on EEA. Extracellular enzymes have pH polymers (Schneider et al. 2012, 2010). This supports optima where the active site is in the most operative previous research showing that soil fungi comprise a conformation (Leprince and Quiquampoix 1996). For significant portion of microbial biomass belowground example, glycosidases have an optimal pH of *5, (Joergensen and Wichern 2008; Strickland and Rousk whereas polyphenol oxidase and peroxidase have their 2010) and regulate C and nutrient cycling in terrestrial highest activity at a pH of *8 (Frankenberger and ecosystems (Hattenschwiler et al. 2005). Numerous Johanson 1982). studies have found significant correlations between Climate may also influence EEA. Enzyme activities phospholipid fatty acid (PLFA) profiles and EEA normally increase with higher temperatures up to an (DeForest et al. 2012; Waldrop et al. 2000; Brockett optimum [40 °C (Stone et al. 2012). Similarly, EEA et al. 2012; Kourtev et al. 2003), but a mechanistic can be affected by soil water concentrations via understanding of how EEA may change among fungal changes in the diffusion rate of substrates and groups is still unclear. Soil EEA may also be inhibitory compounds (Zak et al. 1999; Toberman influenced by microbial groups that are not delineated et al. 2008). At global scales, temperature may be by their fatty acid profiles. For example, soil decom- more influential than moisture in determining EEA poser communities may impact EEA if different (German et al. 2012); at regional scales, however, functional groups produce disparate suites of changes in soil moisture may become more important. enzymes, (i.e., opportunists, decomposers, and miners For example, in a study across seven forests, Brockett (Moorhead and Sinsabaugh 2006). Moreover, oxida- et al. (2012) found that soil moisture was the most tive and hydrolytic enzymes may be produced by consistent predictor of both hydrolytic and oxidative different fungal phyla, as the abundance of Basidio- EEA. mycota is often positively correlated with the activity Soil EEA may also vary seasonally. In southern of oxidative enzymes (Frey et al. 2004). While California, soil moisture and nutrient concentrations correlations between fungal PLFA profiles and EEA can vary two-fold between the growing and dry season are well documented, the relationships between fine- (Parker and Schimel 2011). Plants can also act as scale fungal community composition and EEA have priming agents to stimulate EEA production during not been directly examined in natural systems. Disen- 123 Biogeochemistry (2014) 117:23–37 25 tangling the relative influence of abiotic factors and Materials and methods fungal composition on EEA remains difficult as fungal composition varies over geographic space and We collected five 2.5 9 10 cm soil cores in March between habitats (Lauber et al. 2008). Therefore the 2010 from five sites and in July 2010 from 17 sites environment may indirectly influence EEA through throughout southern California, between 34.61°N, shifts in fungal community composition. Indeed, in 120.23°W; 34.15°N, 116.46°W; and 33.46°N, recent global syntheses, fungal community composi- 117.04°W (Table 1). Our sites included a variety of tion in soils was largely affected by climate and soil ecosystems (grasslands, scrublands, deserts and for- edaphic factors (Tedersoo et al. 2012; Kivlin et al. ests) over a spatial scale large enough to vary in 2011). climate and soil parameters, but small enough to Here, we specifically examined the correlations potentially observe fungal dispersal between sites between abiotic factors, fungal community composi- (Brown and Hovmoeller 2002; Peay et al. 2012). At tion and soil EEA by analyzing EEA in response to each site, we collected the following abiotic variables: ? - both factors (abiotic v. fungal composition) sepa- soil pH, soil C and N, soil NH4 and NO3 , soil 3- rately and concurrently across a variety of ecosys- PO4 , soil moisture, MAP, latitude, longitude, and tems. A subset of enzymes and sites were measured at elevation. We also assayed fungal community com- two time points, March and July, to understand how position at the species, genus, family and order level of seasonality may affect EEA. We predicted that all resolution, and as differences between the relative EEA would be positively correlated to soil nutrient abundance of each phylum. A
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