Evolutionary-Economic Principles as Regulators of Soil Enzyme Production and Ecosystem Function

Allison, Steven D.; Weintraub, Michael N.; Gartner, Tracy B.; Waldrop, Mark P.

doi:10.1007/978-3-642-14225-3_12

Cited by 235 publications

(241 citation statements)

References 75 publications

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“…In support of our hypothesis, we found a significant association between the ability to hydrolyze chitin and use the end products of hydrolysis, regardless of whether we corrected for shared evolutionary history. Allocation to extracellular enzymes represents a significant investment of carbon and nitrogen, and cells should be under selection to regulate production and maximize substrate use (Allison et al, 2007(Allison et al, , 2011. Most of the Vibrio genomes in our data set were capable of complete chitin hydrolysis, which is consistent with their known ecology.…”

Section: Discussionsupporting

confidence: 63%

Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes

2013

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Understanding the relationship between prokaryotic traits and phylogeny is important for predicting and modeling ecological processes. Microbial extracellular enzymes have a pivotal role in nutrient cycling and the decomposition of organic matter, yet little is known about the phylogenetic distribution of genes encoding these enzymes. In this study, we analyzed 3058 annotated prokaryotic genomes to determine which taxa have the genetic potential to produce alkaline phosphatase, chitinase and b-N-acetyl-glucosaminidase enzymes. We then evaluated the relationship between the genetic potential for enzyme production and 16S rRNA phylogeny using the consenTRAIT algorithm, which calculated the phylogenetic depth and corresponding 16S rRNA sequence identity of clades of potential enzyme producers. Nearly half (49.2%) of the genomes analyzed were found to be capable of extracellular enzyme production, and these were non-randomly distributed across most prokaryotic phyla. On average, clades of potential enzymeproducing organisms had a maximum phylogenetic depth of 0.008004-0.009780, though individual clades varied broadly in both size and depth. These values correspond to a minimum 16S rRNA sequence identity of 98.04-98.40%. The distribution pattern we found is an indication of microdiversity, the occurrence of ecologically or physiologically distinct populations within phylogenetically related groups. Additionally, we found positive correlations among the genes encoding different extracellular enzymes. Our results suggest that the capacity to produce extracellular enzymes varies at relatively fine-scale phylogenetic resolution. This variation is consistent with other traits that require a small number of genes and provides insight into the relationship between taxonomy and traits that may be useful for predicting ecological function.

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Section: Discussionsupporting

confidence: 63%

Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes

2013

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“…Soil EEA's are commonly studied to relate shifts in microbial function to soil nutrient cycling; useful indicators to assess microbial nutrient demands in response to climate change, plant community shifts, and more broadly ecosystem functioning [31][32][33] . EEA stoichiometry has been more recently adopted as an index to assess soil biochemical nutrient cycling by intersecting ecological stoichiometric theory and metabolic theory of ecology to assess potential microbial nutrient imbalances corresponding to environmental conditions 5 .…”

Section: Introductionmentioning

confidence: 99%

High-throughput Fluorometric Measurement of Potential Soil Extracellular Enzyme Activities

Bell

Fricks

Rocca

et al. 2013

JoVE

278

224

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Microbes in soils and other environments produce extracellular enzymes to depolymerize and hydrolyze organic macromolecules so that they can be assimilated for energy and nutrients. Measuring soil microbial enzyme activity is crucial in understanding soil ecosystem functional dynamics. The general concept of the fluorescence enzyme assay is that synthetic C-, N-, or P-rich substrates bound with a fluorescent dye are added to soil samples. When intact, the labeled substrates do not fluoresce. Enzyme activity is measured as the increase in fluorescence as the fluorescent dyes are cleaved from their substrates, which allows them to fluoresce. Enzyme measurements can be expressed in units of molarity or activity. To perform this assay, soil slurries are prepared by combining soil with a pH buffer. The pH buffer (typically a 50 mM sodium acetate or 50 mM Tris buffer), is chosen for the buffer's particular acid dissociation constant (pKa) to best match the soil sample pH. The soil slurries are inoculated with a nonlimiting amount of fluorescently labeled (i.e. C-, N-, or P-rich) substrate. Using soil slurries in the assay serves to minimize limitations on enzyme and substrate diffusion. Therefore, this assay controls for differences in substrate limitation, diffusion rates, and soil pH conditions; thus detecting potential enzyme activity rates as a function of the difference in enzyme concentrations (per sample).Fluorescence enzyme assays are typically more sensitive than spectrophotometric (i.e. colorimetric) assays, but can suffer from interference caused by impurities and the instability of many fluorescent compounds when exposed to light; so caution is required when handling fluorescent substrates. Likewise, this method only assesses potential enzyme activities under laboratory conditions when substrates are not limiting. Caution should be used when interpreting the data representing cross-site comparisons with differing temperatures or soil types, as in situ soil type and temperature can influence enzyme kinetics.

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“…Upregulated enzyme production can compensate for diffusive loss of enzymes, thereby increasing enzyme substrate encounter rates closer to the cell and resulting in more monomers being harvested by the cell. Producing more enzymes, however, is an expensive way to optimize the yield of an enzyme strategy, since it will increase the cell's demand for nutrients and energy (43)(44)(45). Substrate (energy) availability for microbes decreases with depth in the ocean (1), so particularly for deep-sea bacteria, increased production rates will not be beneficial, especially when considering the yield of monomers obtained through attached enzymes (i.e., decrease of enzyme diffusivity).…”

Section: Figmentioning

confidence: 99%

A Model of Extracellular Enzymes in Free-Living Microbes: Which Strategy Pays Off?

Traving

Thygesen

Riemann

et al. 2015

Appl Environ Microbiol

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An initial modeling approach was applied to analyze how a single, nonmotile, free-living, heterotrophic bacterial cell may optimize the deployment of its extracellular enzymes. Free-living cells live in a dilute and complex substrate field, and to gain enough substrate, their extracellular enzymes must be utilized efficiently. The model revealed that surface-attached and free enzymes generate unique enzyme and substrate fields, and each deployment strategy has distinctive advantages. For a solitary cell, surface-attached enzymes are suggested to be the most cost-efficient strategy. This strategy entails potential substrates being reduced to very low concentrations. Free enzymes, on the other hand, generate a radically different substrate field, which suggests significant benefits for the strategy if free cells engage in social foraging or experience high substrate concentrations. Swimming has a slight positive effect for the attached-enzyme strategy, while the effect is negative for the free-enzyme strategy. The results of this study suggest that specific dissolved organic compounds in the ocean likely persist below a threshold concentration impervious to biological utilization. This could help explain the persistence and apparent refractory state of oceanic dissolved organic matter (DOM). Microbial extracellular enzyme strategies, therefore, have important implications for larger-scale processes, such as shaping the role of DOM in ocean carbon sequestration. Dissolved organic matter (DOM) in the oceans is one of the largest active reservoirs of organic carbon in the biosphere (1). An intricate web of biotic (e.g., photosynthesis, viral lysis, and grazing) and abiotic (e.g., photodegradation and aggregation) processes contribute to the physical and chemical complexity of DOM (2-4). However, DOM is almost exclusively exploited by the bacterioplankton (5, 6). Microbes face several challenges when consuming DOM. While small molecules approximately 600 to 800 Da in size can be taken up directly (7,8), larger compounds need to be enzymatically hydrolyzed outside the cell before uptake. This two-phase system of hydrolysis and subsequent uptake is a rate-limiting step of microbial enzymatic degradation (9-11), and a mechanistic understanding of these processes, therefore, is of global biogeochemical relevance. Furthermore, the bacterioplankton are faced with the challenges of spatial heterogeneity (12, 13) and individual compounds at extremely dilute concentrations (14-16). For a microbe, there is presumably a delicate balance between the substrate encounter rate and the energy cost associated with carrying and maintaining an enzymatic apparatus for substrate uptake.It has been proposed that bacteria have adapted to the "landscape" of marine DOM by two very different trophic strategies. Copiotrophs use a "feast and famine" strategy where they proliferate from low abundances upon exposure to high substrate levels (17), such as in association with detrital aggregates or phytoplankton blooms. Copiotrophs are distinguished...

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Evolutionary-Economic Principles as Regulators of Soil Enzyme Production and Ecosystem Function

Cited by 235 publications

References 75 publications

Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes

Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes

High-throughput Fluorometric Measurement of Potential Soil Extracellular Enzyme Activities

A Model of Extracellular Enzymes in Free-Living Microbes: Which Strategy Pays Off?

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