Teri C. Balser

Integrating microbial ecology into ecosystem models: challenges and priorities

Microbial communities can potentially mediate feedbacks between global change and ecosystem function, owing to their sensitivity to environmental change and their control over critical biogeochemical processes. Numerous ecosystem models have been developed to predict global change effects, but most do not consider microbial mechanisms in detail. In this idea paper, we examine the extent to which incorporation of microbial ecology into ecosystem models improves predictions of carbon (C) dynamics under warming, changes in precipitation regime, and anthropogenic nitrogen (N) enrichment. We focus on three cases in which this approach might be especially valuable: temporal dynamics in microbial responses to environmental change, variation in ecological function within microbial communities, and N effects on microbial activity. Four microbially-based models have addressed these scenarios. In each case, predictions of the microbial-based models differ—sometimes substantially—from comparable conventional models. However, validation and parameterization of model performance is challenging. We recommend that the development of microbial-based models must occur in conjunction with the development of theoretical frameworks that predict the temporal responses of microbial communities, the phylogenetic distribution of microbial functions, and the response of microbes to N enrichment.

Linking soil process and microbial ecology in freshwater wetland ecosystems

Soil microorganisms mediate many processes such as nitrification, denitrification, and methanogenesis that regulate ecosystem functioning and also feed back to influence atmospheric chemistry. These processes are of particular interest in freshwater wetland ecosystems where nutrient cycling is highly responsive to fluctuating hydrology and nutrients and soil gas releases may be sensitive to climate warming. In this review we briefly summarize research from process and taxonomic approaches to the study of wetland biogeochemistry and microbial ecology, and highlight areas where further research is needed to increase our mechanistic understanding of wetland system functioning. Research in wetland biogeochemistry has most often been focused on processes (e.g., methanogenesis), and less often on microbial communities or on populations of specific microorganisms of interest. Research on process has focused on controls over, and rates of, denitrification, methanogenesis, and methanotrophy. There has been some work on sulfate and iron transformations and wetland enzyme activities. Work to date indicates an important process level role for hydrology and soil nutrient status. The impact of plant species composition on processes is potentially critical, but is as yet poorly understood. Research on microbial communities in wetland soils has primarily focused on bacteria responsible for methanogenesis, denitrification, and sulfate reduction. There has been less work on taxonomic groups such as those responsible for nitrogen fixation, or aerobic processes such as nitrification. Work on general community composition and on wetland mycorrhizal fungi is particularly sparse. The general goal of microbial research has been to understand how microbial groups respond to the environment. There has been relatively little work done on the interactions among environmental controls over process rates, environmental constraints on microbial activities and community composition, and changes in processes at the ecosystem level. Finding ways to link process-based and biochemical or gene-based assays is becoming increasingly important as we seek a mechanistic understanding of the response of wetland ecosystems to current and future anthropogenic perturbations. We discuss the potential of new approaches, and highlight areas for further research.

MICROBIAL COMMUNITY VARIATION AND ITS RELATIONSHIP WITH NITROGEN MINERALIZATION IN HISTORICALLY ALTERED FORESTS

Past land use can impart soil legacies that have important implications for ecosystem function. Although these legacies have been linked with microbially mediated processes, little is known about the long-term influence of land use on soil microbial communities themselves. We examined whether historical land use affected soil microbial community composition (lipid profiles) and whether community composition was related to potential net nitrogen (N) mineralization rates in southern Appalachian (USA) forest stands abandoned from agriculture or logging and reforested >50 yr ago. Microbial community composition was determined by a hybrid procedure of phospholipid fatty acid (PLFA) and fatty acid methyl ester (FAME) analysis. We found that community composition varied significantly with past land use. Communities in formerly farmed stands had a higher relative abundance of markers for gram-negative bacteria and a lower abundance of markers for fungi compared with previously logged and reference (i.e., no disturbance history) stands. Potential net N mineralization rates were negatively correlated with fungal and gram-negative bacterial markers in both farmed and reference stands, and fungal abundance and soil bulk density effectively predicted mineralization rates in all stands. Our results indicate that the alteration of microbial communities by historical land use may influence the ecosystem processes they mediate. This is in contrast to typical expectations about microbial community resilience to change. Here, the decrease in fungal abundance observed from disturbance appeared to result in decreased nitrogen mineralization over the long term.

Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy.

Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy

Microbial response over time to hydrologic and fertilization treatments in a simulated wet prairie

Naturally occurring wetlands are often threatened by runoff from urban areas, while constructed wetlands are increasingly used to filter sediments and nutrients from urban runoff. To analyze the potential effects of urban runoff on wetland soil microbial activity and composition, we combined phospholipid fatty acid analysis (PLFA) with assays of enzyme activities and nitrification potential (indicators of microbial function) in constructed wetland mesocosms. Mesocosm treatments included nutrient addition treatments (high, low, and none) and hydologic regimes (constant flood, early season flood, and intermittent flood) in a full factorial design. We found that changes in hydrologic regime affected both structural (membrane lipid) and functional (enzyme activities and nitrification potentials) aspects of the microbial community to a greater degree than did nutrient additions. For example, the arbuscular mycorrhizal fungal (AMF) lipid indicator appeared to be highly sensitive to constant flooding. Although hydologic treatments were the dominant factor affecting microbial community structure and function, nutrient additions did appear to alter fungal lipid biomarkers (both mycorrhizal and saprotrophic) and nitrification potentials. In addition, samples taken between June and September indicated a seasonal/temporal progression; for example the effect of the early season flood treatment subsided after flooding ended. Finally, correlation between structure and function data indicate that the study of microbial community structure, in addition to function, may be important for understanding wetland ecosystem function.

Bridging the gap between micro - and macro-scale perspectives on the role of microbial communities in global change ecology

In order to understand the role microbial communities play in mediating ecosystem response to disturbances it is essential to address the methodological and conceptual gap that exists between micro- and macro-scale perspectives in ecology. While there is little doubt microorganisms play a central role in ecosystem functioning and therefore in ecosystem response to global change-induced disturbance, our ability to investigate the exact nature of that role is limited by disciplinary and methodological differences among microbial and ecosystem ecologists. In this paper we present results from an interdisciplinary graduate-level seminar class focused on this topic. Through the medium of case studies in global change ecology (soil respiration, nitrogen cycling, plant species invasion and land use/cover change) we highlight differences in our respective approach to ecology and give examples where disciplinary perspective influences our interpretation of the system under study. Finally, we suggest a model for integrating perspectives that may lead to greater interdisciplinary collaboration and enhanced conceptual and mechanistic modeling of ecosystem response to disturbance.

Effect of plant materials on microbial transformation of amino sugars in three soil microcosms

Amino sugars, being predominantly of microbial origin, can help elucidate the role of microbes in carbon and nitrogen cycling in soils. However, little is known about the microbial degradation and synthesis of soil amino sugars as affected by plant-derived organic materials. We conducted a 30-week microcosm study using three soils amended with soybean leaf or maize stalk to investigate changes in the amounts and patterns of amino sugars over time. The total soil amino sugar content initially increased during the incubation, but later decreased. Amino sugar content of soil amended with maize stalk peaked at an earlier time than it did for soybean leaf, suggesting nutrient quantity and substrate composition influence microbial transformation. Temporal dynamics of the proportion of total soil amino sugar to organic matter after plant material addition conformed to parabolic models (r > 0.8; p < 0.01), which tended to converge over time. The models predicted that the proportions would ultimately approach the initial values as determined before amendment. These findings suggest that soil organic matter has the ability to maintain a baseline steady-state level of amino sugars, and support the interpretation of soil amino sugar reservoir as two components: the Stable Pool (SP) and the Transition Pool (TP).

Net microbial amino sugar accumulation process in soil as influenced by different plant material inputs

Identifying the impact of plant material inputs on soil amino sugar synthesis may advance our knowledge of microbial transformation processes in soils. In a 12-week laboratory microcosm incubation, 1, 2, 4, and 6% (w/w) soybean leaf or maize stalk were initially added to soil, respectively, whereas soil without plant addition was used as a control. The results showed that adding organic materials to the soil led to a net accumulation of amino sugars, because of greater microbial synthesis. The ratios of glucosamine to galactosamine and of glucosamine to muramic acid, two indicators differentiating the relative contribution to soil organic matter of fungi and bacteria, showed substantial variance across the gradient of substrate addition. Our results suggest that the amount of nutrients in a given substrate is the primary attribute determining microbial net accumulation of soil amino sugars, especially in the relatively short term, whereas the composition of nutrients might be more important in the relatively long term when nutrients are not sufficient. The use of the two ratios (glucosamine to galactosamine and glucosamine to muramic acid) reflects different dynamics of galactosamine and muramic acid during the decomposition of organic substrates in soils. Muramic acid, compared with galactosamine, is more likely to accumulate in the soil active organic fraction under abundant nutrient conditions, whereas it would be decomposed along with active organic matter when the nutrients are scarce and remain in minor quantities in the clay fraction without being attacked by microbes.

Effects of condensed tannins in conifer leaves on the composition and activity of the soil microbial community in a tropical montane forest

Background and aimsCondensed tannins, a dominant class of plant secondary metabolites, play potentially important roles in plant-soil feedbacks by influencing the soil microbial community. Effects of condensed tannins on the soil microbial community and activity were examined by a short-term tannin-addition experiment under field and laboratory conditions.MethodsCondensed tannins were extracted from the leaves of a dominant conifer (Dacrydium gracilis) in a tropical montane forest on Mt. Kinabalu, Borneo. The extracted tannins were added to soils beneath the conifer and a dominant broadleaf (Lithocarpus clementianus) to evaluate the dependence of the response to tannin addition on the initial composition of the soil microbial community.ResultsEnzyme activities in the field tannin-addition treatment were lower than in the deionized-water treatment. Carbon and nitrogen mineralization were also inhibited by tannin-addition. The fungi-to-bacteria ratio after tannin-addition was higher compared with the distilled-water treatment in the laboratory experiment.ConclusionsBased on our results, we suggest that the higher concentration of condensed tannins in the leaf tissues of Dacrydium than in those of Lithocarpus is a factor influencing the microbial community and activity. This may have influences on subsequent plant performance, which induces plant-soil feedback processes that can control dynamics of the tropical montane forest ecosystem.

Soil fertility and the impact of exotic invasion on microbial communities in Hawaiian forests.

Exotic plant invasions into Hawaiian montane forests have altered many important nutrient cycling processes and pools. Across different ecosystems, researchers are uncovering the mechanisms involved in how invasive plants impact the soil microbial community—the primary mediator of soil nutrient cycling. We examined whether the invasive plant, Hedychium gardnerianum, altered microbial community composition in forests dominated by a native tree, Metrosideros polymorpha, under varying soil nutrient limitations and soil fertility properties within forest plots of the Hawaii long-term substrate age gradient (LSAG). Microbial community lipid analysis revealed that when nutrient limitation (as determined by aboveground net primary production [ANPP]) and soil fertility were taken into account, plant species differentially altered soil microbial community composition. Microbial community characteristics differed under invasive and native plants primarily when N or P was added to the older, highly weathered, P-limited soils. Long-term fertilization with N or P at the P-limited site led to a significant increase in the relative abundance of the saprophytic fungal indicator (18:2ω6c,9c) under the invasive plant. In the younger, N-limited soils, plant species played a minor role in influencing soil microbial community composition. We found that the general rhizosphere microbial community structure was determined more by soil fertility than by plant species. This study indicates that although the aggressive invasion of a nutrient-demanding, rapidly decomposable, and invasive plant into Hawaiian forests had large impacts on soil microbial decomposers, relatively little impact occurred on the overall soil microbial community structure. Instead, soil nutrient conditions were more important determinants of the overall microbial community structure within Hawaii’s montane forests.