Making the most of microbes


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Microorganisms carry out a large number of fundamental processes that underpin ecosystem function. Aside from their importance as symbionts or pathogens of all macro-organisms, microbes influence ecosystem function through the decomposition of organic matter and the subsequent cycling of carbon and nutrients. The enormous diversity and high functional overlap of soil microbes in particular makes this an exciting but challenging area of research in functional ecology. Over 20 years ago, Fenchel (1992) delivered a Tansley Lecture on what ecologists could learn from microbes. This virtual issue takes a look at some of the subsequent advances in ecosystem research, which have been made possible by considering microbial processes and populations within the bigger picture of ecosystem function.

The importance of microbial communities in ecosystem function has been highlighted in recent decades by the recognition that microbially-mediated responses to change will determine future rates of carbon storage and the emission of biogenic greenhouse gases. In their seminal paper, Lloyd and Taylor (1994) demonstrated that the temperature sensitivity of soil respiration could be described by the empirical relationship between increasing activation energy with decreasing temperature. This paved the way for realistic simulations of changes in net ecosystem productivity and its effect on atmospheric CO2 concentrations. A decade later, Allen, Gilooly and Brown (2005) proposed a model incorporating the constraints imposed by temperature and body size on individual metabolic rate to show that the global carbon balance is governed by links between cellular-, individual- and community-level processes. They predicted a net loss of labile carbon from soils with increasing temperature because the consumption of carbon by heterotrophs increases more rapidly with temperature than does plant productivity.

Rapid movement of carbon through the soil food web and the high taxonomic diversity of soil organisms could make the belowground subsystem highly resistant to perturbation (Fitter et al. 2005) but there is still a long way to go before we can fully assess the importance of taxonomic diversity for maintaining soil functions under change. For example, elevated atmospheric CO2 accelerated and increased the flow of recently assimilated carbon through the microbial community in a lowland grassland ecosystem but did not result in substantial changes in microbial community composition (Staddon et al. 2014). The accelerated carbon turnover without concomitant changes in carbon use by microbial functional groups was attributed to greater soil microbial biomass in response to elevated CO2. Conversely, Whitaker et al. (2014) found that soil respiration responses to altered carbon inputs along an elevation gradient in the Andes were best explained by changes in the relative abundances of microbial functional groups.

Some discrepancies may be explained by our lack of understanding of important feedback processes. One such feedback occurs when inputs of labile carbon stimulate the mineralisation and release of stored soil organic carbon through so-called 'priming effects', which could accelerate soil carbon turnover under elevated CO2. The mechanisms underlying priming effects have yet to be determined conclusively but a recent experiment found no evidence of links to microbial growth dynamics or succession of microbial r- and K-strategists (Rousk et al. 2015). The authors proposed that altered extracellular enzyme activity, rather than changes in broad microbial groups, may drive soil organic matter transformations during priming effects. However, shifts within microbial groups or among microorganisms with greater resource-specificity may be more revealing, especially when their links to plants are considered. For example, in a simple model system with different assemblages of rhizosphere bacteria, higher enzyme activity was associated with higher soil bacterial diversity, which increased nitrogen mineralization and enhanced plant productivity, creating a positive feedback on bacterial growth (Weidner et al. 2015). Furthermore, differences in resource-use among soil microbial functional groups create distinct 'energy channels' within the soil food web. Pollierer et al. (2012) used stable isotope labelling to show that root-derived carbon enters the soil animal food web mainly via feeding on ectomycorrhizal fungi but a considerable amount of carbon also entered higher trophic levels through the bacterial energy channel. Collectively, these findings suggest that a better understanding of microbial resource-use and the corresponding flows of energy and nutrients through the soil may help us determine the functional consequences of shifts in microbial communities.

Specific microbial functional groups and feedbacks between plants and microbes may contribute to the conservation of soil nutrients in some systems. Kinzig and Harte (1998) investigated potential feedbacks between plants and different functional groups of soil bacteria and concluded that selection for 'strategic' rather than 'voracious' microbial types would enhance plant productivity and thus increase microbial access to plant-derived carbon. Their simulations suggested that 'strategic' microbes could persist in spatially explicit environments with low levels of disturbance and the mutual benefit could result in plants actively promoting selection of strategic microbial types. It is conceivable that such a feedback mechanism contributes to the formation of 'fertility islands' in tropical arid ecosystems, where soils beneath plants have high concentrations of N and organic matter. The persistence of fertility islands was attributed to net immobilization in the microbial biomass and heterotrophic microbial activity, whereas the size of the carbon and nitrogen pools was linked to inputs of plant material to the soil (Perroni-Ventura et al. 2010).

Microbial nitrogen transformations, such as biological di-nitrogen fixation, also play an important role in the accumulation of nitrogen in the soil during ecosystem development at both early- and late successional stages. Indeed, during ecosystem retrogression in a boreal forest chronosequence, the amount of total nitrogen input through biological fixation increased to levels comparable to atmospheric nitrogen deposition (Lagerstrom et al. 2007). Global change therefore has the potential to substantially alter the nitrogen cycle in different ecosystems via direct and indirect effects on plant symbionts and other soil microorganisms. Barnard et al. (2006) measured strong responses of nitrifying and denitrifying enzyme activity to single and combined climate change treatments in a Mediterranean grassland, which were likely to modify ecosystem nitrogen cycling under a range of different global change scenarios. In a rainfall manipulation experiment, soil nitrogen transformations were influenced by plant species and water availability via interactions among plant transpiration rates, nutrient uptake and microbial activity in the soil (Cregger et al. 2014).Just as microbial processes control the cycling of elements within ecosystems, extraneous changes in resource levels also affect microbial communities and function. Land-use change and increasing atmospheric deposition of nutrients in tropical regions have the potential to disrupt the 'tight' nutrient cycle in lowland tropical forests. The balance of available carbon, nitrogen and phosphorus in particular play an important part in controlling microbial community structure and their associated functions (Fanin et al. 2015). Recent fertilization experiments in tropical forests in French Guiana and China produced a shift towards decomposer-dominated microbial communities and accelerated decomposition of carbon-rich materials (cellulose or coarse woody debris) in response to the addition of phosphorus (Fanin et al. 2015; Chen et al. in press). Although the combined addition of nitrogen and phosphorus had similar or stronger effects than phosphorus alone, nitrogen-fertilization alone did not affect decomposition rates, underlining the importance of elemental stoichiometry for decomposer communities.

Last but not least, microbial ecology provides opportunities for experiments that would be difficult or unfeasible using macroorganisms (Fenchel 1992). The fast turnover times and high adaptive capacities of microorganisms make them a useful tool for model systems to investigate evolutionary and ecological processes. Zhang et al. (2009) tested how niche and neutral mechanisms promote diversity in microcosms with isogenic bacterial populations that were able to diversify into different phenotypes. By treating the phenotypes as analogues of species, they assessed the relative importance of stabilising and equalising mechanisms on phenotypic diversity in the microcosms and used their results to generate hypotheses about the roles of niche and neutral processes for maintaining ecosystem biodiversity and productivity. In a similar vein, Eisenhauer et al. (2013) used variation in the resource use of different bacterial genotypes in model systems to test predictions about the relationship between resource availability and invasibility. Their findings highlight the potential importance of functional diversity and the resulting efficiency of resource use for protecting systems against invasive species.

In conclusion, the study of microbes still has much to offer general ecological research (Fenchel 1992). Due consideration of microbial communities and function is particularly important for assessing changes in ecosystem elemental cycling, species interactions, and successional patterns. Technological advances have greatly improved our understanding of microbial processes but more fundamental research on microbial communities and functions will help us better comprehend ecosystem responses to change.

References and context 


Allen et al. (2005) Linking the global carbon cycle to individual metabolism. Functional Ecology 19: 202-213. 

Barnard et al. (2006) Several components of global change alter nitrifying and denitrifying activities in an annual grassland. Functional Ecology 20: 557-564. 

Chen et al. (in press). Nutrient limitation of woody debris decomposition in a tropical forest: Contrasting effects of N and P addition. Functional Ecology, doi: 10.1111/1365-2435.12471

Cregger et al. (2014) The impact of precipitation change on nitrogen cycling in a semi-arid ecosystem. Functional Ecology 28: 1534-1544.

Eisenhauer et al. (2013) Niche dimensionality links biodiversity and invasibility of microbial communities. Functional Ecology 27: 282-288.

Fanin et al. (2015) Interactive effects of C, N and P fertilization on soil microbial community structure and function in an Amazonian rain forest. Functional Ecology 29: 140-150.

Fenchel (1992) What can ecologists learn from microbes? Life beneath a square centimeter of sediment surface. Functional Ecology 6: 499-507.

Fitter et al. (2005) Biodiversity and ecosystem function in soil. Functional Ecology 19: 369-377. 

Kinzig et al. (1998) Selection of micro-organisms in a spatially explicit environment and implications for plant access to nitrogen. Journal of Ecology 86: 841-853.

Lagerstrom et al. (2007) Ecosystem input of nitrogen through biological fixation in feather mosses during ecosystem retrogression. Functional Ecology 21: 1027-1033

Lloyd & Taylor (1994) On the temperature-dependence of soil respiration. Functional Ecology 8: 315-323

Perroni-Ventura et al. (2010) Carbon-nitrogen interactions in fertility island soil from a tropical semi-arid ecosystem. Functional Ecology 24: 233-242

Pollierer et al. (2012) Carbon flux through fungi and bacteria into the forest soil animal food web as indicated by compound-specific 13C fatty acid analysis. Functional Ecology 26: 978-990

Rousk et al. (2015), Priming of the decomposition of ageing soil organic matter: concentration dependence and microbial control. Functional Ecology 29: 285–296.

Staddon et al. (2014) A decade of free-air CO2 enrichment increased the carbon throughput in a grass-clover ecosystem but did not drastically change carbon allocation patterns. Functional Ecology 28: 538-545.

Weidner et al. (2015). Bacterial diversity amplifies nutrient-based plant–soil feedbacks. Functional Ecology.

Whitaker et al. (2014) Microbial community composition explains soil respiration responses to changing carbon inputs along an Andes-to-Amazon elevation gradient. Journal of Ecology 102: 1058-1071.

Zhang et al. (2009) Quantifying the relative importance of niches and neutrality for coexistence in a model microbial system. Functional Ecology 23: 1139-1147.



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