Correlating the succession of microbial communities from Nigerian soils to petroleum biodegradation.

Whilst biodegradation of different hydrocarbon components has been widely demonstrated to occur by specialist oil-degrading bacteria, less is known about the impact on microbial communities as a function of oil composition by comparing the biodegradation of chemically complex fuels to synthetic products. The objectives of this study were (i) to assess the biodegradation capacity and succession of microbial communities isolated from Nigerian soils in media with crude oil or synthetic oil as sole sources of carbon and energy, and (ii) to assess the temporal variability of the microbial community size. Community profiling was done using 16 S rRNA gene amplicon sequencing (Illumina), and oil profiling using gas chromatography. The biodegradation of natural and synthetic oil differed probably due to the content of sulfur that may interfere with the biodegradation of hydrocarbons. Both alkanes and PAHs in the natural oil were biodegraded faster than in the synthetic oil. Variable community responses were observed during the degradation of alkanes and more simple aromatic compounds, but at later phases of growth they became more homogeneous. The degradation capacity and the size of the community from the more-contaminated soil were higher than those from the less-contaminated soil. Six abundant organisms isolated from the cultures were found to biodegrade oil molecules in pure cultures. Ultimately, this knowledge may contribute to a better understanding of how to improve the biodegradation of crude oil by optimizing culturing conditions through inoculation or bioaugmentation of specific bacteria during ex-situ biodegradation such as biodigesters or landfarming.

Arctic rooting depth distribution influences modelled carbon emissions but cannot be inferred from aboveground vegetation type.

The distribution of roots throughout the soil drives depth-dependent plant-soil interactions and ecosystem processes, particularly in arctic tundra where plant biomass, is predominantly belowground. Vegetation is usually classified from aboveground, but it is unclear whether such classifications are suitable to estimate belowground attributes and their consequences, such as rooting depth distribution and its influence on carbon cycling. We performed a meta-analysis of 55 published arctic rooting depth profiles, testing for differences both between distributions based on aboveground vegetation types (Graminoid, Wetland, Erect-shrub, and Prostrate-shrub tundra) and between 'Root Profile Types' for which we defined three representative and contrasting clusters. We further analyzed potential impacts of these different rooting depth distributions on rhizosphere priming-induced carbon losses from tundra soils. Rooting depth distribution hardly differed between aboveground vegetation types but varied between Root Profile Types. Accordingly, modelled priming-induced carbon emissions were similar between aboveground vegetation types when they were applied to the entire tundra, but ranged from 7.2 to 17.6 Pg C cumulative emissions until 2100 between individual Root Profile Types. Variations in rooting depth distribution are important for the circumpolar tundra carbon-climate feedback but can currently not be inferred adequately from aboveground vegetation type classifications.

Coevolutionary legacies for plant decomposition.

Coevolution has driven speciation and evolutionary novelty in functional traits across the Tree of Life. Classic coevolutionary syndromes such as plant-pollinator, plant-herbivore, and host-parasite have focused strongly on the fitness consequences during the lifetime of the interacting partners. Less is known about the consequences of coevolved traits for ecosystem-level processes, in particular their 'afterlife' legacies for litter decomposition, nutrient cycling, and the functional ecology of decomposers. We review the mechanisms by which traits resulting from coevolution between plants and their consumers, microbial symbionts, or humans, and between microbial decomposers and invertebrates, drive plant litter decomposition pathways and rates. This supports the idea that much of current global variation in the decomposition of plant material is a legacy of coevolution.

Evolution of manipulative microbial behaviors in the rhizosphere.

The rhizosphere has been called "one of the most complex ecosystems on earth" because it is a hotspot for interactions among millions of microbial cells. Many of these are microbes are also participating in a dynamic interplay with host plant tissues, signaling pathways, and metabolites. Historically, breeders have employed a plant-centric perspective when trying to harness the potential of microbiome-derived benefits to improve productivity and resilience of economically important plants. This is potentially problematic because: (i) the evolution of the microbes themselves is often ignored, and (ii) it assumes that the fitness of interacting plants and microbes is strictly aligned. In contrast, a microbe-centric perspective recognizes that putatively beneficial microbes are still under selection to increase their own fitness, even if there are costs to the host. This can lead to the evolution of sophisticated, potentially subtle, ways for microbes to manipulate the phenotype of their hosts, as well as other microbes in the rhizosphere. We illustrate this idea with a review of cases where rhizosphere microbes have been demonstrated to directly manipulate host root growth, architecture and exudation, host nutrient uptake systems, and host immunity and defense. We also discuss indirect effects, whereby fitness outcomes for the plant are a consequence of ecological interactions between rhizosphere microbes. If these consequences are positive for the plant, they can potentially be misconstrued as traits that have evolved to promote host growth, even if they are a result of selection for unrelated functions. The ubiquity of both direct microbial manipulation of hosts and context-dependent, variable indirect effects leads us to argue that an evolutionary perspective on rhizosphere microbial ecology will become increasingly important as we continue to engineer microbial communities for crop production.

Functional microbial ecology in arctic soils: the need for a year-round perspective.

The microbial ecology of arctic and sub-arctic soils is an important aspect of the global carbon cycle, due to the sensitivity of the large soil carbon stocks to ongoing climate warming. These regions are characterized by strong climatic seasonality, but the emphasis of most studies on the short vegetation growing season could potentially limit our ability to predict year-round ecosystem functions. We compiled a database of studies from arctic, subarctic, and boreal environments that include sampling of microbial community and functions outside the growing season. We found that for studies comparing across seasons, in most environments, microbial biomass and community composition vary intra-annually, with the spring thaw period often identified by researchers as the most dynamic time of year. This seasonality of microbial communities will have consequences for predictions of ecosystem function under climate change if it results in: seasonality in process kinetics of microbe-mediated functions; intra-annual variation in the importance of different (a)biotic drivers; and/or potential temporal asynchrony between climate change-related perturbations and their corresponding effects. Future research should focus on (i) sampling throughout the entire year; (ii) linking these multi-season measures of microbial community composition with corresponding functional or physiological measurements to elucidate the temporal dynamics of the links between them; and (iii) identifying dominant biotic and abiotic drivers of intra-annual variation in different ecological contexts.

Optimal growth temperature of Arctic soil bacterial communities increases under experimental warming.

Future climate warming in the Arctic will likely increase the vulnerability of soil carbon stocks to microbial decomposition. However, it remains uncertain to what extent decomposition rates will change in a warmer Arctic, because extended soil warming could induce temperature adaptation of bacterial communities. Here we show that experimental warming induces shifts in the temperature-growth relationships of bacterial communities, which is driven by community turnover and is common across a diverse set of 8 (sub) Arctic soils. The optimal growth temperature (Topt ) of the soil bacterial communities increased 0.27 ± 0.039 (SE) and 0.07 ± 0.028°C per °C of warming over a 0-30°C gradient, depending on the sampling moment. We identify a potential role for substrate depletion and time-lag effects as drivers of temperature adaption in soil bacterial communities, which possibly explain discrepancies between earlier incubation and field studies. The changes in Topt were accompanied by species-level shifts in bacterial community composition, which were mostly soil specific. Despite the clear physiological responses to warming, there was no evidence for a common set of temperature-responsive bacterial amplicon sequence variants. This implies that community composition data without accompanying physiological measurements may have limited utility for the identification of (potential) temperature adaption of soil bacterial communities in the Arctic. Since bacterial communities in Arctic soils are likely to adapt to increasing soil temperature under future climate change, this adaptation to higher temperature should be implemented in soil organic carbon modeling for accurate predictions of the dynamics of Arctic soil carbon stocks.

Toward a function-first framework to make soil microbial ecology predictive.

Soil microbial communities perform vital ecosystem functions, such as the decomposition of organic matter to provide plant nutrition. However, despite the functional importance of soil microorganisms, attribution of ecosystem function to particular constituents of the microbial community has been impeded by a lack of information linking microbial function to community composition and structure. Here, we propose a function-first framework to predict how microbial communities influence ecosystem functions. We first view the microbial community associated with a specific function as a whole and describe the dependence of microbial functions on environmental factors (e.g., the intrinsic temperature dependence of bacterial growth rates). This step defines the aggregate functional response curve of the community. Second, the contribution of the whole community to ecosystem function can be predicted, by combining the functional response curve with current environmental conditions. Functional response curves can then be linked with taxonomic data in order to identify sets of "biomarker" taxa that signal how microbial communities regulate ecosystem functions. Ultimately, such indicator taxa may be used as a diagnostic tool, enabling predictions of ecosystem function from community composition. In this paper, we provide three examples to illustrate the proposed framework, whereby the dependence of bacterial growth on environmental factors, including temperature, pH, and salinity, is defined as the functional response curve used to interlink soil bacterial community structure and function. Applying this framework will make it possible to predict ecosystem functions directly from microbial community composition.

Evidence for strong environmental control on bacterial microbiomes of Antarctic springtails.

Collembola are a key component of the soil biota globally, playing an important role in community and ecosystem dynamics. Equally significant are their associated microbiomes, that can contribute to key metabolic functions. In the present study, we investigated the bacterial community composition of four Antarctic springtail species to assess if and how the extreme Antarctic environment has shaped the collembolans' microbiomes. Springtails were collected from two biogeographical regions, the maritime and the continental Antarctic. From each region, two endemic species, belonging to the genera Cryptopygus (Isotomidae, Entomobryomorpha) and Friesea (Neanuridae, Poduromorpha), were included. This experimental design allowed us to quantify the relative importance of ecological factors (different regions of occurrence) and/or phylogenetic divergence in the host (different Orders) in shaping the Collembola microbiome. The diversity and richness of springtail microbiomes was lower in the Antarctic taxa compared to published information from species from temperate regions. The microbiome composition was predominantly species-specific, with a limited core microbiome shared across the four species examined. While both geographic origin and host species influenced the associated microbiomes, the former was the prevalent driver, with closer similarity between springtails from the same bioregion than between those belonging to the same genus.

Patterns of local, intercontinental and interseasonal variation of soil bacterial and eukaryotic microbial communities.

Although ongoing research has revealed some of the main drivers behind global spatial patterns of microbial communities, spatio-temporal dynamics of these communities still remain largely unexplored. Here, we investigate spatio-temporal variability of both bacterial and eukaryotic soil microbial communities at local and intercontinental scales. We compare how temporal variation in community composition scales with spatial variation in community composition, and explore the extent to which bacteria, protists, fungi and metazoa have similar patterns of temporal community dynamics. All soil microbial groups displayed a strong correlation between spatial distance and community dissimilarity, which was related to the ratio of organism to sample size. Temporal changes were variable, ranging from equal to local between-sample variation, to as large as that between communities several thousand kilometers apart. Moreover, significant correlations were found between bacterial and protist communities, as well as between protist and fungal communities, indicating that these microbial groups change in tandem, potentially driven by interactions between them. We conclude that temporal variation can be considerable in soil microbial communities, and that future studies need to consider temporal variation in order to reliably capture all drivers of soil microbiome changes.

A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem.

Temperature governs most biotic processes, yet we know little about how warming affects whole ecosystems. Here we examined the responses of 128 components of a subarctic grassland to either 5-8 or >50 years of soil warming. Warming of >50 years drove the ecosystem to a new steady state possessing a distinct biotic composition and reduced species richness, biomass and soil organic matter. However, the warmed state was preceded by an overreaction to warming, which was related to organism physiology and was evident after 5-8 years. Ignoring this overreaction yielded errors of >100% for 83 variables when predicting their responses to a realistic warming scenario of 1 °C over 50 years, although some, including soil carbon content, remained stable after 5-8 years. This study challenges long-term ecosystem predictions made from short-term observations, and provides a framework for characterization of ecosystem responses to sustained climate change.

Correction: Long-term in situ permafrost thaw effects on bacterial communities and potential aerobic respiration.

Since the publication of the original article, the authors noticed some errors in reference citation had been introduced throughout the paper. The following text contains excerpts from the original article and how they should appear with correct referencing. The publisher apologises for any inconvenience this has caused readers.

Long-term in situ permafrost thaw effects on bacterial communities and potential aerobic respiration.

The decomposition of large stocks of soil organic carbon in thawing permafrost might depend on more than climate change-induced temperature increases: indirect effects of thawing via altered bacterial community structure (BCS) or rooting patterns are largely unexplored. We used a 10-year in situ permafrost thaw experiment and aerobic incubations to investigate alterations in BCS and potential respiration at different depths, and the extent to which they are related with each other and with root density. Active layer and permafrost BCS strongly differed, and the BCS in formerly frozen soils (below the natural thawfront) converged under induced deep thaw to strongly resemble the active layer BCS, possibly as a result of colonization by overlying microorganisms. Overall, respiration rates decreased with depth and soils showed lower potential respiration when subjected to deeper thaw, which we attributed to gradual labile carbon pool depletion. Despite deeper rooting under induced deep thaw, root density measurements did not improve soil chemistry-based models of potential respiration. However, BCS explained an additional unique portion of variation in respiration, particularly when accounting for differences in organic matter content. Our results suggest that by measuring bacterial community composition, we can improve both our understanding and the modeling of the permafrost carbon feedback.

Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2.

As a consequence of global change processes, plants will increasingly be challenged by extreme climatic events, against a background of elevated atmospheric CO2. We analysed responses of Arabidopsis thaliana to periods of a combination of elevated heat and water deficit at ambient and elevated CO2 in order to gain mechanistic insights regarding changes in primary metabolism. Metabolic changes induced by extremes of climate are dynamic and specific to different classes of molecules. Concentrations of soluble sugars and amino acids increased transiently after short (4-d) exposure to heat and drought, and readjusted to control levels under prolonged (8-d) stress. In contrast, fatty acids showed persistent changes during the stress period. Elevated CO2 reduced the impact of stress on sugar and amino acid metabolism, but not on fatty acids. Integrating metabolite data with transcriptome results revealed that some of the metabolic changes were regulated at the transcriptional level. Multivariate analyses grouped metabolites on the basis of stress exposure time, indicating specificity in metabolic responses to short and prolonged stress. Taken together, the results indicate that dynamic metabolic reprograming plays an important role in plant acclimation to climatic extremes. The extent of such metabolic adjustments is less under high CO2, further pointing towards the role of high CO2 in stress mitigation.

Prolonged exposure does not increase soil microbial community compositional response to warming along geothermal gradients.

Global change is expected to affect soil microbial communities through their responsiveness to temperature. It has been proposed that prolonged exposure to elevated temperatures may lead to progressively larger effects on soil microbial community composition. However, due to the relatively short-term nature of most warming experiments, this idea has been challenging to evaluate. The present study took the advantage of natural geothermal gradients (from +1°C to +19°C above ambient) in two subarctic grasslands to test the hypothesis that long-term exposure (>50 years) intensifies the effect of warming on microbial community composition compared to short-term exposure (5-7 years). Community profiles from amplicon sequencing of bacterial and fungal rRNA genes did not support this hypothesis: significant changes relative to ambient were observed only starting from the warming intensity of +9°C in the long term and +7°C/+3°C in the short term, for bacteria and fungi, respectively. Our results suggest that microbial communities in high-latitude grasslands will not undergo lasting shifts in community composition under the warming predicted for the coming 100 years (+2.2°C to +8.3°C).

Compositional Stability of the Bacterial Community in a Climate-Sensitive Sub-Arctic Peatland.

The climate sensitivity of microbe-mediated soil processes such as carbon and nitrogen cycling offers an interesting case for evaluating the corresponding sensitivity of microbial community composition to environmental change. Better understanding of the degree of linkage between functional and compositional stability would contribute to ongoing efforts to build mechanistic models aiming at predicting rates of microbe-mediated processes. We used an amplicon sequencing approach to test if previously observed large effects of experimental soil warming on C and N cycle fluxes (50-100% increases) in a sub-arctic Sphagnum peatland were reflected in changes in the composition of the soil bacterial community. We found that treatments that previously induced changes to fluxes did not associate with changes in the phylogenetic composition of the soil bacterial community. For both DNA- and RNA-based analyses, variation in bacterial communities could be explained by the hierarchy: spatial variation (12-15% of variance explained) > temporal variation (7-11%) > climate treatment (4-9%). We conclude that the bacterial community in this environment is stable under changing conditions, despite the previously observed sensitivity of process rates-evidence that microbe-mediated soil processes can alter without concomitant changes in bacterial communities. We propose that progress in linking soil microbial communities to ecosystem processes can be advanced by further investigating the relative importance of community composition effects versus physico-chemical factors in controlling biogeochemical process rates in different contexts.

The microbiome of Folsomia candida: an assessment of bacterial diversity in a Wolbachia-containing animal.

The springtail Folsomia candida is an important model organism for soil ecology, ecotoxicology and ecogenomics. The decomposer activities of soil invertebrates like Folsomia depend on their relationship with microbial communities including gut symbionts. In this paper, we apply high-throughput sequencing to provide a detailed characterization of the bacterial community associated with parthenogenetic F. candida. First, we evaluated a method to suppress the amplification of DNA from the endosymbiont Wolbachia, to prevent it from interfering with the identification of less abundant operational taxonomic units (OTUs). The suppression treatment applied was effective against Wolbachia and did not interfere with the detection of the most abundant OTUs (59 OTUs, contributing over 87% of the reads). However, this method did affect the inferred community composition. Significant differences were subsequently observed in the composition of bacterial communities associated with two different strains of F. candida. A total of 832 OTUs were found, of which 45% were only present in one strain and 17% only in the other. Among the 20 most abundant OTUs, 16 were shared between strains. Denaturing gradient gel electrophoresis and clone libraries, although unable to capture the full diversity of the bacterial community, provided results that supported the NGS data.

Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils.

Understanding how communities assemble is a central goal of ecology. This is particularly relevant for communities of arbuscular mycorrhizal fungi (AMF), because the community composition of these beneficial plant symbionts influences important ecosystem processes. Moreover, AMF may be used as sensitive indicators of ecological soil quality if they respond to environmental variation in a predictable way. Here, we use a molecular profiling technique (T-RFLP of 25S rRNA gene fragments) to test which factors determine AM fungal community composition in 40 agricultural soils in the Netherlands. In particular, we test whether species richness, dominance structure and community nestedness are influenced by management type (in pairs of organically and conventionally farmed fields), and we examine the contribution of crop species (maize vs. potato), soil type (sand vs. clay-textured soils) and habitat (plant root vs. bulk soil) on AMF community characteristics. AMF richness varied from 1 to 11 taxa per field. Communities from species-poor fields were found to be subsets of those in richer fields, indicating nestedness and a progressive 'loss' from the species pool. AMF taxa richness and occurrence in soil and plant roots were highly correlated, and richness was related to management intensity (phosphate availability and grass-cropping history together explained 32% and 50% of richness in roots and soils). Soil type together with soil chemical parameters explained only 17% of variance in AMF community structure. We synthesize these results by discussing the potential contribution of a 'bottleneck effect' on AMF communities through increased stochastic effects under environmental stress.

Enzymology under global change: organic nitrogen turnover in alpine and sub-Arctic soils.

Understanding global change impacts on the globally important carbon storage in alpine, Arctic and sub-Arctic soils requires knowledge of the mechanisms underlying the balance between plant primary productivity and decomposition. Given that nitrogen availability limits both processes, understanding the response of the soil nitrogen cycle to shifts in temperature and other global change factors is crucial for predicting the fate of cold biome carbon stores. Measurements of soil enzyme activities at different positions of the nitrogen cycling network are an important tool for this purpose. We review a selection of studies that provide data on potential enzyme activities across natural, seasonal and experimental gradients in cold biomes. Responses of enzyme activities to increased nitrogen availability and temperature are diverse and seasonal dynamics are often larger than differences due to experimental treatments, suggesting that enzyme expression is regulated by a combination of interacting factors reflecting both nutrient supply and demand. The extrapolation from potential enzyme activities to prediction of elemental nitrogen fluxes under field conditions remains challenging. Progress in molecular '-omics' approaches may eventually facilitate deeper understanding of the links between soil microbial community structure and biogeochemical fluxes. In the meantime, accounting for effects of the soil spatial structure and in situ variations in pH and temperature, better mapping of the network of enzymatic processes and the identification of rate-limiting steps under different conditions should advance our ability to predict nitrogen fluxes.

Global meta-analysis of wood decomposition rates: a role for trait variation among tree species?

The carbon flux from woody debris, a crucial uncertainty within global carbon-climate models, is simultaneously affected by climate, site environment and species-based variation in wood quality. In the first global analysis attempting to explicitly tease out the wood quality contribution to decomposition, we found support for our hypothesis that, under a common climate, interspecific differences in wood traits affect woody debris decomposition patterns. A meta-analysis of 36 studies from all forested continents revealed that nitrogen, phosphorus, and C : N ratio correlate with decomposition rates of angiosperms. In addition, gymnosperm wood consistently decomposes slower than angiosperm wood within common sites, a pattern that correlates with clear divergence in wood traits between the two groups. New empirical studies are needed to test whether this difference is due to a direct effect of wood trait variation on decomposer activity or an indirect effect of wood traits on decomposition microsite environment. The wood trait-decomposition results point to an important role for changes in the wood traits of dominant tree species as a driver of carbon cycling, with likely feedback to atmospheric CO(2) particularly where angiosperm species replace gymnosperms regionally. Truly worldwide upscaling of our results will require further site-based multi-species wood trait and decomposition data, particularly from low-latitude ecosystems.