Sarah E. Evans

Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter?

Climate models project that precipitation patterns will likely intensify in the future, resulting in increased duration of droughts and increased frequency of large soil rewetting events, which are stressful to the microorganisms that drive soil biogeochemical cycling. Historical conditions can affect contemporary microbial responses to environmental factors through the persistence of abiotic changes or through the selection of a more tolerant microbial community. We examined how a history of intensified rainfall would alter microbial functional response to drying and rewetting events, whether this historical legacy was mediated through altered microbial community composition, and how long community and functional legacies persisted under similar conditions. We collected soils from a long-term field manipulation (Rainfall Manipulation Plot Study) in Kansas, USA, where rainfall variability was experimentally amplified. We measured respiration, microbial biomass, fungal:bacterial ratios and bacterial community composition after collecting soils from the field experiment, and after subjecting them to a series of drying–rewetting pulses in the lab. Although rainfall history affected respiration and microbial biomass, the differences between field treatments did not persist throughout our 115-day drying–rewetting incubation. However, soils accustomed to more extreme rainfall did change less in response to lab moisture pulses. In contrast, bacterial community composition did not differ between rainfall manipulation treatments, but became more dissimilar in response to drying–rewetting pulses depending on their previous field conditions. Our results suggest that environmental history can affect contemporary rates of biogeochemical processes both through changes in abiotic drivers and through changes in microbial community structure. However, the extremity of the disturbance and the mechanism through which historical legacies occur may influence how long they persist, which determines the importance of these effects for biogeochemical cycling.

Climate change alters ecological strategies of soil bacteria

The timing and magnitude of rainfall events are expected to change in future decades, resulting in longer drought periods and larger rainfall events. Although microbial community composition and function are both sensitive to changes in rainfall, it is unclear whether this is because taxa adopt strategies that maximise fitness under new regimes. We assessed whether bacteria exhibited phylogenetically conserved ecological strategies in response to drying-rewetting, and whether these strategies were altered by historical exposure to experimentally intensified rainfall patterns. By clustering relative abundance patterns, we identified three discrete ecological strategies and found that tolerance to drying-rewetting increased with exposure to intensified rainfall patterns. Changes in strategy were primarily due to changes in community composition, but also to strategy shifts within taxa. These moisture regime-selected ecological strategies may be predictable from disturbance history, and are likely to be linked to traits that influence the functional potential of microbial communities.

Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed

For any enzyme-catalyzed reaction to occur, the corresponding protein-encoding genes and transcripts are necessary prerequisites. Thus, a positive relationship between the abundance of gene or transcripts and corresponding process rates is often assumed. To test this assumption, we conducted a meta-analysis of the relationships between gene and/or transcript abundances and corresponding process rates. We identified 415 studies that quantified the abundance of genes or transcripts for enzymes involved in carbon or nitrogen cycling. However, in only 59 of these manuscripts did the authors report both gene or transcript abundance and rates of the appropriate process. We found that within studies there was a significant but weak positive relationship between gene abundance and the corresponding process. Correlations were not strengthened by accounting for habitat type, differences among genes or reaction products versus reactants, suggesting that other ecological and methodological factors may affect the strength of this relationship. Our findings highlight the need for fundamental research on the factors that control transcription, translation and enzyme function in natural systems to better link genomic and transcriptomic data to ecosystem processes.

Is bacterial moisture niche a good predictor of shifts in community composition under long-term drought?

Both biogeographical and rainfall manipulation studies show that soil water content can be a strong driver of microbial community composition. However, we do not yet know if these patterns emerge because certain bacterial taxa are better able to survive at dry soil moisture regimes or if they are due to other drought-sensitive ecosystem properties indirectly affecting microbial community composition. In this study, we evaluated (1) whether bacterial community composition changed under an 11-year drought manipulation and (2) whether shifts under drought could be explained by variation in the moisture sensitivity of growth among bacterial taxa (moisture niche partitioning). Using 454 pyrosequencing of 16S rRNA, we observed shifts in bacterial community composition under drought, coincident with changes in other soil properties. We wet-up dry soils from drought plots to five moisture levels, and measured respiration and the composition of actively growing communities using bromodeoxyuridine (BrdU) labeling of DNA. The field drought experiment affected the composition of the active community when incubated at different moisture levels in the laboratory, as well as short-term (36-hour) respiration rates. Independent of history, bacterial communities also displayed strong niche partitioning across the wet-up moisture gradient. Although this indicates that moisture has the potential to drive bacterial community composition under long-term drought, species distributions predicted by response to moisture did not reflect the community composition of plots that were subjected to long-term drought. Bacterial community structure was likely more strongly driven by other environmental factors that changed under long-term drought, or not shaped by response to water level upon wet-up. The approach that we present here for linking niches to community composition could be adapted for other environmental variables to aid in predicting microbial species distributions and community responses to environmental change.

Effects of dispersal and selection on stochastic assembly in microbial communities

Stochastic processes can play an important role in microbial community assembly. Dispersal limitation is one process that can increase stochasticity and obscure relationships between environmental variables and microbial community composition, but the relationship between dispersal, selection and stochasticity has not been described in a comprehensive way. We examine how dispersal and its interactions with drift and selection alter the consistency with which microbial communities assemble using a realistic, individual-based model of microbial decomposers. Communities were assembled under different environmental conditions and dispersal rates in repeated simulations, and we examined the compositional difference among replicate communities colonizing the same type of leaf litter (‘within-group distance’), as well as between-group deterministic selection. Dispersal rates below 25% turnover per year resulted in high within-group distance among communities and no significant environmental effects. As dispersal limitation was alleviated, both within- and between-group distance decreased, but despite this homogenization, deterministic environmental effects remained significant. In addition to direct effects of dispersal rate, stochasticity of community composition was influenced by an interaction between dispersal and selection strength. Specifically, communities experiencing stronger selection (less favorable litter chemistries) were more stochastic, possibly because lower biomass and richness intensified drift or priority effects. Overall, we show that dispersal rate can significantly alter patterns of community composition. Partitioning the effects of dispersal, selection and drift based on static patterns of microbial composition will be difficult, if not impossible. Experiments will be required to tease apart these complex interactions between assembly processes shaping microbial communities.

Asymmetric responses of primary productivity to precipitation extremes: A synthesis of grassland precipitation manipulation experiments

Climatic changes are altering Earths hydrological cycle, resulting in altered precipitation amounts, increased interannual variability of precipitation, and more frequent extreme precipitation events. These trends will likely continue into the future, having substantial impacts on net primary productivity (NPP) and associated ecosystem services such as food production and carbon sequestration. Frequently, experimental manipulations of precipitation have linked altered precipitation regimes to changes in NPP. Yet, findings have been diverse and substantial uncertainty still surrounds generalities describing patterns of ecosystem sensitivity to altered precipitation. Additionally, we do not know whether previously observed correlations between NPP and precipitation remain accurate when precipitation changes become extreme. We synthesized results from 83 case studies of experimental precipitation manipulations in grasslands worldwide. We used meta-analytical techniques to search for generalities and asymmetries of aboveground NPP (ANPP) and belowground NPP (BNPP) responses to both the direction and magnitude of precipitation change. Sensitivity (i.e., productivity response standardized by the amount of precipitation change) of BNPP was similar under precipitation additions and reductions, but ANPP was more sensitive to precipitation additions than reductions; this was especially evident in drier ecosystems. Additionally, overall relationships between the magnitude of productivity responses and the magnitude of precipitation change were saturating in form. The saturating form of this relationship was likely driven by ANPP responses to very extreme precipitation increases, although there were limited studies imposing extreme precipitation change, and there was considerable variation among experiments. This highlights the importance of incorporating gradients of manipulations, ranging from extreme drought to extreme precipitation increases into future climate change experiments. Additionally, policy and land management decisions related to global change scenarios should consider how ANPP and BNPP responses may differ, and that ecosystem responses to extreme events might not be predicted from relationships found under moderate environmental changes.

Non-Rainfall Moisture Activates Fungal Decomposition of Surface Litter in the Namib Sand Sea

The hyper-arid western Namib Sand Sea (mean annual rainfall 0–17 mm) is a detritus-based ecosystem in which primary production is driven by large, but infrequent rainfall events. A diverse Namib detritivore community is sustained by minimal moisture inputs from rain and fog. The decomposition of plant material in the Namib Sand Sea (NSS) has long been assumed to be the province of these detritivores, with beetles and termites alone accounting for the majority of litter losses. We have found that a mesophilic Ascomycete community, which responds within minutes to moisture availability, is present on litter of the perennial Namib dune grass Stipagrostis sabulicola. Important fungal traits that allow survival and decomposition in this hyper-arid environment with intense desiccation, temperature and UV radiation stress are darkly-pigmented hyphae, a thermal range that includes the relatively low temperature experienced during fog and dew, and an ability to survive daily thermal and desiccation stress at temperatures as high as 50°C for five hours. While rainfall is very limited in this area, fog and high humidity provide regular periods (≥ 1 hour) of sufficient moisture that can wet substrates and hence allow fungal growth on average every 3 days. Furthermore, these fungi reduce the C/N ratio of the litter by a factor of two and thus detritivores, like the termite Psammotermes allocerus, favor fungal-infected litter parts. Our studies show that despite the hyper-aridity of the NSS, fungi are a key component of energy flow and biogeochemical cycling that should be accounted for in models addressing how the NSS ecosystem will respond to projected climate changes which may alter precipitation, dew and fog regimes.

Understanding How Microbiomes Influence the Systems they Inhabit: Insight from Ecosystem Ecology

Translating the ever-increasing wealth of information on microbiomes (environment, host, or built environment) to advance the understanding of system-level processes is proving to be an exceptional research challenge. One reason for this challenge is that relationships between characteristics of microbiomes and the system-level processes they influence are often evaluated in the absence of a robust conceptual framework and reported without elucidating the underlying causal mechanisms. The reliance on correlative approaches limits the potential to expand the inference of a single relationship to additional systems and advance the field. We propose that research focused on how microbiomes influence the systems they inhabit should work within a common framework and target known microbial processes that contribute to the system-level processes of interest. Here we identify three distinct categories of microbiome characteristics (microbial processes, microbial community properties, and microbial membership) and propose a framework to empirically link each of these categories to each other and the broader system level processes they affect. We posit that it is particularly important to distinguish microbial community properties that can be predicted from constituent taxa (community aggregated traits) from and those properties that are currently unable to be predicted from constituent taxa (emergent properties). Existing methods in microbial ecology can be applied to more explicitly elucidate properties within each of these categories and connect these three categories of microbial characteristics with each other. We view this proposed framework, gleaned from a breadth of research on environmental microbiomes and ecosystem processes, as a promising pathway with the potential to advance discovery and understanding across a broad range of microbiome science.The well-documented significance of microorganisms to the function of virtually all ecosystems has led to the assumption that more information on microbiomes will improve our ability to understand and predict system-level processes. Notably, the importance of the microbiome has become increasingly evident in the environmental sciences and in particular ecosystem ecology. However, translating the ever-increasing wealth of information on environmental microbiomes to advance ecosystem science is proving exceptionally challenging. One reason for this challenge is that correlations between microbiomes and the ecosystem processes they influence are often reported without the underlying causal mechanisms. This limits the predictive power of each correlation to the time and place at which it was identified. In this paper, we assess the assumptions and approaches currently used to establish links between environmental microbiomes and the ecosystems they influence, propose a framework to more effectively harness our understanding of microbiomes to advance ecosystem science, and identify key challenges and solutions required to apply the proposed framework. Specifically, we suggest identifying each microbial process that contributes to the ecosystem process of interest a priori. We then suggest linking information on microbial community membership through microbial community properties (such as biomass elemental ratios) to the microbial processes that drive each ecosystem process (e.g. N -mineralization). A key challenge in this framework will be identifying which microbial community properties can be determined from the constituents of the community (community aggregated traits, CATs) and which properties are unable to be predicted from a list of their constituent taxa (emergent properties, EPs). We view this directed approach as a promising pathway to advance our understanding of how microbiomes influence the systems they inhabit.

Effects of soil nitrogen availability on rhizodeposition in plants: a review

BackgroundSoil contains the majority of terrestrial carbon (C), forming the foundation for soil fertility and nutrient cycling. One key source of soil C is root-derived C, or rhizodeposits, which signal and sustain microbes that cycle nutrients such as nitrogen (N). Although N availability can affect rhizodeposition both quantitatively and qualitatively, these effects remain poorly understood due to conflicting results among studies.ScopeHere, we review studies examining the influence of soil N availability on rhizodeposition. We conduct a quantitative analysis of the response of various rhizodeposition C pools to N availability, and assess methodological aspects potentially underlying the highly variable results among studies. We also review impacts of N availability on the composition and quality of rhizodeposits.ConclusionsEffects of N on rhizodeposition were strongly dependent upon the specific C pools considered and the units for reporting those pools. N additions increased nearly all rhizodeposit C pools when expressed on a per plant basis, and decreased rhizodeposition per unit fixed C for several C pools, while no rhizodeposition C pools were significantly altered when expressed per unit root mass. Nevertheless, N effects were generally mixed due to a combination of variation in experimental methods and species-specific responses. Overall, our review indicates several key challenges for better understanding the mechanistic links between N availability, plant physiology, and microbial function. Identifying such links would substantially improve our ability to predict C- and N-dynamics in changing ecosystems.

Understanding how microbiomes influence the systems they inhabit

Translating the ever-increasing wealth of information on microbiomes (environment, host or built environment) to advance our understanding of system-level processes is proving to be an exceptional research challenge. One reason for this challenge is that relationships between characteristics of microbiomes and the system-level processes that they influence are often evaluated in the absence of a robust conceptual framework and reported without elucidating the underlying causal mechanisms. The reliance on correlative approaches limits the potential to expand the inference of a single relationship to additional systems and advance the field. We propose that research focused on how microbiomes influence the systems they inhabit should work within a common framework and target known microbial processes that contribute to the system-level processes of interest. Here, we identify three distinct categories of microbiome characteristics (microbial processes, microbial community properties and microbial membership) and propose a framework to empirically link each of these categories to each other and the broader system-level processes that they affect. We posit that it is particularly important to distinguish microbial community properties that can be predicted using constituent taxa (community-aggregated traits) from those properties that cannot currently be predicted using constituent taxa (emergent properties). Existing methods in microbial ecology can be applied to more explicitly elucidate properties within each of these three categories of microbial characteristics and connect them with each other. We view this proposed framework, gleaned from a breadth of research on environmental microbiomes and ecosystem processes, as a promising pathway with the potential to advance discovery and understanding across a broad range of microbiome science.This Review Article discusses the importance of considering known microbial processes to inform our understanding of the role of microbial communities in ecosystem processes, and a move away from approaches based solely on correlation analyses.