Large Blooms of Bacillales (Firmicutes) Underlie the Response to Wetting of Cyanobacterial Biocrusts at Various Stages of Maturity.

Biological soil crusts (biocrusts) account for a substantial portion of primary production in dryland ecosystems. They successionally mature to deliver a suite of ecosystem services, such as carbon sequestration, water retention and nutrient cycling, and climate regulation. Biocrust assemblages are extremely well adapted to survive desiccation and to rapidly take advantage of the periodic precipitation events typical of arid ecosystems. Here we focus on the wetting response of incipient cyanobacterial crusts as they mature from "light" to "dark." We sampled a cyanobacterial biocrust chronosequence before (dry) and temporally following a controlled wetting event and used high-throughput 16S rRNA and rRNA gene sequencing to monitor the dynamics of microbial response. Overall, shorter-term changes in phylogenetic beta diversity attributable to periodic wetting were as large as those attributable to biocrust successional stage. Notably, more mature crusts showed significantly higher resistance to precipitation disturbance. A large bloom of a few taxa within the Firmicutes, primarily in the order Bacillales, emerged 18 h after wetting, while filamentous crust-forming cyanobacteria showed variable responses to wet-up across the successional gradient, with populations collapsing in less-developed light crusts but increasing in later-successional-stage dark crusts. Overall, the consistent Bacillales bloom accompanied by the variable collapse of pioneer cyanobacteria of the Oscillatoriales order across the successional gradient suggests that the strong response of few organisms to a hydration pulse with the mortality of the autotroph might have important implications for carbon (C) balance in semiarid ecosystems.IMPORTANCE Desert biological soil crusts are terrestrial topsoil microbial communities common to arid regions that comprise 40% of Earth's terrestrial surface. They successionally develop over years to decades to deliver a suite of ecosystem services of local and global significance. Ecosystem succession toward maturity has been associated with both resistance and resilience to disturbance. Recent work has shown that the impacts of both climate change and physical disturbance on biocrusts increase the potential for successional resetting. A larger proportion of biocrusts are expected to be at an early developmental stage, hence increasing susceptibility to changes in precipitation frequencies. Therefore, it is essential to characterize how biocrusts respond to wetting across early developmental stages. In this study, we document the wetting response of microbial communities from a biocrust chronosequence. Overall, our results suggest that the cumulative effects of altered precipitation frequencies on the stability of biocrusts will depend on biocrust maturity.

Reoxidation of Chromium(III) Products Formed under Different Biogeochemical Regimes.

Hexavalent chromium, Cr(VI), is a widespread and toxic groundwater contaminant. Reductive immobilization to Cr(III) is a treatment option, but its success depends on the long-term potential for reduced chromium precipitates to remain immobilized under oxidizing conditions. In this unique long-term study, aquifer sediments subjected to reductive Cr(VI) immobilization under different biogeochemical regimes were tested for their susceptibility to reoxidation. After reductive treatment for 1 year, sediments were exposed to oxygenated conditions for another 2 years in flow-through, laboratory columns. Under oxidizing conditions, immobilized chromium reduced under predominantly denitrifying conditions was mobilized at low concentrations (≪1 µM Cr(VI); ∼ 3% of Cr(III) deposited) that declined over time. A conceptual model of a limited pool of more soluble Cr(III), and a larger pool of relatively insoluble Cr(III), is proposed. In contrast, almost no chromium was mobilized from columns reduced under predominantly fermentative conditions, and where reducing conditions persisted for several months after introduction of oxidizing conditions, presumably due to the presence of a reservoir of reduced species generated during reductive treatment. The results from this 3-year study demonstrate that biogeochemical conditions present during reductive treatment, and the potential for buildup of reducing species, will impact the long-term sustainability of the remediation effort.

Belowground Response to Drought in a Tropical Forest Soil. II. Change in Microbial Function Impacts Carbon Composition.

Climate model projections for tropical regions show clear perturbation of precipitation patterns leading to increased frequency and severity of drought in some regions. Previous work has shown declining soil moisture to be a strong driver of changes in microbial trait distribution, however, the feedback of any shift in functional potential on ecosystem properties related to carbon cycling are poorly understood. Here we show that drought-induced changes in microbial functional diversity and activity shape, and are in turn shaped by, the composition of dissolved and soil-associated carbon. We also demonstrate that a shift in microbial functional traits that favor the production of hygroscopic compounds alter the efflux of carbon dioxide following soil rewetting. Under drought the composition of the dissolved organic carbon pool changed in a manner consistent with a microbial metabolic response. We hypothesize that this microbial ecophysiological response to changing soil moisture elevates the intracellular carbon demand stimulating extracellular enzyme production, that prompts the observed decline in more complex carbon compounds (e.g., cellulose and lignin). Furthermore, a metabolic response to drought appeared to condition (biologically and physically) the soil, notably through the production of polysaccharides, particularly in experimental plots that had been pre-exposed to a short-term drought. This hysteretic response, in addition to an observed drought-related decline in phosphorus concentration, may have been responsible for a comparatively modest CO2 efflux following wet-up in drought plots relative to control plots.

Bacteria increase arid-land soil surface temperature through the production of sunscreens.

Soil surface temperature, an important driver of terrestrial biogeochemical processes, depends strongly on soil albedo, which can be significantly modified by factors such as plant cover. In sparsely vegetated lands, the soil surface can be colonized by photosynthetic microbes that build biocrust communities. Here we use concurrent physical, biochemical and microbiological analyses to show that mature biocrusts can increase surface soil temperature by as much as 10 °C through the accumulation of large quantities of a secondary metabolite, the microbial sunscreen scytonemin, produced by a group of late-successional cyanobacteria. Scytonemin accumulation decreases soil albedo significantly. Such localized warming has apparent and immediate consequences for the soil microbiome, inducing the replacement of thermosensitive bacterial species with more thermotolerant forms. These results reveal that not only vegetation but also microorganisms are a factor in modifying terrestrial albedo, potentially impacting biosphere feedbacks on past and future climate, and call for a direct assessment of such effects at larger scales.

Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee.

The coffee berry borer (Hypothenemus hampei) is the most devastating insect pest of coffee worldwide with its infestations decreasing crop yield by up to 80%. Caffeine is an alkaloid that can be toxic to insects and is hypothesized to act as a defence mechanism to inhibit herbivory. Here we show that caffeine is degraded in the gut of H. hampei, and that experimental inactivation of the gut microbiota eliminates this activity. We demonstrate that gut microbiota in H. hampei specimens from seven major coffee-producing countries and laboratory-reared colonies share a core of microorganisms. Globally ubiquitous members of the gut microbiota, including prominent Pseudomonas species, subsist on caffeine as a sole source of carbon and nitrogen. Pseudomonas caffeine demethylase genes are expressed in vivo in the gut of H. hampei, and re-inoculation of antibiotic-treated insects with an isolated Pseudomonas strain reinstates caffeine-degradation ability confirming their key role.

Divergent aquifer biogeochemical systems converge on similar and unexpected Cr(VI) reduction products.

In this study of reductive chromium immobilization, we found that flow-through columns constructed with homogenized aquifer sediment and continuously infused with lactate, chromate, and various native electron acceptors diverged to have very different Cr(VI)-reducing biogeochemical regimes characterized by either denitrifying or fermentative conditions (as indicated by effluent chemical data, 16S rRNA pyrotag data, and metatranscriptome data). Despite the two dramatically different biogeochemical environments that evolved in the columns, these regimes created similar Cr(III)-Fe(III) hydroxide precipitates as the predominant Cr(VI) reduction product, as characterized by micro-X-ray fluorescence and micro-X-ray absorption near-edge structure analysis. We discuss two conflicting scenarios of microbially mediated formation of Cr(III)-Fe(III) precipitates, each of which is both supported and contradicted by different lines of evidence: (1) enzymatic reduction of Cr(VI) to Cr(III) followed by coprecipitation of Cr(III) and Fe(III) and (2) both regimes generated at least small amounts of Fe(II), which abiotically reduced Cr(VI) to form a Cr-Fe precipitate. Evidence of zones with different levels of Cr(VI) reduction suggest that local heterogeneity may have confounded interpretation of processes based on bulk measurements. This study indicates that the bulk redox status and biogeochemical regime, as categorized by the dominant electron-accepting process, do not necessarily control the final product of Cr(VI) reduction.

Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought.

Global climate models project a decrease in the magnitude of precipitation in tropical regions. Changes in rainfall patterns have important implications for the moisture content and redox status of tropical soils, yet little is known about how these changes may affect microbial community structure. Specifically, does exposure to prior stress confer increased resistance to subsequent perturbation? Here we reduced the quantity of precipitation throughfall to tropical forest soils in the Luquillo Mountains, Puerto Rico. Treatments included newly established throughfall exclusion plots (de novo excluded), plots undergoing reduction for a second time (pre-excluded) and ambient control plots. Ten months of throughfall exclusion led to a small but statistically significant decline in soil water potential and bacterial populations clearly adapted to increased osmotic stress. Although the water potential decline was small and microbial biomass did not change, phylogenetic diversity in the de novo-excluded plots decreased by ∼40% compared with the control plots, yet pre-excluded plots showed no significant change. On the other hand, the relative abundances of bacterial taxa in both the de novo-excluded and pre-excluded plots changed significantly with throughfall exclusion compared with control plots. Changes in bacterial community structure could be explained by changes in soil pore water chemistry and suggested changes in soil redox. Soluble iron declined in treatment plots and was correlated with decreased soluble phosphorus concentrations, which may have significant implications for microbial productivity in these P-limited systems.