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Empirical evidence for the response of soil carbon cycling to the combined effects of warming, drought and diversity loss is scarce. Microbial carbon use efficiency (CUE) plays a central role in regulating the flow of carbon through soil, yet how biotic and abiotic factors interact to drive it remains unclear. Here, we combine distinct community inocula (a biotic factor) with different temperature and moisture conditions (abiotic factors) to manipulate microbial diversity and community structure within a model soil. While community composition and diversity are the strongest predictors of CUE, abiotic factors modulated the relationship between diversity and CUE, with CUE being positively correlated with bacterial diversity only under high moisture. Altogether these results indicate that the diversity × ecosystem-function relationship can be impaired under non-favorable conditions in soils, and that to understand changes in soil C cycling we need to account for the multiple facets of global changes. Microbial carbon use efficiency has an important role in soil C cycling. Here the authors test the interactive effects of temperature and moisture and manipulate microbial community composition in soil microcosms, showing a positive relationship between microbial diversity and CUE that is contingent on abiotic conditions.

A recent paper by Martiny argues that “high proportions” of bacteria in diverse Earth environments have been cultured. Here we reanalyze a portion of the data in that paper, and argue that the conclusion is based on several technical errors, most notably a calculation of sequence similarity that does not account for sequence gaps, and the reliance on 16S rRNA gene amplicons that are known to be biased towards cultured organisms. We further argue that the paper is also based on a conceptual error: namely, that sequence similarity cannot be used to infer “culturability” because one cannot infer physiology from 16S rRNA gene sequences. Combined with other recent, more reliable studies, the evidence supports the conclusion that most bacterial and archaeal taxa remain uncultured.

Permafrost microbes await the thaw Permafrost soil in the Arctic contains a huge reservoir of carbon. If the climate warms and the permafrost thaws, this carbon would become accessible to microbial degradation, releasing greenhouse gases in the process. The microbes responsible for this process are largely unknown. Metagenomic analysis of DNA isolated from two permafrost soils collected in Alaska reveals a rapid microbial response to thawing, with many functional gene abundances increasing. A draft genome of a novel methanogen was constructed from the sequence data. This study highlights the importance of rapid cycling of methane and nitrogen in thawing permafrost. Permafrost contains an estimated 1672 Pg carbon (C), an amount roughly equivalent to the total currently contained within land plants and the atmosphere 1 , 2 , 3 . This reservoir of C is vulnerable to decomposition as rising global temperatures cause the permafrost to thaw 2 . During thaw, trapped organic matter may become more accessible for microbial degradation and result in greenhouse gas emissions 4 , 5 . Despite recent advances in the use of molecular tools to study permafrost microbial communities 6 , 7 , 8 , 9 , their response to thaw remains unclear. Here we use deep metagenomic sequencing to determine the impact of thaw on microbial phylogenetic and functional genes, and relate these data to measurements of methane emissions. Metagenomics, the direct sequencing of DNA from the environment, allows the examination of whole biochemical pathways and associated processes, as opposed to individual pieces of the metabolic puzzle. Our metagenome analyses reveal that during transition from a frozen to a thawed state there are rapid shifts in many microbial, phylogenetic and functional gene abundances and pathways. After one week of incubation at 5 °C, permafrost metagenomes converge to be more similar to each other than while they are frozen. We find that multiple genes involved in cycling of C and nitrogen shift rapidly during thaw. We also construct the first draft genome from a complex soil metagenome, which corresponds to a novel methanogen. Methane previously accumulated in permafrost is released during thaw and subsequently consumed by methanotrophic bacteria. Together these data point towards the importance of rapid cycling of methane and nitrogen in thawing permafrost.

Soil microbes respond to environmental change by altering how they allocate carbon to growth versus respiration—or carbon use efficiency (CUE). Ecosystem and Earth System models, used to project how global soil C stocks will continue to respond to the climate crisis, often assume that microbes respond homogeneously to changes in the environment. In this study, we quantified how CUE varies with changes in temperature and substrate quality in soil bacteria and evaluated why CUE characteristics may differ between bacterial isolates and in response to altered growth conditions. We found that bacterial taxa capable of rapid growth were more efficient than those limited to slow growth and that taxa with high CUE were more likely to become less efficient at higher temperatures than those that were less efficient to begin with. Together, our results support the idea that the CUE temperature response is constrained by both growth rate and CUE and that this partly explains how bacteria acclimate to a warming world. The strategy that microbial decomposers take with respect to using substrate for growth versus maintenance is one essential biological determinant of the propensity of carbon to remain in soil. To quantify the environmental sensitivity of this key physiological trade-off, we characterized the carbon use efficiency (CUE) of 23 soil bacterial isolates across seven phyla at three temperatures and with up to four substrates. Temperature altered CUE in both an isolate-specific manner and a substrate-specific manner. We searched for genes correlated with the temperature sensitivity of CUE on glucose and deemed those functional genes which were similarly correlated with CUE on other substrates to be validated as markers of CUE. Ultimately, we did not identify any such robust functional gene markers of CUE or its temperature sensitivity. However, we found a positive correlation between rRNA operon copy number and CUE, opposite what was expected. We also found that inefficient taxa increased their CUE with temperature, while those with high CUE showed a decrease in CUE with temperature. Together, our results indicate that CUE is a flexible parameter within bacterial taxa and that the temperature sensitivity of CUE is better explained by observed physiology than by genomic composition across diverse taxa. We conclude that the bacterial CUE response to temperature and substrate is more variable than previously thought. IMPORTANCE Soil microbes respond to environmental change by altering how they allocate carbon to growth versus respiration—or carbon use efficiency (CUE). Ecosystem and Earth System models, used to project how global soil C stocks will continue to respond to the climate crisis, often assume that microbes respond homogeneously to changes in the environment. In this study, we quantified how CUE varies with changes in temperature and substrate quality in soil bacteria and evaluated why CUE characteristics may differ between bacterial isolates and in response to altered growth conditions. We found that bacterial taxa capable of rapid growth were more efficient than those limited to slow growth and that taxa with high CUE were more likely to become less efficient at higher temperatures than those that were less efficient to begin with. Together, our results support the idea that the CUE temperature response is constrained by both growth rate and CUE and that this partly explains how bacteria acclimate to a warming world.

Humid tropical forests are generally characterized by the lack of nitrogen (N) limitation to net primary productivity, yet paradoxically have high potential for N loss. We conducted an intensive field experiment with ⁱ⁵NH₄ and ⁱ⁵NO₃ additions to highly weathered tropical forest soils in Puerto Rico to determine the relative importance of N retention and loss mechanisms. Over one-half of all the NH₄⁺ produced was rapidly converted to NO₃⁻ via the process of gross nitrification. During the first 24 hours, plant roots took up 28% of the inorganic N produced, dominantly as NH₄⁺, and were a greater sink for N than soil microbial biomass. Soil microbes were not a significant sink for added ⁱ⁵NH₄⁺ or ⁱ⁵NO₃⁻ during the first 24 hours, and only for ⁱ⁵NH₄⁺ after 7 days. Patterns of microbial community composition, as determined by terminal restriction fragment length polymorphism analysis (TRFLP), were weakly but significantly correlated with nitrification and denitrification to N₂O. Rates of dissimilatory NO₃⁻ reduction to NH₄⁺ (DNRA) were high in this forest, accounting for up to 25% of gross NH₄⁺ production and 35% of gross nitrification. DNRA was a major sink for NO₃⁻, which may have contributed to the lower rates of N₂O and leaching losses. Despite considerable N conservation via DNRA and plant NH₄⁺ uptake, the fate of ~45% of the NO₃⁻ produced and 4% of the NH₄⁺ produced were not measured in our fluxes, suggesting that other important pathways for N retention and loss (e.g., denitrification to N₂) are important in this system. The high proportion of mineralized N that was rapidly nitrified and the fates of that NO₃⁻ highlight the key role of gross nitrification as a proximate control on N retention and loss in humid tropical forest soils. Furthermore, our results demonstrate the importance of the coupling between DNRA and plant uptake of NH₄⁺ as a potential N-conserving mechanism within tropical forests.

Lignin is often the most difficult portion of plant biomass to degrade, with fungi generally thought to dominate during late stage decomposition. Lignin in feedstock plant material represents a barrier to more efficient plant biomass conversion and can also hinder enzymatic access to cellulose, which is critical for biofuels production. Tropical rain forest soils in Puerto Rico are characterized by frequent anoxic conditions and fluctuating redox, suggesting the presence of lignin-degrading organisms and mechanisms that are different from known fungal decomposers and oxygen-dependent enzyme activities. We explored microbial lignin-degraders by burying bio-traps containing lignin-amended and unamended biosep beads in the soil for 1, 4, 13 and 30 weeks. At each time point, phenol oxidase and peroxidase enzyme activity was found to be elevated in the lignin-amended versus the unamended beads, while cellulolytic enzyme activities were significantly depressed in lignin-amended beads. Quantitative PCR of bacterial communities showed more bacterial colonization in the lignin-amended compared to the unamended beads after one and four weeks, suggesting that the lignin supported increased bacterial abundance. The microbial community was analyzed by small subunit 16S ribosomal RNA genes using microarray (PhyloChip) and by high-throughput amplicon pyrosequencing based on universal primers targeting bacterial, archaeal, and eukaryotic communities. Community trends were significantly affected by time and the presence of lignin on the beads. Lignin-amended beads have higher relative abundances of representatives from the phyla Actinobacteria, Firmicutes, Acidobacteria and Proteobacteria compared to unamended beads. This study suggests that in low and fluctuating redox soils, bacteria could play a role in anaerobic lignin decomposition.

Across biomes, soil biodiversity promotes ecosystem functions. However, whether this relationship will be maintained within ecosystems under climate change is uncertain. Here, using two long-term soil warming experiments, we investigated how warming affects the relationship between ecosystem functions and bacterial diversity across seasons, soil horizons, and warming duration. Soils were sampled from these warming experiments located at the Harvard Forest Long-Term Ecological Research (LTER) site, where soils had been heated +5°C above ambient for 13 or 28 years at the time of sampling. We assessed seven measurements representative of different ecosystem functions and nutrient pools. We also surveyed bacterial community diversity. We found that ecosystem function was significantly affected by season, with autumn samples having a higher intercept than summer samples in our model, suggesting a higher overall baseline of ecosystem function in the fall. The effect of warming on bacterial diversity was similarly affected by season, where warming in the summer was associated with decreased bacterial evenness in the organic horizon. Despite the decreased bacterial evenness in the warmed plots, we found that the relationship between ecosystem function and bacterial diversity was unaffected by warming or warming duration. Our findings highlight that season is a consistent driver of ecosystem function as well as a modulator of climate change effects on bacterial community evenness.

The production of lignocellulosic-derived biofuels is a highly promising source of alternative energy, but it has been constrained by the lack of a microbial platform capable to efficiently degrade this recalcitrant material and cope with by-products that can be toxic to cells. Species that naturally grow in environments where carbon is mainly available as lignin are promising for finding new ways of removing the lignin that protects cellulose for improved conversion of lignin to fuel precursors. Enterobacter lignolyticus SCF1 is a facultative anaerobic Gammaproteobacteria isolated from tropical rain forest soil collected in El Yunque forest, Puerto Rico under anoxic growth conditions with lignin as sole carbon source. Whole transcriptome analysis of SCF1 during E.lignolyticus SCF1 lignin degradation was conducted on cells grown in the presence (0.1%, w/w) and the absence of lignin, where samples were taken at three different times during growth, beginning of exponential phase, mid-exponential phase and beginning of stationary phase. Lignin-amended cultures achieved twice the cell biomass as unamended cultures over three days, and in this time degraded 60% of lignin. Transcripts in early exponential phase reflected this accelerated growth. A complement of laccases, aryl-alcohol dehydrogenases, and peroxidases were most up-regulated in lignin amended conditions in mid-exponential and early stationary phases compared to unamended growth. The association of hydrogen production by way of the formate hydrogenlyase complex with lignin degradation suggests a possible value added to lignin degradation in the future.

Lignin is the second most abundant carbon polymer on earth and despite having more fuel value than cellulose, it currently is considered a waste byproduct in many industrial lignocellulose applications. Valorization of lignin relies on effective and green methods of de-lignification, with a growing interest in the use of microbes. Here we investigate the physiology and molecular response of the novel facultative anaerobic bacterium, Tolumonas lignolytica BRL6-1, to lignin under anoxic conditions. Physiological and biochemical changes were compared between cells grown anaerobically in either lignin-amended or unamended conditions. In the presence of lignin, BRL6-1 accumulates higher biomass and has a shorter lag phase compared to unamended conditions, and 14% of the proteins determined to be significantly higher in abundance by log.sub.2 fold-change of 2 or greater were related to Fe(II) transport in late logarithmic phase. Ferrozine assays of the supernatant confirmed that Fe(III) was bound to lignin and reduced to Fe(II) only in the presence of BRL6-1, suggesting redox activity by the cells. LC-MS/MS analysis of the secretome showed an extra band at 20 kDa in lignin-amended conditions. Protein sequencing of this band identified a protein of unknown function with homology to enzymes in the radical SAM superfamily. Expression of this protein in lignin-amended conditions suggests its role in radical formation. From our findings, we suggest that BRL6-1 is using a protein in the radical SAM superfamily to interact with the Fe(III) bound to lignin and reducing it to Fe(II) for cellular use, increasing BRL6-1 yield under lignin-amended conditions. This interaction potentially generates organic free radicals and causes a radical cascade which could modify and depolymerize lignin. Further research should clarify the extent to which this mechanism is similar to previously described aerobic chelator-mediated Fenton chemistry or radical producing lignolytic enzymes, such as lignin peroxidases, but under anoxic conditions.

The direction and magnitude of climate warming effects on ecosystem processes such as carbon cycling remain uncertain. Soil fungi are central to these processes due to their roles as decomposers of soil organic matter, as mycorrhizal symbionts, and as determinants of plant diversity. Yet despite their importance to ecosystem functioning, we lack a clear understanding of the long‐term response of soil fungal communities to warming. Toward this goal, we characterized soil fungal communities in two replicated soil warming experiments at the Harvard Forest (Petersham, Massachusetts, USA) which had experienced 5°C above ambient soil temperatures for 5 and 20 yr at the time of sampling. We assessed fungal diversity and community composition by sequencing the ITS2 region of rDNA using Illumina technology, along with soil C concentrations and chemistry. Three main findings emerged: (1) long‐, but not short‐term warming resulted in compositional shifts in the soil fungal community, particularly in the saprotrophic and unknown components of the community; (2) soil C concentrations and the total C stored in the organic horizon declined in response to both short‐ (5 yr) and long‐term (20 yr) warming; and (3) following long‐term warming, shifts in fungal guild relative abundances were associated with substantial changes in soil organic matter chemistry, particularly the relative abundance of lignin. Taken together, our results suggest that shifts with warming in the relative abundance of fungal functional groups and dominant fungal taxa are related to observed losses in total soil C.