Tree species diversity increases soil microbial carbon use efficiency in a subtropical forest.

Plant communities strongly influence soil microbial communities and, in turn, soil carbon (C) cycling. Microbial carbon use efficiency (CUE) is an important parameter for predicting soil C accumulation, yet how plant and soil microbial community traits influence microbial CUE remains poorly understood. Here, we determined how soil microbial CUE is influenced by plant and soil microbial community traits, by studying a natural gradient of plant species diversity in a subtropical forest. Our results showed that microbial CUE increased with increasing tree species diversity, suggesting a correlation between plant community traits and soil C storage. The specific soil properties that explained the greatest variation in microbial CUE were associated with microbial communities (biomass, enzyme activities and the ratio of oligotrophic to copiotrophic taxa); there were weaker correlations with plant-input properties, soil chemistry and soil organic C quality and its mineral protection. Overall, high microbial CUE was associated with soil properties correlated with increased tree species diversity: higher substrate availability (simple SOM chemical structures and weak mineral organic associations) and high microbial growth rates despite increased community dominance by oligotrophic strategists. Our results point to a mechanism by which increased tree species diversity may increase the forest C sink by affecting carbon use with the soil microbial community.

Substrate availability and not thermal acclimation controls microbial temperature sensitivity response to long-term warming.

Microbes are responsible for cycling carbon (C) through soils, and predicted changes in soil C stocks under climate change are highly sensitive to shifts in the mechanisms assumed to control the microbial physiological response to warming. Two mechanisms have been suggested to explain the long-term warming impact on microbial physiology: microbial thermal acclimation and changes in the quantity and quality of substrates available for microbial metabolism. Yet studies disentangling these two mechanisms are lacking. To resolve the drivers of changes in microbial physiology in response to long-term warming, we sampled soils from 13- and 28-year-old soil warming experiments in different seasons. We performed short-term laboratory incubations across a range of temperatures to measure the relationships between temperature sensitivity of physiology (growth, respiration, carbon use efficiency, and extracellular enzyme activity) and the chemical composition of soil organic matter. We observed apparent thermal acclimation of microbial respiration, but only in summer, when warming had exacerbated the seasonally-induced, already small dissolved organic matter pools. Irrespective of warming, greater quantity and quality of soil carbon increased the extracellular enzymatic pool and its temperature sensitivity. We propose that fresh litter input into the system seasonally cancels apparent thermal acclimation of C-cycling processes to decadal warming. Our findings reveal that long-term warming has indirectly affected microbial physiology via reduced C availability in this system, implying that earth system models including these negative feedbacks may be best suited to describe long-term warming effects on these soils.

Maintaining grass coverage increases methane uptake in Amazonian pastures, with a reduction of methanogenic archaea in the rhizosphere.

Cattle ranching is the largest driver of deforestation in the Brazilian Amazon. The rainforest-to-pasture conversion affects the methane cycle in upland soils, changing it from sink to source of atmospheric methane. However, it remains unknown if management practices could reduce the impact of land-use on methane cycling. In this work, we evaluated how pasture management can regulate the soil methane cycle either by maintaining continuous grass coverage on pasture soils, or by liming the soil to amend acidity. Methane fluxes from forest and pasture soils were evaluated in moisture-controlled greenhouse experiments with and without grass cover (Urochloa brizantha cv. Marandu) or liming. We also assessed changes in the soil microbial community structure of both bare (bulk) and rhizospheric pasture soils through high throughput sequencing of the 16S rRNA gene, and quantified the methane cycling microbiota by their respective marker genes related to methane generation (mcrA) or oxidation (pmoA). The experiments used soils from eastern and western Amazonia, and concurrent field studies allowed us to confirm greenhouse data. The presence of a grass cover not only increased methane uptake by up to 35% in pasture soils, but also reduced the abundance of the methane-producing community. In the grass rhizosphere this reduction was up to 10-fold. Methane-producing archaea belonged to the genera Methanosarcina sp., Methanocella sp., Methanobacterium sp., and Rice Cluster I. Further, we showed that soil liming to increasing pH compromised the capacity of forest and pasture soils to be a sink for methane, and instead converted formerly methane-consuming forest soils to become methane sources in only 40-80 days. Liming reduced the relative abundance of Beijerinckiacea family in forest soils, which account for many known methanotrophs. Our results demonstrate that pasture management that maintains grass coverage can mitigate soil methane emissions, compared to bare (bulk) pasture soil.

Plant biodiversity promotes sustainable agriculture directly and via belowground effects.

While the positive relationship between plant biodiversity and ecosystem functioning (BEF) is well established, the extent to which this is mediated via belowground microbial processes is poorly understood. Growing evidence suggests that plant community structure influences soil microbial diversity, which in turn promotes functions desired for sustainable agriculture. Here, we outline the 'plant-directed' and soil microbe-mediated mechanisms expected to promote positive BEF. We identify how this knowledge can be utilized in plant diversification schemes to maximize ecosystem functioning in agroecosystems, which are typically species poor and sensitive to biotic and abiotic stressors. In the face of resource overexploitation and global change, bridging the gaps between biodiversity science and agricultural practices is crucial to meet food security in the Anthropocene.

Direct evidence for the role of microbial community composition in the formation of soil organic matter composition and persistence.

The largest terrestrial carbon sink on earth is soil carbon stocks. As the climate changes, the rate at which the Earth's climate warms depends in part on the persistence of soil organic carbon. Microbial turnover forms the backbone of soil organic matter (SOM) formation and it has been recently proposed that SOM molecular complexity is a key driver of stability. Despite this, the links between microbial diversity, chemical complexity and biogeochemical nature of SOM remain missing. Here we tested the hypotheses that distinct microbial communities shape the composition of SOM, and microbial-derived SOM has distinct decomposition potential depending on its community of origin. We inoculated microbial communities of varying diversities into a model soil matrix amended with simple carbon (cellobiose) and measured the thermal stability of the resultant SOM. Using a Rock-Eval® ramped thermal analysis, we found that microbial community composition drives the chemical fingerprint of soil carbon. While diversity was not a driver of SOM composition, bacteria-only communities lead to more thermally labile soil C pools than communities with bacteria and fungi. Our results provide direct evidence for a link between microbial community structure, SOM composition, and thermal stability. This evidence demonstrates the relevance of soil microorganisms in building persistent SOM stocks.

Microbial diversity drives carbon use efficiency in a model soil.

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.

Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria.

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.

Draft Genome Sequence of Acidobacteria Group 1 Acidipila sp. Strain EB88, Isolated from Forest Soil.

Here, we present the genome sequence of a member of the group I Acidobacteria, Acidipila sp. strain EB88, which was isolated from temperate forest soil. Like many other members of its class, its genome contains evidence of the potential to utilize a broad range of sugars.

Peaks of in situ N2 O emissions are influenced by N2 O-producing and reducing microbial communities across arable soils.

Agriculture is the main source of terrestrial N2 O emissions, a potent greenhouse gas and the main cause of ozone depletion. The reduction of N2 O into N2 by microorganisms carrying the nitrous oxide reductase gene (nosZ) is the only known biological process eliminating this greenhouse gas. Recent studies showed that a previously unknown clade of N2 O-reducers (nosZII) was related to the potential capacity of the soil to act as a N2 O sink. However, little is known about how this group responds to different agricultural practices. Here, we investigated how N2 O-producers and N2 O-reducers were affected by agricultural practices across a range of cropping systems in order to evaluate the consequences for N2 O emissions. The abundance of both ammonia-oxidizers and denitrifiers was quantified by real-time qPCR, and the diversity of nosZ clades was determined by 454 pyrosequencing. Denitrification and nitrification potential activities as well as in situ N2 O emissions were also assessed. Overall, greatest differences in microbial activity, diversity, and abundance were observed between sites rather than between agricultural practices at each site. To better understand the contribution of abiotic and biotic factors to the in situ N2 O emissions, we subdivided more than 59,000 field measurements into fractions from low to high rates. We found that the low N2 O emission rates were mainly explained by variation in soil properties (up to 59%), while the high rates were explained by variation in abundance and diversity of microbial communities (up to 68%). Notably, the diversity of the nosZII clade but not of the nosZI clade was important to explain the variation of in situ N2 O emissions. Altogether, these results lay the foundation for a better understanding of the response of N2 O-reducing bacteria to agricultural practices and how it may ultimately affect N2 O emissions.

The diversity of the N2O reducers matters for the N2O:N2 denitrification end-product ratio across an annual and a perennial cropping system.

Agriculture is the main source of terrestrial emissions of N2O, a potent greenhouse gas and the main cause of ozone layer depletion. The reduction of N2O into N2 by microorganisms carrying the nitrous oxide reductase gene (nosZ) is the only biological process known to eliminate this greenhouse gas. Recent studies showed that a previously unknown clade of N2O-reducers was related to the capacity of the soil to act as an N2O sink, opening the way for new strategies to mitigate emissions. Here, we investigated whether the agricultural practices could differently influence the two N2O reducer clades with consequences for denitrification end-products. The abundance of N2O-reducers and producers was quantified by real-time PCR, and the diversity of both nosZ clades was determined by 454 pyrosequencing. Potential N2O production and potential denitrification activity were used to calculate the denitrification gaseous end-product ratio. Overall, the results showed limited differences between management practices but there were significant differences between cropping systems in both the abundance and structure of the nosZII community, as well as in the [rN2O/r(N2O+N2)] ratio. More limited differences were observed in the nosZI community, suggesting that the newly identified nosZII clade is more sensitive than nosZI to environmental changes. Potential denitrification activity and potential N2O production were explained mainly by the soil properties while the diversity of the nosZII clade on its own explained 26% of the denitrification end-product ratio, which highlights the importance of understanding the ecology of this newly identified clade of N2O reducers for mitigation strategies.