The size and diversity of microbes determine carbon use efficiency in soil.

Soil is home to a multitude of microorganisms from all three domains of life. These organisms and their interactions are crucial in driving the cycling of soil carbon. One key indicator of this process is Microbial Carbon Use Efficiency (CUE), which shows how microbes influence soil carbon storage through their biomass production. Although CUE varies among different microorganisms, there have been few studies that directly examine how biotic factors influence CUE. One such factor could be body size, which can impact microbial growth rates and interactions in soil, thereby influencing CUE. Despite this, evidence demonstrating a direct causal connection between microbial biodiversity and CUE is still scarce. To address these knowledge gaps, we conducted an experiment where we manipulated microbial body size and biodiversity through size-selective filtering. Our findings show that manipulating the structure of the microbial community can reduce CUE by approximately 65%. When we restricted the maximum body size of the microbial community, we observed a reduction in bacterial diversity and functional potential, which in turn lowered the community's CUE. Interestingly, when we included large body size micro-eukarya in the soil, it shifted the soil carbon cycling, increasing CUE by approximately 50% and the soil carbon to nitrogen ratio by about 25%. Our metrics of microbial diversity and community structure were able to explain 36%-50% of the variation in CUE. This highlights the importance of microbial traits, community structure and trophic interactions in mediating soil carbon cycling.

Shifts in bacterial traits under chronic nitrogen deposition align with soil processes in arbuscular, but not ectomycorrhizal-associated trees.

Nitrogen (N) deposition increases soil carbon (C) storage by reducing microbial activity. These effects vary in soil beneath trees that associate with arbuscular (AM) and ectomycorrhizal (ECM) fungi. Variation in carbon C and N uptake traits among microbes may explain differences in soil nutrient cycling between mycorrhizal associations in response to high N loads, a mechanism not previously examined due to methodological limitations. Here, we used quantitative Stable Isotope Probing (qSIP) to measure bacterial C and N assimilation rates from an added organic compound, which we conceptualize as functional traits. As such, we applied a trait-based approach to explore whether variation in assimilation rates of bacterial taxa can inform shifts in soil function under chronic N deposition. We show taxon-specific and community-wide declines of bacterial C and N uptake under chronic N deposition in both AM and ECM soils. N deposition-induced reductions in microbial activity were mirrored by declines in soil organic matter mineralization rates in AM but not ECM soils. Our findings suggest C and N uptake traits of bacterial communities can predict C cycling feedbacks to N deposition in AM soils, but additional data, for instance on the traits of fungi, may be needed to connect microbial traits with soil C and N cycling in ECM systems. Our study also highlights the potential of employing qSIP in conjunction with trait-based analytical approaches to inform how ecological processes of microbial communities influence soil functioning.

The predictive power of phylogeny on growth rates in soil bacterial communities.

Predicting ecosystem function is critical to assess and mitigate the impacts of climate change. Quantitative predictions of microbially mediated ecosystem processes are typically uninformed by microbial biodiversity. Yet new tools allow the measurement of taxon-specific traits within natural microbial communities. There is mounting evidence of a phylogenetic signal in these traits, which may support prediction and microbiome management frameworks. We investigated phylogeny-based trait prediction using bacterial growth rates from soil communities in Arctic, boreal, temperate, and tropical ecosystems. Here we show that phylogeny predicts growth rates of soil bacteria, explaining an average of 31%, and up to 58%, of the variation within ecosystems. Despite limited overlap in community composition across these ecosystems, shared nodes in the phylogeny enabled ancestral trait reconstruction and cross-ecosystem predictions. Phylogenetic relationships could explain up to 38% (averaging 14%) of the variation in growth rates across the highly disparate ecosystems studied. Our results suggest that shared evolutionary history contributes to similarity in the relative growth rates of related bacteria in the wild, allowing phylogeny-based predictions to explain a substantial amount of the variation in taxon-specific functional traits, within and across ecosystems.

Phylogenetic organization in the assimilation of chemically distinct substrates by soil bacteria.

Soils are among the most biodiverse habitats on earth and while the species composition of microbial communities can influence decomposition rates and pathways, the functional significance of many microbial species and phylogenetic groups remains unknown. If bacteria exhibit phylogenetic organization in their function, this could enable ecologically meaningful classification of bacterial clades. Here, we show non-random phylogenetic organization in the rates of relative carbon assimilation for both rapidly mineralized substrates (amino acids and glucose) assimilated by many microbial taxa and slowly mineralized substrates (lipids and cellulose) assimilated by relatively few microbial taxa. When mapped onto bacterial phylogeny using ancestral character estimation this phylogenetic organization enabled the identification of clades involved in the decomposition of specific soil organic matter substrates. Phylogenetic organization in substrate assimilation could provide a basis for predicting the functional attributes of uncharacterized microbial taxa and understanding the significance of microbial community composition for soil organic matter decomposition.

Land use intensification destabilizes stream microbial biodiversity and decreases metabolic efficiency.

Urbanization and agricultural intensification can transform landscapes. Changes in land-use can lead to increases in storm runoff and nutrient loadings which can impair the health and function of stream ecosystems. Microorganisms are an integral component of stream ecosystems. Due to the sensitivity of microorganisms to perturbations, changes in hydrology and water chemistry may alter microbial activity and structure. These shifts in microbial community dynamics may alter stream metabolism and water quality, potentially impacting higher trophic levels. Here we examine the effects of land-use and associated changes in water chemistry on sediment microbial communities by studying the West Run Watershed (WRW) a mixed-land-use system in West Virginia, USA. Streams were sampled throughout the growing season at six sites within the WRW spanning different levels of land use intensification. The proportion of land impacted by agricultural and urban development was positively correlated with temporal variation in stream sediment microbial community composition (adj R2 = 0.65), suggesting development can destabilize microbial communities. Moreover, streams in developed watersheds had an increased metabolic quotient (20-50% higher), this indicates that microorganisms have greater respiration per unit biomass and signifies reduced metabolic efficiency. Further, our results suggest that land use associated changes in water chemistry alter microbial function both directly and indirectly via changes in microbial community composition and biomass. Taken together our results suggest that highly developed watersheds with elevated conductivity, metal ion concentration, and pH impose stress on microbial communities resulting in reduced microbial efficiency and elevated respiration.

Stream sediment bacterial communities exhibit temporally-consistent and distinct thresholds to land use change in a mixed-use watershed.

Freshwater ecosystems are susceptible to biodiversity losses due to land conversion. This is particularly true for the conversion of land from forests for agriculture and urban development. Freshwater sediments harbor microorganisms that provide vital ecosystem services. In dynamic habitats like freshwater sediments, microbial communities can be shaped by many processes, although the relative contributions of environmental factors to microbial community dynamics remain unclear. Given the future projected increase in land use change, it is important to ascertain how associated changes in stream physico-chemistry will influence sediment microbiomes. Here, we characterized stream chemistry and sediment bacterial community composition along a mixed land-use gradient in West Virginia, USA across one growing season. Sediment bacterial community richness was unaffected by increasing anthropogenic land use, though microbial communities were compositionally distinct across sites. Community threshold analysis revealed greater community resilience to agricultural land use than urban land use. Further, predicted metagenomes suggest differences in potential microbial function across changes in land use. The results of this study suggest that low levels of urban land use change can alter sediment bacterial community composition and predicted functional capacity in a mixed-use watershed, which could impact stream ecosystem services in the face of global land use change.

Novel microbial community composition and carbon biogeochemistry emerge over time following saltwater intrusion in wetlands.

Sea level rise and changes in precipitation can cause saltwater intrusion into historically freshwater wetlands, leading to shifts in microbial metabolism that alter greenhouse gas emissions and soil carbon sequestration. Saltwater intrusion modifies soil physicochemistry and can immediately affect microbial metabolism, but further alterations to biogeochemical processing can occur over time as microbial communities adapt to the changed environmental conditions. To assess temporal changes in microbial community composition and biogeochemical activity due to saltwater intrusion, soil cores were transplanted from a tidal freshwater marsh to a downstream mesohaline marsh and periodically sampled over 1 year. This experimental saltwater intrusion produced immediate changes in carbon mineralization rates, whereas shifts in the community composition developed more gradually. Salinity affected the composition of the prokaryotic community but did not exert a strong influence on the community composition of fungi. After only 1 week of saltwater exposure, carbon dioxide production doubled and methane production decreased by three orders of magnitude. By 1 month, carbon dioxide production in the transplant was comparable to the saltwater controls. Over time, we observed a partial recovery in methane production which strongly correlated with an increase in the relative abundance of three orders of hydrogenotrophic methanogens. Taken together, our results suggest that ecosystem responses to saltwater intrusion are dynamic over time as complex interactions develop between microbial communities and the soil organic carbon pool. The gradual changes in microbial community structure we observed suggest that previously freshwater wetlands may not experience an equilibration of ecosystem function until long after initial saltwater intrusion. Our results suggest that during this transitional period, likely lasting years to decades, these ecosystems may exhibit enhanced greenhouse gas production through greater soil respiration and continued methanogenesis.