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Biological Mechanisms May Contribute to Soil Carbon Saturation Patterns: Modeling Archive

This Modeling Archive is in support of a TES-SFA publication “Biological Mechanisms May Contribute to Soil Carbon Saturation Patterns” (Craig et al., 2021). We ran and evaluated a multi-assumption soil organic carbon (SOC) model to investigate whether alternative assumptions regarding constraints on soil microbial biomass could lead to soil carbon saturation patterns. We developed this model in the Multi-Assumption Architecture and Testbed (MAAT, https://github.com/walkeranthonyp/MAAT, tag: v1.2.1_Craig2021; Walker et al. 2018). Using MAAT, we embedded three alternative hypotheses in a microbially explicit three-pool SOC model: 1) the efficiency of mineral-associated SOC formation decreases as mineral-associated SOC approaches a maximum value (“Mineral saturation”), 2) the microbial biomass turnover rate increases with increasing microbial biomass (“Density-dependent turnover”), and 3) community carbon use efficiency decreases as microbial biomass increases toward an upper limit (“Density-dependent growth”). We ran a factorial combination of these hypotheses resulting in eight models for three different classes of model (linear decay, Michaelis-Menten decay, or reverse Michaelis-Menten decay), resulting in 24 models, 12 of which are presented or discussed in the related publication. Models were parameterized using values from previous studies with similar models (Wang et al. 2013, Wieder et al. 2014, Li et al. 2014, Georgiou et al. 2017, Hassink and Whitmore 1997) and ran to an approximate steady state (200 years) at six (6) different C input rates corresponding to 0.5, 1, 2, 4, 7, and 10 times the default input value. Further model details are available in the related publication. This archive contains output from three MAAT simulations, and scripts to run these simulations and process and plot the data. Simulations are labeled “lin”, “MM_highKm”, and “RMM_highKm” reflecting factorial runs for linear, Michealis-Menten, and reverse Michaelis-Menten models, respectively. This archive contains: • 3 R scripts prepended with “init_MAAT_” to initialize runs (1 for each simulation), • 1 csv file containing years over which to run simulations (“met_year.csv”), • 1 bash script (.bs) to run MAAT, • 6 XML files that are output from MAAT describing a run (2 for each simulation), • 3 model output csv files prepended by “out_” (1 for each simulation), and • 1 analysis R script for reproducing figures 3 and 4 in Craig et al. 2021. See included user guide (Craig_2021_modeling_archive_20210315.pdf) for file organization details.

54 ENVIRONMENTAL SCIENCES↗

Biological mechanisms may contribute to soil carbon saturation patterns

Increasing soil organic carbon (SOC) storage is a key strategy to mitigate rising atmospheric CO 2 , yet SOC pools often appear to saturate, or increase at a declining rate, as carbon (C) inputs increase. Soil C saturation is commonly hypothesized to result from the finite amount of reactive mineral surface area available for retaining SOC, and is accordingly represented in SOC models as a physicochemically determined SOC upper limit. However, mineral-associated SOC is largely microbially generated. In this perspective, we present the hypothesis that apparent SOC saturation patterns could emerge as a result of ecological constraints on microbial biomass—for example, via competition or predation—leading to reduced C flow through microbes and a reduced rate of mineral-associated SOC formation as soil C inputs increase. Microbially explicit SOC models offer an opportunity to explore this hypothesis, yet most of these models predict linear microbial biomass increases with C inputs and insensitivity of SOC to input rates. Synthesis of 54 C addition studies revealed constraints on microbial biomass as C inputs increase. Different hypotheses limiting microbial density were embedded in a three-pool SOC model without explicit limits on mineral surface area. As inputs increased, the model demonstrated either no change, linear, or apparently saturating increases in mineral-associated and particulate SOC pools. Taken together, our results suggest that microbial constraints are common and could lead to reduced mineral-associated SOC formation as input rates increase. We conclude that SOC responses to altered C inputs—or any environmental change—are influenced by the ecological factors that limit microbial populations, allowing for a wider range of potential SOC responses to stimuli. Understanding how biotic versus abiotic factors contribute to these patterns will better enable us to predict and manage soil C dynamics.

54 ENVIRONMENTAL SCIENCES↗

The GREEN ‘omics of Nutrient Feedbacks to Soil Warming

The GREEN ‘omics of Nutrient Feedbacks in Soil project advanced the DOE Biological and Environmental Research (BER) mission by developing and applying isotope-enabled ’omics tools to understand how soil microbes regulate carbon and nutrient cycling. Guided by the Growth Rate, growth Efficiency, and stoichiometry of Essential Nutrients (GREEN ’omics) framework, the project aimed to build a predictive, systems-level understanding of microbial traits that control ecosystem biogeochemistry. In a collaboration among Northern Arizona University (lead), West Virginia University, Lawrence Livermore National Laboratory, and Pacific Northwest National Laboratory, we combined quantitative stable isotope probing (qSIP), Chip-SIP, NanoSIMS, and genome-resolved metagenomics across long-term experiments in Arctic, boreal, temperate, and tropical ecosystems. The project produced three key outcomes: 1) We showed that community-weighted temperature sensitivities of bacterial growth (Q10) can predict ecosystem-scale soil respiration responses across diverse soils. 2) We provided the first in situ evidence for density-dependent population dynamics in soil bacteria and demonstrated that nutrient additions intensify competition, concentrating carbon use into fewer taxa. 3) We improved and extended isotope-enabled ’omics methods by quantifying qSIP measurement error to guide experimental design and coupling SIP with genome-resolved metagenomics to reveal cross-kingdom interactions among bacteria, fungi, and viruses. Together, these results show that a small number of microbial traits and taxa exert disproportionate control over soil carbon and nutrient cycling, providing critical data and methods to improve representation of microbial processes in Earth system models.

54 ENVIRONMENTAL SCIENCES↗

Nutrients strengthen density dependence of per-capita growth and mortality rates in the soil bacterial community

Density dependence in an ecological community has been observed in many macro-organismal ecosystems and is hypothesized to maintain biodiversity but is poorly understood in microbial ecosystems. Here, in this study, we analyze data from an experiment using quantitative stable isotope probing (qSIP) to estimate per-capita growth and mortality rates of bacterial populations in soils from several ecosystems along an elevation gradient which were subject to nutrient addition of either carbon alone (glucose; C) or carbon with nitrogen (glucose + ammonium-sulfate; C + N). Across all ecosystems, we found that higher population densities, quantified by the abundance of genomes per gram of soil, had lower per-capita growth rates in C + N-amended soils. Similarly, bacterial mortality rates in C + N-amended soils increased at a significantly higher rate with increasing population size than mortality rates in control and C-amended soils. In contrast to the hypothesis that density dependence would promote or maintain diversity, we observed significantly lower bacterial diversity in soils with stronger negative density-dependent growth. Here, density dependence was significantly but weakly responsive to nutrients and was not associated with higher bacterial diversity.

59 BASIC BIOLOGICAL SCIENCES↗

Taxon-specific microbial growth and mortality patterns reveal distinct temporal population responses to rewetting in a California grassland soil

Abstract Microbial activity increases after rewetting dry soil, resulting in a pulse of carbon mineralization and nutrient availability. The biogeochemical responses to wet-up are reasonably well understood and known to be microbially mediated. Yet, the population level dynamics, and the resulting changes in microbial community patterns, are not well understood as ecological phenomena. Here, we used sequencing of 16S rRNA genes coupled with heavy water (H218O) DNA quantitative stable isotope probing to estimate population-specific rates of growth and mortality in response to a simulated wet-up event in a California annual grassland soil. Bacterial growth and mortality responded rapidly to wet-up, within 3 h, and continued throughout the 168 h incubation, with patterns of sequential growth observed at the phylum level. Of the 37 phyla detected in the prewet community, growth was found in 18 phyla while mortality was measured in 26 phyla. Rapid growth and mortality rates were measurable within 3 h of wet-up but had contrasting characteristics; growth at 3 h was dominated by select taxa within the Proteobacteria and Firmicutes, whereas mortality was taxonomically widespread. Furthermore, across the community, mortality exhibited density-independence, consistent with the indiscriminate shock resulting from dry-down and wet-up, whereas growth was density-dependent, consistent with control by competition or predation. Total aggregated growth across the community was highly correlated with total soil CO2 production. Together, these results illustrate how previously “invisible” population responses can translate quantitatively to emergent observations of ecosystem-scale biogeochemistry.

58 GEOSCIENCES↗

Tipping points emerge from weak mutualism in metacommunities

The coexistence of obligate mutualists is often precariously close to tipping points where small environmental changes can drive catastrophic shifts in species composition. For example, microbial ecosystems can collapse by the decline of a strain that provides an essential resource on which other strains cross-feed. Here, we show that tipping points, ecosystem collapse, bistability and hysteresis arise even with very weak (non-obligate) mutualism provided the population is spatially structured. Based on numeric solutions of a metacommunity model and mean-field analyses, we demonstrate that weak mutualism lowers the minimal dispersal rate necessary to avoid stochastic extinction, while species need to overcome a mean threshold density to survive in this low dispersal rate regime. Our results allow us to make numerous predictions for mutualistic metacommunities regarding tipping points, hysteresis effects, and recovery from external perturbations, and let us draw general conclusions for ecosystems even with random, not necessarily mutualistic, interactions and systems with density-dependent dispersal rather than direct mutualistic interactions.

59 BASIC BIOLOGICAL SCIENCES↗