Carbon control on terrestrial ecosystem function across contrasting site productivities: the carbon connection revisited

Abstract

Understanding how altered soil organic carbon (SOC) availability affects microbial communities and their function is imperative in predicting impacts of global change on soil carbon (C) storage and ecosystem function. However, the response of soil microbial communities and their function to depleted C availability in situ is unclear. We evaluated the role of soil C inputs in controlling microbial biomass, community composition, physiology, and function by (1) experimentally excluding plant C inputs in situ for 9 yr in four temperate forest ecosystems along a productivity gradient in Oregon, USA; and (2) integrating these findings with published data from similar C‐exclusion studies into a global meta‐analysis. Excluding plant C inputs for 9 yr resulted in a 13% decrease in SOC across the four Oregon sites and an overall shift in the microbial community composition, with a 45% decrease in the fungal : bacterial ratio and a 13% increase in Gram‐positive : Gram‐negative bacterial ratio. Although gross N mineralization decreased under C exclusion, decreases in gross N immobilization were greater, resulting in increased net N mineralization rates in all but the lowest‐productivity site. Microbial biomass showed a variable response to C exclusion that was method dependent; however, we detected a 29% decrease in C‐use efficiency across the sites, with greater declines occurring in less‐productive sites. Although extracellular enzyme activity increased with C exclusion, C exclusion resulted in a 31% decrease in microbial respiration across all sites. Our meta‐analyses of published data with similar C‐exclusion treatments were largely consistent with our experimental results, showing decreased SOC, fungal : bacterial ratios, and microbial respiration, and increased Gram‐positive : Gram‐negative bacterial ratio following exclusion of C inputs to soil. Effect sizes of SOC and respiration correlated negatively with the duration of C exclusion; however, there were immediate effects of C exclusion on microbial community composition and biomass that were unaltered by duration of treatment. Our field‐based experimental results and analyses demonstrate unequivocally the dominant control of C availability on soil microbial biomass, community composition, and function, and provide additional insight into the mechanisms for these effects in forest ecosystems.

Changes in plant inputs alter soil carbon and microbial communities in forest ecosystems

“…This mechanism can also explain the increased GP‐to‐GN ratio under litter removal, as most Gram‐positive bacteria are oligotrophic communities and can use more recalcitrant C sources from SOM like fungi (Kramer & Gleixner, 2008; Zechmeister‐Boltenstern et al, 2015). Beyond reducing belowground C inputs by root exclusion, root removal can also directly decrease the biomass of symbiotic fungi (e.g., arbuscular mycorrhizal and ectomycorrhizal fungi) associated with plant roots (Dove et al, 2019; Whalen et al, 2021). Therefore, root removal induced larger negative effects on fungi than bacteria (24.8%, 95% CI: 16.2%–32.4% vs. 13.9%, 95% CI: 6.6%–20.6%; p = .049), and consequently decreased fungal‐to‐bacterial ratio (Figure 2c).…”

“…Similar to litter addition, litter removal also increased fungal-to-bacterial ratio, likely because litter removal caused continuous losses of soil labile C (Figures 2 and 6b; Lajtha, Townsend, et al, 2014), and fungi can produce oxidative enzymes more efficiently than bacteria to decompose recalcitrant C to maintain their growth (Cusack et al, 2011). This mechanism can also explain the increased GP-to-GN ratio under litter removal, as most Gram-positive bacteria are oligotrophic communities and can use more recalcitrant C sources from SOM like fungi (Kramer reducing belowground C inputs by root exclusion, root removal can also directly decrease the biomass of symbiotic fungi (e.g., arbuscular mycorrhizal and ectomycorrhizal fungi) associated with plant roots (Dove et al, 2019;Whalen et al, 2021). Therefore, root removal induced larger negative effects on fungi than bacteria (24.8%, 95% CI: 16.2%-32.4% vs. 13.9%, 95% CI: 6.6%-20.6%; p = .049), and consequently decreased fungal-to-bacterial ratio (Figure 2c).…”

“…Plant inputs from litter (refers to aboveground litter hereafter) and roots are the dominant source of carbon (C) pools in soils and regulate soil biogeochemical processes and microbial communities in terrestrial ecosystems (Dove et al, 2019). The altered plant productivity and C allocation between above‐ and belowground components under global changes (e.g., elevated CO 2 , warming and nutrient deposition) can change the quantity and quality of plant inputs introduced into the soil (Janssens et al, 2010; Sayer et al, 2011; Terrer et al, 2016).…”

Aboveground litter inputs determine carbon storage across soil profiles: a meta-analysis

“…However, such management practices not only differ in the quality and quantity of organic matter added or removed from the ecosystem but can also entail substantial soil disturbance. Although previous meta-analyses have investigated how litter manipulation, biomass harvesting, thinning, or straw incorporation affects soil C storage (Nave et al 2010;Xu et al 2013;James and Harrison 2016;Zhang et al 2018;Dove et al 2019;Mathew et al 2017Mathew et al , 2020, there is still much uncertainty in our understanding of how changes in aboveground plant litter inputs will affect soil C storage. Importantly, we know very little about how soil C content is affected at different soil depths across ecosystems and whether the impact of treatments increases or attenuates over time.…”

Continental-scale patterns of extracellular enzyme activity in the subsoil: an overlooked reservoir of microbial activity

“…Because EEs both respond to and influence soil properties, the study of EEs has led to greater insights into soil C persistence (Billings & Ballantyne 2013;Birge et al 2015;Dove et al 2019), nitrogen (N) and phosphorus (P) mineralization Waring et al 2014;Chen et al 2018), ecosystem development (Olander & Vitousek 2000;Selmants & Hart 2010;Turneret al 2014), and microbial metabolism (Sinsabaugh & Shah 2011Sinsabaugh et al 2013). Given that the methods for measuring EE activity in soils are relatively high-throughput, inexpensive, and reproducible across laboratories (Dick et al2018), it is one of the most common soil biogeochemical measurements ('Soil extracellular enzyme activity' resulted in 2,013 records using Clarivate Analytics Web of Science as of Jan. 28, 2020).…”