Elevated [CO₂] enhances soil respiration and AMF abundance in a semiarid peanut agroecosystem

Highlights

• Elevated atmospheric carbon dioxide [CO₂] increased soil respiration by 82%.

• Elevated [CO₂] increased arbuscular mycorrhizal fungi by 49%.

• Drought enhanced the positive effect of Elevated [CO₂] on arbuscular mycorrhizal fungi.

• Soil microbial abundance and β-Glucosidase activity were not altered by Elevated [CO₂].

Abstract

Rising atmospheric carbon dioxide [CO₂] is a main climate change driver, and soil respiration is the most relevant contributor to ecosystem respiration. However, the soil microbiome and respiration responses of semiarid agroecosystems under elevated [CO₂] (eCO₂) conditions must be better understood. In particular, peanut agroecosystems host rhizobia and arbuscular mycorrhizal fungi (AMF) associations. Here, we sought to address the following questions: a) Does eCO₂ conditions (650 µmol CO₂ m⁻² s⁻¹, +250 µmol CO₂ m⁻² s⁻¹, aCO₂, control) alter soil chemical properties, soil microbial community size and composition, soil respiration, and β-Glucosidase activity? b) Are these responses influenced by transient water deficit periods? We conducted this study in a typical West Texas semiarid region (no well-watered treatment and drought was not an experimental factor) during two consecutive growing seasons (May-Oct). We induced the atmospheric CO₂ enrichment using field-installed Canopy Evapotranspiration and Assimilation (CETA) systems. Our results showed no consistent significant changes in soil moisture, C: N ratio, total soil microbial EL-FAME abundance, or β-Glucosidase activity. However, we found that eCO₂ increased soil temperature (+1 °C), AMF abundance (EL-FAME marker, +49%), and soil respiration (+82%). Our findings suggest that in future semiarid climates, peanut agroecosystems may experience: 1) increased soil metabolic activity as a result of increased autotrophic respiration; 2) increased AMF, which could further facilitate plant nutrient and water uptake; and 3) minimal change in the total size of the microbial community and C cycling enzyme activity during the growing season. In this manuscript, we demonstrated that soil respiration and temperature could be indicators of ecosystem productivity and climate feedback. Furthermore, soil organic carbon and AMF were good indicators of poor nutrient soil ecosystem transitional health across well-watered and water-deficit cycles. This study will increase our understanding of how these changes will affect soil ecology and climate feedback and will provide new insight into the peanut agroecosystem carbon source/sink functioning and productivity in future climates.

Introduction

The predicted increase in atmospheric carbon dioxide [CO₂] will alter agroecosystem productivity (Anderson et al., 2012, Ryan et al., 2017, Ziemblińska et al., 2016) through changes in the plant growth and soil microbial communities (Drigo et al., 2010). Carbon sequestration by plants and soils has helped counteract rising atmospheric [CO₂] (Cramer et al., 2001; Drigo et al., 2008). At current atmospheric levels, the [CO₂] in the soil interspace can reach about 2000–38000 ppm. Thus, belowground plant roots and soil fauna are already exposed to very high [CO₂] (Drigo et al., 2008), and most of them have developed strategies to cope with this enriched [CO₂] microenvironment. In this context, the predicted changes in atmospheric [CO₂] are most likely to impact the belowground components through plant compensatory adjustments (Miguel Feijó Barreira et al., 2018).

Soil respiration (Rs) is the result of CO₂ efflux at the biosphere-pedosphere interface through heterotrophic respiration (litter, soil organic carbon, and rhizo-deposit decomposition by free soil microbes and microbe’s extracellular enzymes) and autotrophic/belowground plant respiration (including seed, roots, and microbial roots’ respiratory enzymes) (Hanson et al., 2000; Wang et al., 2014; Zhu et al., 2016). Soil respiration could be altered by abiotic and biotic factors, including changes in atmospheric [CO₂], soil moisture, and soil microbial community structure and function. Previous research confirmed the increased Rs trend over time (Bond-Lamberty et al., 2018), indicating a significant environmental concern. Along with this trend, rising atmospheric [CO₂] stimulates Rs in diverse ecosystems (Chen et al., 2021; Gao et al., 2020a; Meeran et al., 2021), leading to soil carbon losses and potentially a reduced ecosystem C sink capacity. Soil water content may influence Rs (Moinet et al., 2019); thus, during drought episodes, Rs can be reduced (Borken et al., 2006, Meeran et al., 2021, Selsted et al., 2012; Wang et al., 2014; Zhou et al., 2020) by 17% (Zhou et al., 2020). Overall, this drought-induced decrease in Rs may be minimized by rising CO₂ conditions.

Soil health is the term used to describe a functional ecosystem for sustainable life (Lehmann et al., 2020). Soil microbial communities drive 80–90% of the soil decomposition processes (Hanson et al., 2000) and play a critical role in soil health. In this context, increased rhizosphere respiration may result from complex interactions between factors associated with plant-soil-microbe relations (Drigo et al., 2008). Furthermore, plant decomposition and nutrient incorporation in soil are driven by extracellular soil enzyme activities (EAs) produced by microbes. These EAs can be stabilized in the soil matrix, including the C cycling enzyme (β-Glucosidase), which is involved in the limiting step of cellulose degradation and is used as an indicator of microbial C cycling rate (Wilson and Franklin, 2002). These responses might vary with climatic changes. For example, the effects of elevated [CO₂] (eCO₂) may be influenced by variations in soil water, soil temperature (Drake et al., 2018), and nutrient availabilities (Oren et al., 2001, Terrer et al., 2016). Overall, the positive effect of eCO₂ on Rs, even in warm and dried environments, has been extensively reported (Gao et al., 2020b, Meeran et al., 2021). The increase in C uptake by plants under high CO₂ shifts the C balance, and plants may use different compensatory mechanisms to counterbalance this shift. Plant compensatory mechanisms refer to the ability of plants to offset the negative impact of stress by coordinated physiological adjustments. Compensatory growth is the ability of plants to recover from the stress by restoring growth and development (Mangel and Munch, 2005), and it is also related to resiliency, stress survival strategy, and stability at the organism and ecosystem level (Gonzalez and Loreau, 2009; Li et al., 2021).

Peanuts can form symbiotic associations with both mycorrhizal fungi and N₂ fixation bacteria. The symbiotic association, combined with the unique biology of pod development belowground and adaptation to semiarid conditions, makes the peanut agroecosystem a unique and impactful model for understanding plant-microbial relationships in response to climatic variability. However, the impact of rising [CO₂] on soil microbial communities in peanut agroecosystems, especially in nutrient- and water-limited semiarid environments, still needs to be better understood. Fig. 1 shows the proposed conceptual model of the effects of eCO₂ in a semiarid peanut agroecosystem (Fig. 2).

The main objective of this study was to investigate the effects of eCO₂ on the soil microbial community size, structure, activities (respiration and C cycling enzyme activity), and other selected chemical properties in semiarid peanut agroecosystems subjected to drying and wetting cycles. Our previous work highlights the increased biomass productivity and C uptake under enriched CO₂ conditions (Laza et al., 2021), which has been associated with increased in soil respiration. AMF has also been reported as a significant driver (12%) of the total Rs in forests (Zheng et al., 2022). Based on such results, we hypothesized that in peanuts, which is a strong C sink crop (Laza et al., 2021), the induced increase in C uptake, plant growth, and C allocation belowground (hence the demand for water and nutrients) by eCO₂, may stimulate plant interactions with beneficial microbes (AMF), increasing Rs.