Predominance of positive priming effects induced by algal and terrestrial organic matter input in saline lake sediments

Abstract

Priming effect (PE) is a key biogeochemical process regulating organic carbon mineralization. However, the impacts of climate change-related factors on PE remain largely unclear in lakes with a large salinity range. The patterns of PE induced by algal (¹³C-labeled Chlorella vulgaris) and terrestrial grass (¹³C-labeled Festuca ovina) organic matter (OM) at 8 °C and 18 °C were investigated in lake sediments with a salinity range from 0.7 to 376.3 g L⁻¹. The results showed that the intensities of early (7^th day) and late (42^nd day) PEs in the studied lake sediments ranged −51.0%–3833.7% and −55.2%–1874.5% of basal respiration, respectively; positive PE predominated over negative PE. Climate-related factors (e.g., salinity, temperature, OM types) exhibited significant influences on the intensity and/or direction of PE. Positive PE was more likely to occur in the sediments of hypersaline lakes than in freshwater/saline lakes, while negative PE showed an inverse trend. PE intensity induced by algal OM was significantly different at 8 °C and 18 °C, but no temperature influence was observed for that induced by grass OM. The effect of temperature increase on PE induced by algal OM was negative and positive in the early and late stages of incubation, respectively. The types of OM (algal OM vs. grass OM) supply significantly (P < 0.05) affected PE intensity except for the late PE intensity at 8 °C. Overall, these results suggest that organic carbon mineralization in lake sediments may be enhanced by positive PEs induced by the increased input of both allochthonous and autochthonous OM, and the autochthonous OM-induced PE is more susceptible to climate warming than that by allochthonous OM. These results help understand the carbon cycle in lakes under global climate change.

Introduction

The priming effect (PE) is an increase (positive PE) or decrease (negative PE) in the mineralization of native organic carbon resulting from the input of fresh organic matter (OM) (Bernard et al., 2022, Guenet et al., 2010, Kuzyakov, 2010). PE intensity has been considered one key modeling parameter for estimating carbon storage in ecosystems, playing a pivotal role in predicting the global carbon budget (Guenet et al., 2018). Up to now, although PE intensity has been widely evaluated in a huge number of soils, limited attention has been paid on the estimation of PE intensity in aquatic ecosystems (e.g., lakes), which are important component of the global carbon cycle (Bengtsson et al., 2018, Bianchi, 2011).

Lakes are globally distributed aquatic ecosystems that emit approximately 0.6 Pg carbon per year to the atmosphere, contributing significantly to the global carbon budget (Cole et al., 2007, Holgerson and Raymond, 2016, Tranvik et al., 2009). Quantifying PE intensity in lakes is of great significance for understanding global carbon cycling. Previous studies have shown that the input of algal and terrestrial plant OM can induce positive or negative PE, with their potential intensities ranging from −23.2% to 44.8% and from 12.8% to 265.4% of the basal respiration in lake water and sediment, respectively (Bengtsson et al., 2018, Wang et al., 2021c, Yang et al., 2022b). So far, the datasets of lake PE intensity are very scarce, which is far from being employed for carbon storage model prediction; more efforts are needed to investigate PE intensity in lake ecosystems.

It is widely recognized that positive PE can be driven by two distinct microbial mechanisms: stoichiometric decomposition and nutrient mining (Chen et al., 2014, Fontaine et al., 2004, Razanamalala et al., 2018, Yang et al., 2020a). The stoichiometric decomposition theory indicates that microbial decomposers of fresh OM release extra extracellular enzymes to promote the mineralization of native OM. The nutrient mining theory believes that microbial cometabolisms stimulate some microorganisms to extract nutrients from native OM to enhance their growth, thereby increasing the mineralization of native OM (Blagodatskaya and Kuzyakov, 2008, Fontaine et al., 2003, Razanamalala et al., 2018). Previous studies have suggested that in response to the input of fresh OM, stoichiometric decomposition mechanism usually governs the early stage of PE generation, while nutrient mining mechanism frequently controls the late stage of PE generation when available nutrients are depleted (Razanamalala et al., 2018, Yang et al., 2020a). Considering the different generation mechanisms of early and late PE, it is reasonable to hypothesize that the regulatory factors of their intensities will be distinctly different in lakes.

In recent decades, climate change has remarkably altered lake environmental conditions (Guo et al., 2022, Wang et al., 2018, Woolway et al., 2020, Yan and Zheng, 2015). For example, dry climate accelerates water evaporation, reduces water storage, and thus increases lake salinity; in contrast, a humid climate increases precipitation, increases lake storage, and thus reduces lake water salinity. In addition, climate warming increases the temperature of lake water. These changing environment conditions may affect PE intensity in lakes (Yang et al., 2020a, Yang et al., 2022b). Therefore, it is of great significance to explore environmental impact on PE intensity for assessing the carbon feedbacks of lakes on climate change. Mounting evidences indicate that PE intensity can be regulated by many factors, such as temperature, pH, organic carbon content, organic carbon stability, the properties of supplied OM (Bastida et al., 2019, Chen et al., 2019, Finley et al., 2018, Liu et al., 2020, Reinsch et al., 2013, Ren et al., 2022, Wang et al., 2016, Zhang et al., 2019). The abovementioned PE intensity-regulating factors are primarily revealed in soil studies, except for two recent studies about the influence of salinity on the PE intensity in lake sediments (Yang et al., 2020a, Yang et al., 2022b). Hence, much remains unknown about the dominant factors regulating lake PE intensity. This knowledge gap has greatly hindered the prediction of lake carbon dynamics under global change. Additionally, it is also important to reveal the patterns of lake PE intensity under different temperatures, which is crucial to understand the temperature sensitivity of PE intensity and its feedback to climate warming (Zhang et al., 2022). Such knowledge is still lacking in lakes, which limits the understanding of lake carbon dynamics.

To address these knowledge gaps in lake PE intensity and its regulating factors, this study selected widespread lake algae (¹³C-labeled Chlorella vulgaris) and terrestrial grass leaf (¹³C-labeled Festuca ovina) as typical representatives of autochthonous and allochthonous OM types, respectively, and conducted laboratory simulation incubation experiments at 8 °C and 18 °C to investigate the PE generation process in the microcosms of lake sediments with different salinities ranging 0.7–376.3 g L⁻¹. The objectives of this study were to (1) quantify early and late PE intensities in the lake sediments with different salinities; (2) reveal the differences of the PE intensity patterns in response to different OM supplies (algal OM vs. terrestrial grass OM) and incubation temperatures (8 °C vs. 18 °C); and (3) assess the regulating factors of lake PE intensities.