availability during vegetation restoration under different climate conditions in karst soil
Dan Xiao1,2,#, Xunyang He1,2,#, Wei Zhang1,2*, Peilei Hu 1,2, Mingming Sun 2,3, and Kelin Wang1,2*
1Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha 410125, China
2Huanjiang Observation and Research Station for Karst Ecosystems, Chinese Academy of Sciences, Huanjiang 547100, China
3 College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China
# These authors contributed equally to the manuscript.
*Corresponding author:
Wei Zhang (E-mail: zhangw@isa.ac.cn ; Tel: 86-0731-84619720; Fax: 86-0731-84612685) and Kelin Wang (E-mail:kelin@isa.ac.cn ; Tel: 86-0731-84615201; Fax: 86-0731-84612685)
Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha 410125, China
Abstract
To determine the mechanisms underlying the response of microbial interactions to vegetation restoration under different climate conditions, we examined the changes occurring at two temperature levels in soil bacterial, fungal, and protist microbiomes under a reference cropland and a plantation forest and a shrubland. Bacterial and protist diversity levels in the high-temperature region of Guangxi (20.9 °C) were higher in cropland than in shrubland or plantation forest. By contrast, fungal richness was lower under cropland than shrubland. The bacterial phyla Cyanobacteria, Gemmatimonadetes, and Nitrospirae, the fungal taxa Ascomycota and Mucoromycota, and the protist groups Ciliophora, Lobosa, and Ochrophyta had lower abundance under vegetation restoration than cropland. There were no significant differences between shrubland and plantation forest in terms of bacterial, fungal, or protist diversity or community composition. A co-occurrence network revealed higher numbers of correlated links among bacterial, fungal, and protist taxa in the low-temperature region of Guizhou (14.6 °C) than Guangxi. Stronger interactions were observed among microbial taxa under cropland than under vegetation restoration. Protist groups Cercozoa and Lobosa showed the highest numbers of links with bacterial phyla Acidobacteria and Proteobacteria and with fungal phylum Ascomycota. Hence, a strong food web existed among these microbiomes. Proteobacteria, Acidobacteria, Ascomycota, and Cercozoa were correlated with soil nutrient levels. Therefore, these dominant taxa determined nutrient availability. The predation of bacteria and fungi by protists was more intense at low temperature than high temperature. Key bacterial, fungal, and protist groups, their co-occurrence networks, and environmental temperature influence soil nutrient accumulation during vegetation restoration.
Keywords :
Climate level, Co-occurrence network, Karst ecosystem, Soil nutrient, Vegetation type
1 INTRODUCTION
Soil microbes are the key drivers in nutrient cycling and storage, which in turn, determine ecosystem stability. Microbial diversity and community composition are affected by soil nutrient availability, vegetation type, and climate conditions (Fan et al., 2020; Liu et al., 2019a; Waldrop et al., 2006). Global warming and rainfall strongly influence plant growth and substrate properties and influence atmospheric carbon (C) and nitrogen (N) dynamics (such as CO2 and N2O flux) by increasing microbial activity (Crowther et al., 2019; Talukder et al., 2021). Understanding the mechanism by which microorganisms respond to temperature and precipitation during vegetation restoration is vital for predicting soil nutrient maintenance and the effects of global climate change on it.
Bacteria, fungi, and protists play fundamental roles in regulating soil nutrient cycling. Bacterial and fungal taxa utilize different substrates (Schneider et al., 2012; van der Wal et al., 2013). Most bacterial groups such as the Proteobacteria and Actinobacteria prefer abundant resources (Baldrian et al., 2012; Fierer et al., 2012; Schneider et al., 2012). However, certain oligotrophs such as the Acidobacteria adapt to poor nutrient environments such as low C content (Ai et al., 2015). Compared to bacteria, fungi can tolerate extreme environments. Ascomycota and the Basidiomycota degrade recalcitrant carbon (van der Wal et al., 2013). Thus, the functions of bacteria and fungi differ under rich and limiting nutrient conditions. Protists directly consume bacteria and fungi under limiting available sources and play a key role in soil food web stability (Geisen et al., 2018, 2021). Consequently, bacterial and fungal population sizes and community compositions are modified by protists, which therefore, indirectly affect nutrient availability (Geisen et al., 2018). Previous studies focused on the impact of bacterial and fungal abundance and diversity on soil nutrient cycling (Lian et al., 2017; Xiao et al., 2017). However, the potential interactions among bacteria, fungi, and protists in co-occurrence networks and changes in soil nutrient (C, N, and P) levels are poorly understood. Co-occurrence patterns may involve biotic interactions (Kara et al., 2013). Vegetation restoration and climate conditions are key factors determining soil C, N, and P availability. Hence, they indirectly affect soil microbial communities. For this reason, it is useful and informative to explore the microbiological mechanisms controlling soil nutrient levels under various vegetation types and climate conditions.
Variations in the soil nutrients exploited by microbial communities are influenced by vegetation type, temperature, and precipitation. Plant diversity increases when cropland is converted to vegetation restoration. There are numerous plant species under natural vegetation restoration as opposed to a single species under managed vegetation restoration (Hu et al., 2020; Ladygina et al., 2010; Lan and Sediments, 2021). High plant diversity increases nutrient (and especially organic C) levels through litter input and root exudates. In this manner, it induces microbial growth and alters microbial community composition (Liu et al., 2008; Mellado-Vázquez et al., 2016). Temperature and precipitation directly and indirectly affect microbial communities. Low temperature and precipitation levels limit microbial growth (Pettersson and Bååth, 2003; Pietikainen et al., 2005; Stefan et al., 2014; Zhou et al., 2012). By contrast, elevated temperature and precipitation stimulate plant growth and root exudation, thereby indirectly enhancing microbial activity (Zhou et al., 2012). Climate level and vegetation type can influence microbial communities. Nevertheless, it is uncertain whether bacterial, fungal, or protist communities differ under natural and managed vegetation restoration on calcareous (alkaline karst) soils in response to climate change.
The karst region is distributed across southwestern China and covers an area of about 550,000 km2 (Jiang et al., 2014). Karst ecosystems are fragile; their substrate consists of shallow, discontinuous soil (Liu et al., 2019b; Wang et al., 2019). However, human population pressure forced agricultural expansion through the twentieth century and rapidly degraded the land in this region (Wang et al., 2019; Wen et al., 2016). Soil nutrient (organic C and total N) loss occurs more rapidly in karst than non-karst ecosystems when the forest is anthropogenically converted to cultivation (Chen et al., 2012; Li et al., 2021; Zhang et al., 2013). Several ecological restoration projects such as the ‘Grain-for-Green’ project were implemented to restore and reconstruct vegetation in karst regions (Wang et al., 2004; Wang et al., 2019). Natural and artificial vegetation restoration measures were then widely promoted in these areas (Hu et al., 2018; Li et al., 2021; Wang et al., 2019). Understanding the mechanism underlying the response of microorganisms to different restoration measures in karst region contributes to nutrient accumulation and ecosystem stability. Soil pH was the key factor determining microbial community composition there. The relatively high pH and Ca content characteristic of karst soil suggest that its microbial diversity and community composition differ from those of non-karst soils in response to vegetation restoration (Hu et al., 2021; Lan and Sediments, 2021). However, it is unknown how bacteria, fungi, protists, and their interactions regulate nutrient availability in calcareous soils during vegetation restoration especially in response to changes in temperature and precipitation.
We selected plantation forest, a shrubland, and a cropland in the karst region and compared their soil properties and microbial (bacterial, fungal, and protist) profiles under two different climate conditions. The aims of this study were to 1) identify the key factors contributing to changes in bacterial, fungal, and protist diversity and community composition, 2) elucidate the interactive relationships among bacterial, fungal, and protist groups, and 3) determine the key microbiome controllers under natural and managed vegetation restoration and different climate conditions. We hypothesized that 1) bacterial, fungal, and protist community compositions differ between cropland and natural and managed vegetation restoration as microbial diversity is relatively higher under natural than managed vegetation restoration, and 2) the associations among bacterial, fungal, and protist groups are stronger under high temperature and precipitation than they are under conditions of low temperature and precipitation.
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