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.
2