Climate warming alters the soil microbial association network and role of keystone taxa in determining wheat quality in the field
Introduction
The critical role of soil microbes, such as bacteria, fungi, and arbuscular mycorrhizal (AM) fungi, in terrestrial nutrition cycling is now well understood (Fierer, 2017). For instance, studies of soil bacteria have shown that these tiny organisms strongly influence biological decomposition (Hossain and Sugiyama, 2020) and mineralization (Carrillo et al., 2016), and the release of greenhouse gases (CO2, N2O, and CH4) from soil (Kong et al., 2016). These processes can affect plants’ growth and productivity by mediating their nutritional status and biogeochemical cycles (Mooshammer et al., 2014). The fungi, another group of essential organisms (biotas) in soil (Taylor et al., 2010), serve as engines of carbon- and nutrient-recycling of dead organic matter (such as forms of nitrogen and phosphorus) into other living organisms and the atmosphere (Talbot et al., 2015), which also can strongly impact plant development. Among them, the arbuscular mycorrhizal (AM) fungi are notably beneficial to plants, because they engage in mutualistic symbiosis with about 80% of extant terrestrial plant species, including agricultural crops (Parniske, 2008; Zhang et al., 2019). This fungal type provides its host with water, minerals, and nutrients (Smith and Read, 2008), and can also enhance the tolerance of drought (Augé et al., 2015), salinity (Porcel et al., 2012), and heavy metal toxicity (Cornejo et al., 2013, Tamayo et al., 2014) by host plants, even their resistance to diseases (El-Sharkawy et al., 2018).
It is also well known that soil microbes not only play a pivotal role in plants’ quality and yield, but they also harbor a sensitive composition and functional response to various plant growth stages and environmental changes such as climate warming (Shi et al., 2020b). For example, by analyzing 126 samples at different temperatures, Zhou et al. (2016) showed that environmental temperature has a pervasive influence on the variation in soil microbial diversity through. However, such studies are mostly focused on forest grassland or tundra soils, leaving fewer studies available concerning how temperature affects soil microorganisms in agricultural soils, especially in wheat fields (Y. Li et al., 2021).
Climate warming poses one of the most serious challenges to plants’ growth in the future (Reich et al., 2018). Particularly, it has already led to marked changes in the biodiversity of plants and animals, as well as microbial biodiversity (Yu et al., 2018). Some studies reported that elevated temperatures could increase microbial activity and cause shifts in the microbial community to adapt to higher temperatures (Zhang et al., 2005, Bradford et al., 2008); however, other research has reported that climate warming strongly reduces microbial activity (Zhang et al., 2015). Several viewpoints were laid down to explain these conflicting results, such as the modulating effects of moisture change (Zhou et al., 2016). Some studies found that physiological changes in plants could affect the soil microbial community, and these arguably could be altered by climate warming (Damatta et al., 2009). Such findings suggest the effect of climate warming upon the microbial community belowground is not only directly caused by rising temperature but is also linked to a plant’s growth conditions during its exposure to climate warming.
Microbes living in soils are rarely independent, instead, they are apt to form ecological clusters and complex interactions that include mutualism, commensalism, and parasitism (Faust and Raes, 2012, Banerjee et al., 2016). It is well known that less than 1% of all microbial organisms can be cultured using current technology (Fierer, 2017). But thanks to the co-occurrence analysis approach, it is now possible to investigate these complicated interactions between the microbes (Faust et al., 2012). A fair number of previous studies have quantified microbial association network patterns in forest (Ma et al., 2016, Ma et al., 2020), grassland (Shi et al., 2019) and agriculture soils (Jiao et al., 2019, Shi et al., 2020a), often finding they could vary along environmental gradients (e.g., nutrient cycling, interannual climate). Yet, surprisingly little is known about how such associated networks of co-occurring microbial taxa may change under climate warming conditions (Yuan et al., 2021). Further, species within the network (i.e., the nodes) have different roles due to their topological positions (Faust et al., 2015). Some nodes feature more connections within the ecological clusters (i.e., module hubs), whereas other nodes are highly connected between ecological clusters (i.e., connectors), but occasionally some nodes emerge in the network highly connected within and between the ecological clusters (network hubs); those left-over nodes lacking lower or no connections in the network are termed ‘peripherals’ (Guimerà and Amaral, 2005, Poudel et al., 2016). Usually, the above nodes which play hubs or connectors role in the network are defined as keystone species (Banerjee et al., 2018). More recently, it was shown that the complexity of a microbial network and its number of keystone species could be augmented under warming conditions (Yuan et al., 2021), and another study reported that keystone species had positive roles in determining crop production levels (Fan et al., 2020a, Fan et al., 2020b). However, before generalizations can be made, more empirical evidence is needed from various terrestrial ecosystems. Due to their critical role in food security and supply, it is imperative that we investigate the microbial networks in soils of agricultural lands under expected climate warming conditions.
Wheat (Triticum aestivum) was selected for study here because it grows on 225 million hectares worldwide at latitudes of 60°N to 44°S. Around 600 million tons of wheat are harvested annually (Ekboir, 2002). Globally, wheat is a vital staple food crop, accounting for about 20% of the calories consumed by all humans (Brenchley et al., 2012). Therefore, the significance of maintaining the safety of wheat productivity cannot be ignored and the pivotal role of soil microbes in nutrition cycling and plant growth cannot be overlooked under climate warming scenarios. Our study aimed to identify the effects of plant growth associated with climate warming on the soil microbial community under a warming treatment. We hypothesized that warming and wheat growth would alter the structure and association network of the microbial community, and that the number of keystone species would increase due to warming effects. Additionally, these changes in soil microbes driven by warming were anticipated to have close relationships with grain mass or quality.
Section snippets
Study site
The field experiment was carried out on sandy soil farmland (soil type: Ochric Aquic Cambosols) at Henan University, Kaifeng, in Henan Province, China (E: 114.23, N: 34.52; elevation: 73 m a.s.l.). The site lies within a temperate continental monsoon climate, characterized by dry springs that follow dry and cold winters with strong winds (Wang et al., 2020). Precipitation averages 670 mm annually while the mean annual temperature is 14 °C, with a minimum and maximum monthly average of − 4 °C
Effects of warming on soil physical and chemical properties as well as grain quality and mass
At the maturation stage, the temperature was significantly higher in the soil of the warming plots than no-warming plots (Fig. S1a), but average soil moisture was significantly lower at the maturation stage than at CK, although there was no difference between CM plots and WM plots (Fig. S1b). For the pH, total carbon, total nitrogen, and total phosphorus values in soil, there were no significant differences among these plots (Fig. S1c–f).
The sugar and protein contents and Zeleny of wheat grain
Discussion
Agricultural ecosystems are sensitive to environmental changes and extremely vulnerable to climate change (Beck, 2013). Soil microbes within agroecosystems play an important role in nutrition cycling and are sensitive to environmental changes (Fierer, 2017). Thus, climate change is having a huge impact on the interactions that occur between a soil microbial community and agro-ecosystem health as well as plant growth (Castro et al., 2010, Lupatini et al., 2017). However, most studies have
Conclusion
In summary, the response of soil microbial communities to the experimental warming demonstrated the changes induced by temperature and wheat plant growth in the microbial community structure. It suggests that climatic warming could alter ecosystem functioning by altering the soil microbial community in an agroecosystem. Wheat planting and warming not only can influence the microbial association network but they also can increase the number of the keystone species, especially promoting the role
Funding
This work was supported by the National Natural Science Foundation of China [grant number 42077053] and the Major Public Welfare Projects in Henan Province [grant number 201300311300].
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We would like to thank Xi Wang, Shanshan Shuai, and Yannan Li of Henan University, for their support in carrying our experiment, as well as the editors from service center Elixigen Co. for assistance during the preparation of this manuscript.
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