Climate warming alters the soil microbial association network and role of keystone taxa in determining wheat quality in the field

Highlights

• Warming can enhance network complexity but wheat planting may weaken it.

• Wheat planting and warming could increase the number of microbial keystone species.

• Keystone species had the strongest relationship with grain mass and quality.

Abstract

The soil microbial community is an essential biotic component in plant-soil feedback processes that can alter plant fitness, growth, and reproduction. Further, they may exert an influence on plants by forming a microbial association network. Accordingly, pronounced changes in the soil microbial community induced by climate warming is vital when evaluating the future risks on plants posed by global climate change. Although the climate warming issue has gained much attention for its impact upon soil microbial communities, attempts to identify its effects on their network associations through plant growth stages, especially in agroecosystems, remains limited and generally understudied. Here, the effects of elevated temperature in association with wheat plant growth upon soil bacteria, fungi, and arbuscular mycorrhizal (AM) fungi were determined in a field experiment. Our results revealed the alpha diversity of soil bacteria (ACE and Chao values) decreased through plant growth stages, while the relative abundances of bacteria and fungi between seeding time and mature stage were revealed significantly distinct in the PCA analysis. The derived microbial association network showed that warming could enhance the complexity of the network and wheat planting might weaken it. We also found the wheat planting and warming could increase the number of keystone species. Furthermore, the keystone species had the strongest relationship with the grain mass and quality of wheat. These findings could provide a better understanding of plant-soil feedback dynamics in wheat crops, along with those in other similar agroecosystems in the future under global climate change.

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.