Effects of plant encroachment on multifunctionality in bauxite residue
Bauxite residue commonly exhibit high salinity and alkalinity, which largely limits plant growth and ecological restoration. In this study, the long-term plant encroachment decreased the alkalinity and salinity in bauxite residue, whereas increase nutrient conditions, microbial biomass, and microbial functions in bauxite residue. On one hand, plant growth improved residue properties by several direct pathways including physiological metabolism and root activities. Plant growth could promote the dissolution of alkaline minerals and its leaching in bauxite residue by secreting organic acid, thus decreasing alkalinity in bauxite residue (Kong et al., 2017; Kong et al., 2018). Plant growth also could increase the storage of organic carbon by plant residues and rhizo-deposits, (Zhu et al., 2023). In addition, the plant growth could protect the organic carbon from rapid decomposing by promoting the aggregates formation, thus indirectly increased organic carbon content (Zhu et al., 2018; Zhu et al., 2016). On the other hand, the improved residue properties by plant growth could promote the development of microbial communities, including increase microbial biomass and functions (Wu et al., 2020; Wu et al., 2021). The developed microbial communities also could improve residue properties through microbial activities such as neutralize alkalinity by organic acids secretion, promote aggregates formation by extracellular polymeric substances (EPS) secretion, and increase carbon accumulation by microbial necromass (Xue et al., 2023).
Effects of plant encroachment on microbial diversity and stability in bauxite residue
The high alkalinity and salinity, as well as limited nutrients restricted the development of microbial communities in bauxite residue. In this study, plant encroachment increased microbial diversity and richness in bauxite residue. The microbial community may be promoted by the alleviated environmental pressures and increased environmental resources following plant encroachment in bauxite residue. One on hand, the increased organic carbon and available nitrogen and phosphorus provide more substrate for microbial activities, thus accelerated the metabolism and enhanced development of microbial communities (Banerjee et al., 2020). On the other hand, the decreased alkalinity and salinity alleviated environmental pressures posed on microbial communities and promote the development of microbial communities in bauxite residue (Hernandez et al., 2021).
As we all known, soil microbial communities play a critical role in maintaining ecosystem multifunctionality by supporting biochemical processes including litter decomposition and organic matter mineralization (van der Heijden et al., 2008), which linked the transformation of matter and energy between above- and belowground communities (Wardle et al., 2004). Soil microbes can regulate soil functions by improve soil structure and hydraulic properties in degraded lands (Coban et al., 2022). In addition, soil microbes also could regulate EMF resistance by changing microbial composition (Delgado-Baquerizo et al., 2017). Our findings found that EMF increased with increasing soil microbial diversity, which was likely due to the functional complementary effect of soil microbes (Wagg et al., 2019). For example, the degradation of straw from complex and recalcitrant polymers into simpler and more labile monomers, required the cooperation of a large and diverse group of microorganisms, including Cellulose degrading bacteria and lignin-degrading bacteria. In addition, there are a variety of microbial groups indirectly involved in straw degradation, which acts as an electron transfer "bridge", are beneficial to release excess reducing force accumulated during degradation, relieve substrate restriction generated during straw degradation, and promote straw degradation (Bao et al., 2019). Nitrogen-fixing microorganisms can provide nitrogen and alleviate the obstacle of straw degradation due to high C/N (Bao et al., 2019).
Microbial community stability, which was a novel indicator to describe the degree of variation or turnover of microbial communities, plays a critical role in sustaining functions and services rendered by soil ecosystems (Xun et al., 2021). Network analysis is a promising data analysis method to provide comprehensive insights into microbial community dynamics and help identify co-occurrence patterns at phylogenetic levels (Barberan et al., 2012). Higher modularity and greater abundances of negative correlations have been implicated in the increased stability of microbial community networks. In this study, the microbial community in vegetated sites (BA, BC, and BH) exhibited higher modularity and greater correlations than that in unvegetated sites (CK), indicating that the plant encroachment increased microbial stability in bauxite residue. The increased network stability may be related to the decreased alkalinity and salinity, as well as the enhanced resource supplement (e.g., increased availability of water, soil carbon and nutrients) (Guo et al., 2020). In addition, most soil microbes are sensitive to the changes in temperature. The increased soil organic matter content and decreased bulk density induced by plant encroachment in bauxite residue can cause an decrease in soil thermal conductivity and an increase in soil heat capacity, which benefit to the stabilization of microbial community (Guo et al., 2018).
Soil microbial network complexity also played a vital role in maintaining EMF and multiple ecosystem functions. Our findings revealed that EMF were positively associated with increasing network complexity of microbial communities in bauxite residue. These results coincided with previous studies that higher microbial network complexity commonly supported higher ecosystem functions (Qiu et al., 2021; Wagg et al., 2019). The microbially-driven ecological processes are commonly comprised of several associated metabolic pathways, which conducted by a myriad of interactions among taxa. More tightly connected microbial members could utilize resource more efficiency, and regulate the metabolic of ecological processes (Morriën et al., 2017).
Effects of plant encroachment on microbial communities in bauxite residue
Plant encroachment significantly decreased the relative abundance of Firmicutes, Euryarchaeota, Cyanobacteria, and Bacteroidetes in bauxite residue whereas increased the relative abundance of Proteobacteria, Actinobacteria, Acidobacteria, Chloroflex, and Planctomycetes in bauxite residue (Fig. 3). Firmicutes and Actinobacteria were adaptive to saline-alkali environments including saline soils, soda lakes and alkaline mine tailings, due to the mechanisms such as generating stress resistant endospores and self-repairing DNA (Filippidou et al., 2015). In addition, members of Actinobacteria are sensitive to soil water conditions and negatively correlated with soil moisture (Naylor et al., 2017). In our study, plant encroachment significantly increased soil moisture in bauxite residue, which might decrease the abundance of Actinobacteria. The Proteobacteria was the most abundant phylum in most of the soil samples collected in this study. Many Proteobacteria are considered to have relatively fast growth rate and capability to use various substrates, which could fast respond to the improved environmental conditions (Spain et al., 2009). Bacteroidetes were commonly contributed to the decomposition of macromolecules such as starch, cellulose, fiber, and chitin. The plant growth induced fallen leaves and death root may contribute to the enrichment of Bacteroidetes in bauxite residue (Deng et al., 2020). Acidobacteria are considered to be oligotrophs and are also restricted by soil moisture, having negative correlations with most soil nutrients but a positive correlation with soil moisture (Kielak et al., 2009). However, the abundance of Acidobacteria showed significantly positive relationships with soil nutrients in this study. This may related to the decreased pH in vegetated site, as the abundance of Acidobacteria in soils is correlated with soil pH (Lauber et al., 2009). The positive effects of decreasing pH in influencing the abundance of Acidobacteria likely offset the negative effects of increasing soil nutrients.
Bacillaceae and Geodermatophilaceae are spore-forming species and capable to grow in nutrient-poor biotopes such as dry soils or mineral rock (del Carmen Montero-Calasanz et al., 2013; Montero-Calasanz et al., 2012). They have been reported to resist oxidative stress, heavy metals, exposure to high gamma ionizing radiation, UV light, as well as desiccation, and were shown to survive in the atmosphere (del Carmen Montero-Calasanz et al., 2013; Montero-Calasanz et al., 2012). Our data show that plant encroachment increased the relative abundances of Acidobacteriaceae, Beijerinckiaceae, Blastocatellaceae, Frankiaceae, Nitrosomonadaceae, Rhizobiaceae, and Sphingomonadaceae. This response pattern is likely due to the dependency of these taxa on higher levels of soil moisture and nutrients as shown in Fig. S7. Moreover, we found a significant increase in the presence of the N fixing bacteria, Beijerinckiaceae and Rhizobiaceae in vegetated sites. Plant root exudates promote the development of N fixing bacteria mainly due to the presence of microbial-available carbon sources, which increase the number of microorganisms in the rhizosphere (Li et al., 2021). In addition, the increased C/N may contribute to the development of N fixing bacteria. Zheng (Zheng et al., 2023) found that the process of microbial nitrogen fixation was mainly driven by higher carbon to nitrogen ratio, not merely nitrogen content. Further research is needed to confirm this supposition, including the comparison of N2 fixation rates between vegetated and unvegetated sites in bauxite residue deposit areas. Overall, these results suggest that the shift in composition of bacteria was closely related with the response of bauxite residue properties following plant encroachment.
Implications
Our findings have important implications for understanding the impact of plant encroachment on the structure and function of microbial communities in bauxite residue and how plant encroachment is associated with specific soil microbiota. Plant encroachment induced increases in diversity and complexity of soil microbial communities in bauxite residue. Importantly, soil microorganisms have essential supports on soil multifunctionality in diverse ecosystems by enhancing decomposition and nutrient cycling as well as resources availability (Delgado-Baquerizo et al., 2016; Delgado-Baquerizo et al., 2020). The plant encroachment-induced strong association within bacterial communities and networks and the improvement in bauxite residue quality emphasized the importance of soil communities in supporting multifunctionality in the soil formation process of bauxite residue. Moreover, since diverse and complex microbial communities are more resilient to environmental stresses than simple ones (Allison and Martiny, 2008), the increase of microbial diversity and complexity induced by plant encroachment may have long-term positive effects on ecology functions in bauxite residue. Therefore, the increase of microbial diversity and complexity in bauxite residue can contribute to soil multifunctionality, which accelerate soil formation process and strengthen ecosystem services that the soil provides. The improvement of both aspects should be considered when rehabilitating degraded soils. Future research is needed to examine how the microbial communities and functions recovered in response to ecological restoration promotion practices.
Network complexity and network topology as well as keystone taxa are assessed using statistical tools and are based on correlations (Banerjee et al., 2016; Berry and Widder, 2014; Ma et al., 2016). Such correlations do not necessarily show cause-effect relationships, but displayed potential interaction within microbial communities. Although network complexity and keystone taxa play important role in microbial communities (Fuhrman, 2009) and were significantly correlated with MF (Figs. 3 and 4), the present study did not directly examine such a role. Therefore, how the keystone taxa regulate the relationship between bacterial communities and plant encroachment should be explicitly examined.