Fig. 6 Predicted functional analysis of soil fungi of A. spinulosa
Discussion
Structural and functional characteristics of the fungal community ofA. spinulosa rhizosphere soil
The plant root zone is defined as the area between 0.5 and 4 mm from the root system. It serves as a medium for the exchange of various substances, such as harmful substances or nutrients, between the soil and plant. This channel is also affected by the activities of and substances secreted from the plant root system itself (Wei Li et al. 2022). The closer the microorganisms are to the plant root system, the higher is their abundance, diversity, and dominance in the soil (Lu Han 2022). An analysis of the phylogenetic and differential structure of the fungal community between the A. spinulosa rhizosphere and theA. spinulosa nonrhizosphere soils. A high degree of aggregation was observed in the soil fungal phylogeny of the A. spinulosarhizosphere, with the highest aggregation observed in Ascomycota, Mortierellomycota, and Rozellomycota. This is consistent with the findings of most studies on the microbial community structure of rhizosphere soil (Lai et al. 2023; YinYin et al. 2023). LEfSe identifies communities or species that have a significant differential impact on sample delineation (Zewei Zhang et al. 2022). The fungi of the A. spinulosa rhizosphere soil differed mainly at the genus level, such asCutaneotrichosporon , Chaetopsina , Dendrosporium ,Tubulicium , Shiraia , Perenniporia ,Simplicillium , and Capitofimbria . While investigating the structure of rhizosphere soil microbial communities, a previous study showed that the species contributing more to the differences in the community structure was also concentrated in the bacterial groups at the genus level (Su Liu et al. 2023).
The number and species of indicator taxa were representative and characteristic of the community structure. In the present study, with decreasing taxonomic levels, the number of soil community indicator taxa slightly increased in the A. spinulosa nonrhizosphere compared with that the rhizosphere. This may be due to the significant impact of plant roots on the structure of the soil microbial community. Differences in the rhizosphere secretion type and content altered the activity of soil fungi and their ecological niche, leading to the aggregation of specific indicator taxa and reducing the number of indicator taxa (Boyuan Han et al. 2022). In contrast, the fungal community indicator taxa of the A. spinulosa rhizosphere soil differed markedly at different taxonomic levels. At the phylum level, Chytridiomycota was the indicator taxon in the A. spinulosarhizosphere, whereas Glomeromycota was the indicator taxon in theA. spinulosa nonrhizosphere; Basidiomycota was a common phylum acting as an indicator taxon. This is in general agreement with the results of a previous study (Zeliang Yang et al. 2020). The microbial decomposition of plant residues affects the input of soil organic matter, and fungi belonging to Chytridiomycota contribute to soil carbon content by providing organic matter to the soil and enhancing soil nutrient cycling through plant residue decomposition (Jinxian Liu et al. 2019). Glomeromycota comprises various crucial symbiotic fungi of the plant root system that influence plant water acquisition and soil stability (YouSan Wang and RunJin Liu 2017). However, their abundance is significantly reduced by plant and nutrient additions (Xiansheng Wang et al. 2022). Basidiomycota fungi are prevalent in soil and are the key fungal degraders of complex wood fibers (Yujie Zhou et al. 2021). In this study, at the order level, the obvious fungal community indicator taxa of the A. spinulosa rhizosphere and nonrhizosphere soils were Chantharellales and Orbiliales, respectively. Studies have shown that Cantharellales is closely related to N and P curing rates in fine plant roots (Li et al. 2015). At the family level, the obvious fungal community indicator taxa of theA. spinulosainter-rhizosphere and nonrhizosphere soils were Ceratobasidiaceae and Cordycipitaceae, respectively. Ceratobasidiaceae is the dominant group of mycorrhizal fungi that can easily interact with plant roots to form mycorrhizal associations that affect plant growth (Esposito et al. 2016; Yajuan Fu et al. 2019; Jiayao Li et al. 2021). At the genus level, the obvious fungal community indicator taxa of the A. spinulosarhizosphere and nonrhizosphere soils were Tolypocladium andAgaricus , respectively. Tolypocladium is a basic fungal group that protects plants by inhibiting the pathogenic fungus that causes black pod disease (palm blight) (Wenxia Cui 2017). At the species level, a relatively large number of the unclassified fungal community indicator taxa of the A. spinulosa rhizosphere soil were observed. The obvious fungal community indicator taxa of the A. spinulosa rhizosphere soil were the unclassified species of the generaCiliolarina and Serendipita . The identification of unclassified indicator taxa may be beneficial for elucidating the construction mechanism of the rhizosphere soil fungal community ofA. spinulosa . Regarding habitat indicator species, the A. spinulosa nonrhizosphere and rhizosphere intervals were evident at the family and species levels, respectively. In total, 24 nonrhizosphere and 3 rhizosphere indicator taxa were observed. This indicates that plant habitat influences the soil fungal community structure between plant roots and that this community has a stronger indicator effect.
The functional predictions indicated that saprotrophs were predominant in A. spinulosa roots as well as in the nonrhizosphere soil. An increased proportion of pathotrophs was also observed in the A. spinulosa roots. Among the main functional groups of pathotrophs, theA. spinulosa rhizosphere and nonrhizosphere soils were dominated by animal pathogens. The proportion of pathotrophs among the rhizosphere soil fungi of A. spinulosa increased with an increase in the relative abundance of animal pathogens. Simultaneously, the relative abundance of saprotroph–symbiotroph increased and that of pathotroph–saprotroph decreased in the A. spinulosa rhizosphere. Saprophytic fungi are the main functional group involved in the decomposition of organic matter such as plant residues and animal manure (MaoSen Li et al. 2022). A. spinulosa roots are covered with a thick layer of apomictic material throughout the year, and the high abundance of soil decay fungi is conducive to accelerated material recycling.
Characteristics of the co-occurrence network of soil fungi between theA. spinulosa rhizosphere and nonrhizosphere roots
The key taxa play a linking role in the construction of microbial networks. They also influence the construction of ecological networks in biomes. The key fungal taxa of A. spinulosa differed at different taxonomic levels between the rhizosphere and non-rhizosphere soils. The key fungal taxa of the A. spinulosa rhizosphere soil were Ascomycota and its unclassified groups, whereas those of the nonrhizosphere soil were Chytridiomycota and its unclassified taxa. Ascomycota is positively correlated with total carbon and hemicellulose content and plays a crucial role in plant decomposition (Fuxing Cui et al. 2021). Some fungi belonging to the phylum Chytridiomycota are partial plant parasites. They compete for plant nutrients and produce mobile spores during asexual reproduction. These spores act as a mediator for viral transmission. The endemic key fungal phylum in theA. spinulosa rhizosphere soil was Combomycota, whereas those in the nonrhizosphere soil were Glomeromycota, Trapomycota, and Neospora. Some comb fungi belonging to Combomycota are fungal parasites, with their feeding hyphae invading the tissues of other pathogenic fungi and exerting an antagonistic effect (Huang et al. 2022).
Microbial co-occurrence networks indicate the complex interactions between species in microbial communities (Xun Wang et al. 2022). The positive linkage indicates that the fungi are positively correlated with each other and have similar ecological niches or mutualistic symbiosis. In contrast, the negative linkage indicates that fungi are negatively correlated with each other, and an antagonistic or competitive relationship may exist between them (Hou et al. 2020). When the clustering coefficient is higher and the proportion of negative correlation is lower, a higher extent of synergism and stability of the biome are observed (ZhiQi et al. 2021). The clustering coefficients of the fungal community of the A. spinulosa inter-rhizosphere soil at the levels of order, family, genus, and species were higher than those of the nonrhizosphere soil. In contrast, the negative correlation ratio was lower in the rhizosphere soil than in the nonrhizosphere soil. This indicates that the fungal community of the A. spinulosarhizosphere soil had a higher extent of network synergy and connectivity than that of the nonrhizosphere soil. Positive correlations were observed between the fungal communities of the A. spinulosarhizosphere and nonrhizosphere soils, indicating that the soil fungal community structure is relatively stable. The proportion of negative correlations between the fungal communities of the A. spinulosarhizosphere and nonrhizosphere soils was high at the levels of order and family, respectively. This indicated that the rhizosphere of A. spinulosa plants mainly influences the aggregation of fungal species at the order level. The higher average degree and average clustering coefficient as well as shorter average path length of the fungal community network of the A. spinulosa rhizosphere soil indicated higher connectivity and more complex interactions between species (Yang Y et al. 2019). High network centrality is a crucial indicator for assessing the connectivity of the co-occurrence network (Martín González et al. 2010). The highest network center mesocentricity was observed at the species level for both fungal communities of the A. spinulosarhizosphere and nonrhizosphere soils, but it was higher for the rhizosphere soil (0.23) than for the nonrhizosphere soil (0.12). Species such as Neocosmospora rubicola , Microconidia undetermined,Archaea undetermined, Ascomycota undetermined, andMetarhizium carneum occupy the top five intermediate centralities in the A. spinulosa rhizosphere and may play crucial roles in maintaining the structure and function of the rhizosphere fungal community.
Conclusion
Soil fungal phylogeny was more concentrated in the A. spinulosarhizosphere, with Cutaneotrichosporon being the main differential group. Basidiomycota was a common phylum in the rhizosphere and nonrhizosphere soils. The rhizosphere soil fungi of A. spinulosawere more strongly affected by habitat-indicating effects. The key taxa of the rhizosphere soil fungal community of A. spinulosa were Ascomycota and its unclassified group, with complex symbiotic networks and more intense interspecific competition observed at the order level. The increase in the relative abundance of the animal pathogen was the main factor responsible for the increase in the proportion of pathotrophs among the fungi of the A. spinulosa rhizosphere soil. The ecological specialization of soil fungi was stronger among the plant roots. Investigating the unclassified taxa would be of great significance for further revealing the construction pattern of soil fungal communities among the A. spinulosa roots.