Fusarium wilt of banana (Musa spp.) caused by the fungal pathogen Fusarium oxysporum f. sp. cubense (Foc) is a typical soilborne disease, that severely devastates the banana industry worldwide, and soil microbial diversity is closely related to the spread of Fusarium wilt. To understand the relationship between microbial species and Fusarium wilt, it is important to understand the microbial diversity of the Fusarium wilt-diseased and disease-free soils from banana fields.
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Based on sequencing analysis of the bacterial 16S rRNA genes and fungal internal transcribed spacer (ITS) sequences, Foc abundance, fungal or bacterial richness and diversity were higher in the diseased soils than in the disease-free soils. Although Ascomycota and Zygomycota were the most abundant fungi phyla in all soil samples, Ascomycota abundance was significantly reduced in the disease-free soils. Mortierella (36.64%) was predominant in the disease-free soils. Regarding bacterial phyla, Proteobacteria, Acidobacteria, Chloroflexi, Firmicutes, Actinobacteria, Gemmatimonadetes, Bacteroidetes, Nitrospirae, Verrucomicrobia and Planctomycetes were dominant phyla in all soil samples. In particular, Firmicutes contributed 16.20% of the total abundance of disease-free soils. At the bacterial genus level, Bacillus, Lactococcus and Pseudomonas were abundant in disease-free soils with abundances of 8.20, 5.81 and 2.71%, respectively; lower abundances, of 4.12, 2.35 and 1.36%, respectively, were found in diseased soils. The distribution characteristics of fungal and bacterial genera may contribute to the abundance decrease of Foc in the disease-free soils.
Unique distributions of bacteria and fungi were observed in the diseased and disease-free soil samples from banana fields. These specific genera are useful for constructing a healthy microbial community structure of soil.
In the present study, we performed a comparative microbiome analysis of the Fusarium wilt-diseased and Fusarium wilt-suppressive (disease-free) rhizosphere soils. Based on 454-pyrosequencing of the fungal internal transcribed spacer (ITS) region and the bacterial 16S rRNA gene, changes in dominant bacterial and fungal species were investigated in both types of soils. Additionally, correlations between soil chemical properties and microbial distributions were analyzed. Our results offer new insight into identifying fungal and bacterial genera associated with Fusarium wilt disease-free soils and suggest the microbial genera and mechanisms involved in Fusarium wilt suppressiveness.
For the top 15 dominant fungal genera and phyla (Fig. 6c, d), Mortierella, Fusarium, Pseudallescheria, Nectriaceae, Chloridium, Chaetomium, Humicola, Trichoderma, Ascomycota were the dominant fungal genera in all soil samples (Fig. 6c), with relative abundance of more than 1%. Higher proportions of Mortierella, Fusarium, Pseudallescheria, Nectriaceae, Aspergillus and Penicillium were demonstrated. At the phylum level, Ascomycota and Zygomycota were considered to be dominant phyla and showed an obvious difference between the diseased soil samples and the disease-free soil samples (Fig. 6d).
For fungi, Mortierella, Fusarium, Pseudallescheria and Nectriaceae with over 0.1% of relative abundance were enriched in the diseased and disease-free soil samples. An obvious difference was observed in their relative abundance between both types of soils. In contrast, Fusarium, Pseudallescheria and Nectriaceae were enriched in the diseased soils with the abundances of 16.39, 8.71 and 9.00%, respectively, whereas only 8.30, 2.62 and 1.20% were detected in the disease-free soils, respectively. The most abundant genus Mortierella (34.64%) was detected in the disease-free soils, with only 15.44% abundance in the diseased soils. In addition, we found that the relative abundances of Aspergillus and Penicillium were 3.30 and 3.01%, respectively, in the disease-free soil samples, and 0.34 and 0.52%, respectively, in the diseased soil samples (Table 3).
Significant differences between the diseased and disease-free soils were found for 15 bacterial genera, with a relative abundance of more than 0.1%. Compared with the diseased soils, Bacillus, Lactococcus, Pseudomonas, Sphingomonas, Psychrobacter, Oceanobacillus, Brochothrix, Carnobacterium, Flavisolibacter, Streptococcus and Burkholderia were abundant in the disease-free soils. Bacillus, Lactococcus and Pseudomonas exhibited abundances of 8.20, 5.81 and 2.71% in the disease-free soils, respectively, and 4.12, 2.35 and 1.36% in the diseased soils. The abundance of Streptococcus in the diseased and disease-free soils was also significantly different (Table 3).
Redundancy analysis (RDA) was employed to evaluate the soil environmental variables and phylum abundance. Our data showed that the first and second RDA components explained 30.24% of the total fungal phylum variation (Fig. 7a) and 57.32% of the total bacterial phylum variation (Fig. 7b). The diseased and disease-free soil samples were obviously differentiated by the results of fungal and bacterial RDA1 (Fig. 7a and b). For the distribution of microbial species, Fusarium showed negative correlations with pH and AP but positive correlations with TOC and TON. Bacillus had positive correlations with pH and AP but negative correlations with TOC and TON.
By contrast, Mortierella, Fusarium, Pseudallescheria, Nectriaceae, Chloridium, Chaetomium, Humicola, Trichoderma and Ascomycota were the dominant genera in both types of soil samples. Although the soil conditions or plant varieties could cause different distributions of the dominant fungal genera, Fusarium is frequently considered as one of the most dominant genera in some studies [6, 18, 28]. Nonetheless, the dominant genera Trichoderma and Mortierella were enriched in the disease-free soils, whereas Fusarium, Pseudallescheria, Nectriacea, Chaetomium, Humicola, Sordarionmyetes and Gibellulopsis demonstrated a decreasing tendency. Trichoderma has been widely used as a biological control agent against various pathogens [29], and although Mortierella has not been as a biological control agent, some antifungal and antibacterial metabolites proved to be produced by isolates of Mortierella [30,31,32,33]. Considering the only 8.30% of Fusarium abundance in the disease-free soils, we speculated that Trichoderma and Mortierella may be associated with suppression of banana Fusarium wilt disease. However, whether the regulation mechanism is through direct antagonism or resource competition, especially in the case of Mortierella is currently unknown.
Our results indicated that the higher abundance and diversity of bacteria were detected in the diseased soils. However, opposite results showed that a large number of OTUs were observed in the Fusarium wilt disease-free soils [25]. No significant difference of bacterial community distribution and diversity was exhibited in the rhizosphere soil samples of diseased and disease-free apple tree [34]. It may be caused by the field sampling time or soil microorganism changes in the presence of pathogens. Although many studies has shown that increased microbial diversity played an important role in the control of diseases [35,36,37], the relative abundance of several bacterial taxa is a more important indicator of disease suppression than the exclusive presence of specific bacterial taxa [17, 38]. It was supported by that most of abundant phyla such as Proteobacteria, Acidobacteria, Chloroflexi, Firmicutes, Actinobacteria, Gemmatimonadetes, Bacteroidetes, Nitrospirae, Verrucomicrobia and Planctomycete were abundant in both types of soil samples. Proteobacteria and Firmicutes were the most dominant phyla, which were similar to the previous studies on diseases infected by Rhizoctonia solani [38, 39]. It might be related to the different growth rate of bacteria [40, 41]. In addition, the higher abundance of Firmicutes in the disease-free soils supported that the disease incidence was negatively correlated with the richness of Firmicutes [18]. Similarly, the abundances of Acidobacteria and Firmicutes in a wheat rhizosphere were positively correlated with disease suppression [42]. Moreover, the abundances of Bacillus, Lactococcus and Pseudomonas in the disease-free soils were two folds than those in the diseased soils (Table 3). Bacillus and Pseudomonas were proved to be responsible for natural suppression of Fusarium wilt disease [25, 43,44,45,46,47]. Streptococcus was also enriched in disease-free soils probably because of the antagonist relationship between Streptococcus and Fusarium oxysporum [48], suggesting that Streptococcus may participate resistance to Fusarium wilt disease. Actually, the complex phenomenon of disease suppression in soils cannot be simply ascribed to a single bacterial taxon or group, but was governed by microbial consortia [38]. Plants and microbiota established a microenvironment on the roots with a complex interaction. A model of seven-species community evidenced that beneficial microbes inhibited the infection of phytopathogenic fungus Fusarium verticillioides in plant roots [11]. This model system research provides a useful method for future research on the banana-microbe interaction. However, we should fully recognize the effect of beneficial species on Fusarium suppression before assembling model community on banana. Comparisons of bacterial communities from banana Fusarium wilt diseased and diseased-free soils will prove to be essential for constructing disease suppressive soil in the future. 2ff7e9595c
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