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. 2022 Apr 28:13:792568.
doi: 10.3389/fmicb.2022.792568. eCollection 2022.

Black Truffles Affect Quercus aliena Physiology and Root-Associated nirK- and nirS-Type Denitrifying Bacterial Communities in the Initial Stage of Inoculation

Zongjing Kang  1   2 , Xiaolin Li  2 , Yan Li  1 , Lei Ye  2 , Bo Zhang  2 , Xiaoping Zhang  1   2 , Petri Penttinen  1   3 , Yunfu Gu  1
Affiliations

Black Truffles Affect Quercus aliena Physiology and Root-Associated nirK- and nirS-Type Denitrifying Bacterial Communities in the Initial Stage of Inoculation

Zongjing Kang et al. Front Microbiol. .

Abstract

Truffles (Tuber spp.) are edible ectomycorrhizal fungi with high economic value. Bacteria in ectomycorrhizosphere soils are considered to be associated with the nutrient uptake of truffles and hosts. Whether Tuber spp. inoculation can affect the growth of Quercus aliena, the ectomycorrhizosphere soil, and the rhizosphere nirK and nirS-denitrifier communities at the ectomycorrhizae formation stage is still unclear. Therefore, we inoculated Q. aliena with the black truffles Tuber melanosporum and Tuber indicum, determined the physiological activity and morphological indices of Q. aliena seedlings, analyzed the physicochemical properties of ectomycorrhizosphere soils, and applied DNA sequencing to assess the nirK and nirS- denitrifier community structure in ectomycorrhizosphere soils. Peroxidase activity was higher in the seedlings inoculated with T. melanosporum than in the T. indicum inoculation and uninoculated control treatments. The available phosphorus contents were lower and nitrate contents were higher in those with truffle inoculation, and T. melanosporum treatment differed more from the control than the T. indicum treatment. The richness of the nirK-community was highest in the T. indicum treatment and lowest in the uninoculated treatment. The differences in nirK-community composition across treatments were not statistically significant, but the nirS communities were different. The nirS-type bacteria correlated with three environmental factors (pH, available phosphorus, and nitrate contents), whereas the nirK-type bacteria were only associated with the nitrate contents. Generally, this work revealed that inoculation with Tuber spp. would change a few nutrient contents and richness of nirK-type bacteria and had little effects on growth of Q. aliena seedlings in the initial stage of inoculation. The results of this study may provide in-depth insights into the relationships between Tuber spp. and hosts, which should be taken into account when developing truffle production methods.

Keywords: Quercus aliena; Tuber indicum; Tuber melanosporum; denitrifying bacteria; ectomycorrhizosphere; growth of host plants; soil properties.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Two ectomycorrhizae and roots of Quercus aliena without Tuber species partner, Scale bar = 1 mm. (A,D) Ectomycorrhizae of Q. aliena seedlings with Tuber indicum; (B,E) root of Q. aliena without Tuber partner; (C,F) Ectomycorrhizae of Q. aliena seedling with Tuber melanosporum.
FIGURE 2
FIGURE 2
Structural characteristics of Quercus aliena root tips with or without Tuber partner. (A) Cross section of Tuber indicum ectomycorrhizae, Scale bar = 50 μm; (B) Q. aliena roots without Tuber partner, Scale bar = 40 μm; (C) Tuber melanosporum ectomycorrhizae, Scale bar = 50 μm; (D) longitudinal section of T. indicum ectomycorrhizae Scale bar = 50 μm; (E) Q. aliena roots without Tuber partner, Scale bar = 50 μm; (F) T. melanosporum ectomycorrhizae, Scale bar = 50 μm; (G) mantle cell of T. indicum ectomycorrhizae, Scale bar = 20 μm; (H) cell of root tips without Tuber partner, Scale bar = 50 μm. (I) mantle cell of T. melanosporum ectomycorrhizae, Scale bar = 20 μm.
FIGURE 3
FIGURE 3
Family level taxonomic composition of (A) nirK- and (B) nirS-type denitrifier communities in the rhizosphere soil of Quercus aliena. CK.ali, uninoculated Q. aliena; ind.ali, Q. aliena inoculated with Tuber indicum; and mel.ali, Q. aliena inoculated with Tuber melanosporum.
FIGURE 4
FIGURE 4
Heat-maps of the most abundant (A) nirK- and (B) nirS-type denitrifying bacterial genera in rhizosphere soil of Quercus aliena. CK.ali, uninoculated Q. aliena; ind.ali, Q. aliena inoculated with Tuber indicum; and mel.ali, Q. aliena inoculated with Tuber melanosporum.
FIGURE 5
FIGURE 5
Non-metric multidimensional scaling (NMDS) plots of (A) nirK- and (B) nirS-type denitrifying bacterial communities in rhizosphere soil of Quercus aliena. CK.ali, rhizosphere soil of Q. aliena without Tuber partner; mel.ali, ectomycorrhizosphere soil of Q. aliena with Tuber melanosporum partner; and ind.ali, ectomycorrhizosphere soil of Q. aliena with Tuber indicum partner.
FIGURE 6
FIGURE 6
Redundancy analysis (RDA) between (A) nirK- and (B) nirS-type denitrifying bacterial communities and soil factors in the rhizosphere soil of Quercus aliena. CK.ali, rhizosphere soil of Q. aliena without Tuber partner; mel.ali, ectomycorrhizosphere soil of Q. aliena with Tuber melanosporum partner; and ind.ali, ectomycorrhizosphere soil of Q. aliena with Tuber indicum partner.
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