Evidence for involvement of keystone fungal taxa in organic phosphorus mineralization in subtropical soil and the impact of labile carbon

https://doi.org/10.1016/j.soilbio.2020.107900Get rights and content

Highlights

  • Fungi acted as a key driving organic P (Po) mineralization in acidic soil.

  • Labile carbon promoted Po mineralization.

  • The keystone fugal taxa negatively regulate the growth of Po-mineralizing taxa.

  • Labile carbon activated fungal Po mineralization by limiting the growth of keystone fungal taxa.

Abstract

Soil organic carbon (SOC) derived from manure increase phosphorus (P) availability by increasing the proportion of organic P (Po) in total P. However, what role SOC plays in the process of converting Po to available P (AP) and who modulates Po mineralization are still poorly understood. In this study, we collected three soil samples under long-term filed treatment with different organic (no carbon, straw, and manure) inputs. By comparing bacterial and fungal lecithin-enrichment liquid cultures, we observed that the lecithin-enriched fungal community showed higher capability for Po mineralization. Using high-throughput sequencing of the field and lecithin-enriched microbial communities, we identified Po-mineralizing taxa in the soil. Co-occurrence network analysis revealed that the keystone fungal taxa Geastrum sp. and Chaetomium sp. in the fungal network negatively associated with Po-mineralizing fungal taxa, whereas keystone bacterial taxon was not directly related to Po-mineralizing bacteria. We found labile C limits the growth of keystone fungal taxa and that the addition of lactose enhanced Po mineralization by increasing the abundance of Po-mineralizing fungal taxa. Our results emphasize the importance of soil fungi for Po mineralization in acidic soil from a community perspective and provide evidence that easily degradable C drives Po mineralization and influences P availability through limitation of keystone fungal taxa. Our study gives insight into the biological mechanisms underlying specific organic carbon-induced interactions between fungal taxa and provides crucial information for the facilitation of P cycling.

Introduction

Soil available phosphorus (AP) is the limiting factor controlling crop growth in acidic soils because of strong phosphorus (P) adsorption on minerals and precipitation by metal ions (Vance et al., 2003; Elser et al., 2007). Organic P (Po) accounts for 30–80% of the total P pool, and could become bioavailable for plants after mineralization by microorganisms. According to a conceptual model proposed by McGill and Cole (1981), soil Po mineralization is driven by P stress and not inhibit by the mineralization of organic matter. This has been partly supported by field experiments, where the activities of Po-transforming enzymes decreased with P fertilization (Clarholm, 1993; Colvan et al., 2001). However, an increasing number of studies have argued that Po mineralization is linked to the microbial need for carbon (C) (Romanya et al., 2017). A possible explanation is that some enzymes involved in Po mineralization are not related to P status but dependant on microbial biomass (Nannipieri et al., 2011, 2012). Bacteria and fungi comprise more than 90% of the soil microbial biomass. Their growth is commonly limited by C availability and they preferentially hydrolyse organic molecules with low C:P ratio for energy and C requirement, releasing Pi as a by-product (Spohn et al., 2013; Colman et al., 2005; Wang et al., 2016). However, less is known about how soil C:P stoichiometry drive microbial Po mineralization.

Soil microbes mineralize Po through the release of extracellular enzymes (Eivazi and Tabatabai, 1977). Numerous studies have evaluated the effect of different nutrient inputs on bacterial Po mineralization by detecting genes coding for alkaline phosphatase (phoD) (Ragot et al., 2015; Wei et al., 2019; Dai et al., 2020). Luo et al. (2019) reported the importance of manure amendment to phoD-harboring bacterial abundance and activity. Unlike bacteria that prefer using simple compounds, some fungal taxa preferentially utilize more complex carbon substrates in soil (Rinnan and Bååth, 2009), which requires a higher energy investment. Whether different carbon sources drive differences in fungal mineralization remains to be uncovered. In addition, due to the different pH ranges for optimal growth, compared with bacteria, soil fungal growth and activity would be expected to dominant in acidic soils (Rousk et al., 2010). Although, a range of soil fungi have been screened and selected for their efficient Po mineralizing capacity (Jayachandran et al., 1992), whether, and how much, the fungal community contributes to Po mineralization in acidic soil is still unknown.

To explore the associations between SOC and Po mineralization and evaluate the contribution of bacteria and fungi in Po mineralization in acidic soil, we collected soil samples from a long-term (>28 years) fertilization experiment that had received mineral (NPK), mineral plus manure (NPKM) and mineral plus straw (NPKS) application to acidic soil (Chen et al., 2018). Lecithin, the first Po detected in soil and widely used to isolate soil Po-mineralizing species (Rogers et al., 1941; Feng et al., 2003; Li et al., 2019b), was used as the unique P source to enrich Po-mineralizing bacterial and fungal communities. Using high-throughput sequencing of soil and lecithin enriched microbial communities, Po-mineralizing bacterial and fungal taxa were identified from soil microbial taxa. We hypothesized that (1) C-derived from manure or straw could stimulate Po mobilization and enhance P availability; (2) the soil fungal community contributes more to Po mineralization in acidic soil than bacteria; and (3) different forms of organic C may control Po mineralization by modulating fungal composition.

Section snippets

Field experimental design and soil sampling

The field site is located at the Yingtan Red Soil Ecological Experimental Station of the Chinese Academy of Sciences in Jiangxi Province in subtropical China (28°12′N, 116°55′E) (Chen et al., 2018). The soil is a typical acidic loamy clay that is derived from Quaternary Red Clay and classified as a Ferralic Cambisol (WRB, 2006). The site has a subtropical, humid monsoon climate with an annual average temperature of 17.6 °C and annual precipitation of 1795 mm. The field experiment was initiated

Effects of field treatments on P availability and stoichiomestry

Even under long-term equivalent TN and TP inputs, NPK and NPKS had similar level of P pool, in both content and form, while NPKM contained larger P pool with significantly higher Po, Pi, and AP than NPK or NPKS (P < 0.05, Fig. 1). Po, which had the same concentration as Pi in NPK and NPKS, was significant higher than Pi in NPKM (P < 0.05).

In addition to the variation in P pool, soil pH, SOC, TN and AN were elevated in NPKM (P < 0.05), whereas NPKS contained higher TN (P < 0.05, Table 1). The

Discussion

Although many studies have emphasized that a lower C:P ratio enhances microbial Po mineralization, the underlying microbial ecological mechanism is still ambiguous (Spohn et al., 2013; Wang et al., 2016; Luo et al., 2019). Using the novel approach of constructing microbial association networks opens the way to predict the complex interactions and functional community alterations (Carr et al., 2019; Chen et al., 2020). Further validation of these interactions or alterations with additional

Conclusions

Under the premise of equal nitrogen and phosphorus input, manure effectively reduced the C:P ratio and increased P availability by enlarging Po pool. Soil fungi were important contributors to Po mineralization in acidic soil. Compared with straw, the labile carbon in manure promoted fungal Po mineralization by inhibiting the growth of fungal keystones that limit Po-mineralizing species growth. These findings add new context to the current concepts about low C:P ratio facilitates microbial Po

Declaration of competing interest

The authors declare no conflicts of interest.

Acknowledgements

We thank Jianbo Fan and Renfeng Tu for their work in the field experiment. This study was financially supported by the National Key R&D Program [grant number 2016YFD0200309], the National Natural Science Foundation of China [grant number 41977098, 41922048 and 41807050], and the Natural Science Foundation of Jiangsu Province [grant number BK20191510].

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    Yan Chen and Ruibo Sun contributed equally to this work.

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